darwinian natural selection - information for educators |...

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Survival of the fattest.The photoshows a pack of African wild

dogs bringing down an impala.Data gathered by Alistair Pole

and colleagues (2003) show thatwild dogs prey on the skinniest,

weakest impala.The graphshows, for different times of year,

the mean amount of stored fatin the bone marrow of impala

taken by wild dogs versus arandom sample of impala.

3Darwinian Natural Selection

It is quite conceiveable,” Darwin wrote in his introduction to On the Originof Species (1859, p. 3) “that a naturalist, reflecting on the mutual affinities of

organic beings, on their embryological relations, their geographical distribution,geological succession, and other such facts, might come to the conclusion thateach species had not been independently created, but had descended fromother species.”

This assertion concerns the pattern of life’s history. A growing body of evi-dence, amassed by Darwin and the early evolutionists who were his intellectualforebears, indicated that both fossilized and living organisms were derived withmodification from either a single common ancestor or a few.The evidence wasindirect and the interpretation startling, but Darwin’s argument was so com-pelling that scientific debate over descent with modification virtually ended bythe mid-1870s. Evolution was, and is, an established fact.

“Nevertheless,” he continued,“such a conclusion, even if well founded, wouldbe unsatisfactory, until it could be shown how the innumerable species inhabit-ing this world have been modified. ”

Darwin knew as well as anyone that the mere recognition of a pattern doesnot amount to a complete scientific theory. If we are to claim any understandingof life’s history, we must explain not only what happened, but how.What is themechanism that produces the pattern we call evolution? Chapter 2 focused onthe evidence for descent with modification; this chapter introduces the process,natural selection, that Darwin asserted produces the pattern.

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74 Part I Introduction

3.1 Artificial Selection: Domestic Animals and PlantsTo understand the mechanism of evolution in nature, Darwin studied the mech-anism of evolution under domestication.That is, he studied the method plant andanimal breeders use to modify their crops and livestock. Darwin’s favorite do-mestic organism was the pigeon. Darwin became a pigeon breeder himself tolearn the experts’ techniques.To refine a particular breed of pigeon so that, forexample, the birds’ tail feathers fan more spectacularly, or their body feathers curlmore elegantly, breeders employ artificial selection.They scrutinize their flocksand select the individuals with the most desirable traits.These birds the breedersmate with each other to produce the next generation. If the desirable traits arepassed from parents to offspring, then the next generation, consisting of the prog-eny of only the selected birds, will show the desirable traits in a higher propor-tion than existed in last year’s flock.

Our favorite domestic organism is the tomato.The domestic tomato, Solanumlycopersicum, occurs around the world, both in cultivation and as a weedy escapee.It is closely related to, and can interbreed with, several species of wild tomatoes,all found in western South America (Spooner et al. 2005).The domestic tomatowas first cultivated by Native Americans before Europeans arrived in the NewWorld (Tanksley 2004). It traveled back to Europe with the early explorers andspread around the globe from there (Albala 2002).

The power of artificial selection is evident in Figure 3.1. All species of wildtomato have small fruit like the currant tomato on the left, typically less than acentimeter across and weighing just a few grams (Frary et al. 2000).The ancestorof the domestic tomato probably had similarly tiny fruit. Modern varieties of do-mestic tomato, like the Red Giant on the right, have fruit 15 cm or more acrossthat can weigh more than a kilogram. Descent with modification, indeed.

To increase the frequency ofdesirable traits in their

stocks, plant and animalbreeders employ artificial

selection.

Wild tomato(Solanum pimpinellifolium)

Domestic tomato(Solanum lycopersicum)

Figure 3.1 Wild and domestictomatoes Wild tomatoes havetiny fruit, like that of the curranttomato on the left. Domestictomatoes are descended fromtiny-fruited ancestors, but as a re-sult of artificial selection havelarge fruit, like that of the RedGiant on the right. From Frary etal. (2000).

Research by molecular biologists allows us to understand at least part of whathappened during the domestication of tomatoes at the level of individual genes.Tomatoes carry, on chromosome 2, a gene called fw2.2 (Tanksley 2004). Thegene encodes a protein made during early fruit development (Frary et al. 2000).The protein’s job is to repress cell division; the more of the protein a plant makes,the smaller its fruit (Liu et al. 2003). Changes in the nucleotide sequence in thefw2.2 promoter—the gene’s on-off switch—alter the timing of production andthe total amount of protein made (Cong et al. 2002; Nesbitt and Tanksley 2002).

Every wild tomato ever tested has carried alleles of fw2.2 associated with highproduction of the repressor protein and small fruit (Tanksley 2004). Every culti-vated tomato has carried alleles associated with low production of the proteinand large fruit. Anne Frary and collegues (2000), working in the laboratory ofSteven Tanksley, used genetic engineering to place copies of a small-fruit allele

Chapter 3 Darwinian Natural Selection 75

Tanksley enivisions a scenario in which early tomato farmers noticed varia-tion in fruit size among their plants (Nesbitt and Tanksley 2002;Tanksley 2004).Some of this variation was due to the plants’ possession of different alleles of thefw2.2 gene. Large fruit alleles might have been present as rare variants prior todomestication, or they might have arisen as new mutations in cultivated popula-tions. Because the farmers preferred larger tomatoes, year after year they plantedtheir fields with seeds from the largest fruit of the previous crop. By this disci-pline the farmers eventually eliminated small-fruited alleles from their stocks.

Farmers practicing artificial selection can change more than size.The domes-ticated vegetables shown in Figure 3.3—broccoli, brussels sprouts, cauliflower,kale, and kohlrabi—are strikingly different in achitecture.Yet all can readily inter-breed, and are classified by botanists as varieties of wild cabbage, Brassica oleracea,from which they are derived.

Broccoli(flower cluster)

Cabbage (condensed shoot)

Brussell sprouts (lateral buds)

Kohllrabi(swollen stems and leaf bases)

Wild cabbage

Genetically unmanipulated domestic tomato

Domestic tomato of the same variety with wild allele of fw2.2 added

into domestic tomatoes.The fruit on the left in Figure 3.2 is from an unmanip-ulated plant; the fruit on the right is from a sibling of the unmanipulated plantthat has been genetically modified to carry the wild, small-fruit allele of fw2.2.The fruits differ in size by about 30%.

Figure 3.2 A genetically de-termined difference in fruit sizeThese tomatoes are from siblingplants.The one on the left carriesonly domestic alleles of the fw2.2gene.The one on the right car-ries, in addition, copies of the wildallele.The fw2.2 gene encodes aprotein that represses fruitgrowth. From Frary et al. (2000).

Figure 3.3 Wild and domesticvarieties of Brassica oleraceaCauliflower (Brassica oleraceabotrytis), broccoli (Brassica oler-acea italica), brussels sprouts(Brassica oleracea gemmifera), kale(Brassica oleracea acephala), andkohlrabi (Brassica oleracea gongy-lodes) are all derived from wildcabbage (Brassica oleracea oler-acea). After Niklaus (1997).


3.2 Evolution by Natural SelectionDarwin realized that a process much like artificial selection happens in nature.His Theory of Evolution by Natural Selection holds that descent with modifica-tion is the logical outcome of four postulates, which he laid out in his introduc-tion to On the Origin of Species by Means of Natural Selection. Darwin (1859, p. 459)considered the rest of the book one long argument in their support. Darwin’spostulates, claims about the nature of populations, are as follows:

1. Individuals within populations are variable.2. The variations among individuals are, at least in part, passed from parents

to offspring.3. In every generation, some individuals are more successful at surviving and re-

producing than others.4. The survival and reproduction of individuals are not random; instead they are

tied to the variation among individuals.The individuals with the most favor-able variations, those who are better at surviving and reproducing, are natural-ly selected.

If these four postulates are true, then the composition of the populationchanges from one generation to the next. Figure 3.4 shows how Darwin’s the-ory might play out in a population of chilies eaten by packrats.

Mild Hot

(1) There is variation among individuals.

X X

(4) Some variants survive and reproduceat higher rates than others.

Outcome: The composition of the population changes from one generation to the next.

(2) The variation is inherited.

(3) More individuals are born than will survive to reproduce.

Figure 3.4 Darwin’s Theoryof Evolution by Natural Selec-tion Darwin’s theory consists offour claims about populations oforganisms and a logical outcomethat follows, as a matter of simplemathematics, if the four postu-lates are true.These cartoonsshow how the theory might workin a population of chili plantswhose fruits are attacked bypackrats. If the chilies vary in thespiciness of their fruit, and if pack-rats prefer milder chilies, and ifthe hot survivors pass their spice-ness to their offspring, then thepopulation will show a higherproportion of hot-fruited chilieseach generation. Inspired byTewksbury and Nabhan (2001).

Darwin and Wallace realizedthat a process similar to

artificial selection happensautomatically in nature.


The logic is straightforward: If there are differences among the individualsin a population that can be passed on to offspring, and if there is differentialsuccess among those individuals in surviving and/or reproducing, then sometraits will be passed on more frequently than others.As a result, the character-istics of the population will change slightly with each succeeding generation.This is Darwinian evolution: gradual change in populations over time.

Note that while the logic is straightforward it contains a subtlety that cancause confusion. To understand how natural selection works, we have to thinkstatistically. The selection itself—the surviving and reproducing—happens toindividuals, but what changes is populations. Recall the HIV virions discussedin Chapter 1. Because of differences in the amino acid sequences of the reversetranscriptase active site, individual virions within the same host varied in theirability to synthesize DNA in the presence of AZT.Virions with mutant forms ofreverse transcriptase that were less likely to bind AZT reproduced more success-fully.When they reproduced, they passed their reverse transcriptase mutations totheir offspring. In the next generation, then, a higher percentage of virions car-ried the modified form of reverse transcriptase than in the generation before.This change in the population is evolution by natural selection.

Darwin referred to the individuals who are better at surviving and reproduc-ing, and whose offspring make up a greater percentage of the population in thenext generation, as more fit. In so doing he gave the everyday English words fitand fitness a new meaning. Darwinian fitness is the ability of an individual tosurvive and reproduce in its environment.

An important aspect of fitness is its relative nature. Fitness refers to how wellan individual survives and how many offspring it produces compared to other in-dividuals of its species. Biologists use the word adaptation to refer to a trait orcharacteristic of an organism, like a modified form of reverse transcriptase, thatincreases its fitness relative to individuals without the trait.

Darwin’s mechanism of evolution was, incidentally, discovered independentlyby a colleague of Darwin’s named Alfred Russel Wallace.Though trained in Eng-land, Wallace had been making his living in Malaysia by selling natural historyspecimens to private collectors.While recuperating from a bout with malaria in1858, he wrote a manuscript explaining natural selection and sent it to Darwin.Darwin, who had written his first draft on the subject in 1842 but never pub-lished it, immediately realized that he and Wallace had formulated the same the-ory. Brief papers by Darwin and by Wallace were read together before theLinnean Society of London, and Darwin then rushed On the Origin of Species intopublication (17 years after he had written the first draft).Today, Darwin’s name ismore prominently associated with the Theory of Evolution by Natural Selectionfor two reasons: He had clearly thought of it before Wallace, and his book pro-vided a full exposition of the idea, along with massive documentation.

One of the most attractive aspects of the Darwin–Wallace theory is thateach of the four postulates and their logical consequence can be verified independently.That is, the theory is testable.There are neither hidden assump-tions nor anything that has to be accepted uncritically. In the next two sec-tions, we examine each of the four assertions, and Darwin’s predicted result, byreviewing two studies: a recent experiment on snapdragons and an ongoingstudy of finches in the Galápagos Islands off the coast of Ecuador.These stud-ies show that the Theory of Evolution by Natural Selection be tested rigor-ously, by direct observation.

Natural selection is a processthat produces descent withmodification, or evolution.

An adaptation is acharacteristic that increasesthe fitness of an individualcompared to individualswithout the trait.

The Theory of Evolution byNatural Selection is testable.


3.3 The Evolution of Flower Color in an ExperimentalSnapdragon Population

Kristina Niovi Jones and Jennifer Reithel (2001) wanted to know whether nat-ural selection by bumblebees could influence the evolution of a floral trait con-trolled by alleles of a single gene.To find out, they established an experimentalpopulation of 48 snapdragons in which they made sure that Darwin’s postulates1 and 2 were true. Then they monitored the plants and their offspring to seewhether postulates 3 and 4, and the predicted outcome, were true as well.

Postulate 1:There Is Variation among IndividualsThe snapdragons in Jones and Reithel’s population varied in flower color.Three-quarters of the plants had flowers that were almost pure white, with just twospots of yellow on the lower lip.The rest had flowers that were yellow all over.

Postulate 2: Some of the Variation Is HeritableThe variation in color among Jones and Reithel’s plants was due to differencesin the plants’ genotypes for a single gene.The gene has two alleles, which wewill call S and s. Individuals with either genotype SS or Ss have white flowerswith just two spots of yellow. Individuals with genotype ss are yellow all over.Among the 48 plants in the experimental population, 12 were SS, 24 were Ss,and 12 were ss. Figure 3.5a shows the variation in phenotype among Jones andReithel’s snapdragons, and the variation in genotype responsible for it.

Testing Postulate 3: Do Individuals Vary in Their Success at Surviving or Reproducing?Although Jones and Reithel ran their experiment in a meadow in Colorado, theykept their snapdragons in pots and made sure all of the plants survived.

The researchers did not intervene, however, to help the snapdragons repro-duce. Instead, they let free-living bumblebees pollinate the plants.To gauge theplants’ success at reproducing by exporting pollen, Jones and Reithel tracked thenumber of times bees visited each flower.To gauge the plants’ success at repro-ducing by making seeds, the researchers counted the seeds produced from eachfruit. Consistent with Darwin’s third postulate, the plants showed considerablevariation in reproductive success, both as pollen donors and as seed mothers.

Testing Postulate 4: Is Reproduction Nonrandom?Jones and Reithel expected that one color would attract more bees than theother, but they did not know which color it would be.The yellow spots on oth-erwise white snapdragons are thought to serve as nectar guides, helping bumble-bees find the reward the flower offers.All-yellow flowers lack nectar guides andso might be less attractive to bees, or they might be more visible against the back-ground vegetation and thus more attractive. Jones and Reithel found that whiteflowers attracted twice as many bee visits as yellow flowers (Figure 3.5b, left).

Reproductive success through seed production was less strongly associatedwith color than was success through pollen donation. Nonetheless, the whiteplants were somewhat more robust than the yellow plants and so produced, onaverage, slightly more seeds per fruit (Figure 3.5b, right).

When researchers set up aplant population in which

postulates 1 and 2 were true,they found that postulate 3

was true as well Á

as were postulate 4 ÁÁ


SS Ss ss

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(a) Composition of parental population

Figure 3.5 Darwin’s Theoryof Evolution by Natural Selec-tion demonstrated in an exper-imental population ofsnapdragons (a) The plants inthe parental population vary inflower color.This variation inphenotype is due to variation ingenotype.The graph shows thenumber of plants in the popula-tion with each of the three pos-sible genotypes. (b) The whiteplants are more successful at re-producing.They are visited bybumblebees twice as often (left),and make more seeds (right). (c)Because plants with white flow-ers are more successful at pass-ing on their genes, they occupy alarger fraction of the populationin the next generation. Preparedfrom data in Jones and Reithel2001. [In (b) left, the verticalbars show the size of the stan-dard error ; they indicate the ac-curacy of the researchers’estimate of the mean number ofbee visits. In (b) right, the valuesfor relative seed set were calcu-lated as the fraction of seeds ac-tually produced by plants with aparticular genotype divided bythe fraction of seeds expectedbased on the frequencies of thegenotypes.]

Consistent with Darwin’s fourth postulate, reproductive success was not ran-dom.Through both pollen donation and seed production, white plants had high-er reproductive success than yellow plants.

Testing Darwin’s Prediction: Did the Population Evolve?The bumblebees that volunteered to participate in Jones and Reithel’s experi-ment played the same role that Darwin did in breeding pigeons:They selectedparticular individuals and granted them high reproductive success. Since whiteplants had higher reproductive success than yellow, and since flower color is de-termined by genes, the next generation of snapdragons should have had a higherproportion of white flowers.

Indeed, the next generation did have a higher proportion of white flowers(Figure 3.5c).Among the plants in the starting population, 75% had white flow-ers; among their offspring, 77% had white flowers.The snapdragon populationevolved as predicted. An increase of two percentage points in the proportion ofwhite flowers might not seem like much. But modest changes can accumulateover many generations.With Jones and Reithel’s population evolving at this rate,it would not take many years for white flowers to all but take over.

and Darwin's predictionthat the population wouldevolve as a result.

Á


Jones and Reithel’s experiment shows that Darwin’s theory works, at least inexperimental populations when researchers have made certain that Darwin’s firsttwo postulates hold. But does the theory work in completely natural popula-tions, in which researchers have manipulated nothing? To find out, we turn to re-search on Darwin’s finches in the Galápagos Islands.

3.4 The Evolution of Beak Shape in Galápagos FinchesPeter Grant and Rosemary Grant and their colleagues have been studying finch-es in the Galápagos Archipelago since 1973 (see P. R. Grant 1999; B. R. Grantand P. R. Grant 1989, 2003; P. R. Grant and B. R. Grant 2002a, 2002b, 2005.2006; B. R. Grant 2003). Collectively called Darwin’s finches, the birds are de-rived from a small flock of grassquits that invaded the archipelago from Centralor South America some 2.3 million years ago (Sato et al. 2001).The descendentsof this flock today comprise 13 species that live in the Galápagos, plus a 14th thatlives on Cocos Island. Close examination of the evolutionary tree in Figure 3.6reveals that all of these species are closely related.The deepest split on the treeseparates two lineages of warbler finches that still recognize each other as poten-tial mates and are thus classified (despite each having its own name) as belonging

Geospizadifficilis

Sharp-beaked ground finch

Ground finches

Geospizafuliginosa

Geospizafortis

Geospizamagnirostris

Geospizascandens

Geospizaconirostris

Geospizadifficilis

Small ground finch

Medium ground finch

Large ground finch

Cactus ground finch

Large cactus ground finch


Tree finches

Camarhynchusparvulus

Camarhynchuspsittacula

Camarhynchuspauper

Cactospizapallida

Small insectivorous tree finch

Large insectivorous tree finch

Large insectivorous tree finchon Isla Floreana

Woodpecker finch

Pinarolaxesinornata

Cocos finch

Platyspizacrassirostris

Vegetarian tree finch

fusca

Gray warbler finch

Certhideaolivacea

(Branch lengths are arbitrary)

Warbler finches

Cactospizaheliobates

Mangrove finch

Olive warbler finch

Certhidea

Figure 3.6 Diversity in Darwin’s finches These finches are all descended from a common ancestral population (red arrow) thattraveled from Central or South America to the Galápagos Archipelago.The evolutionary tree, estimated from similarities and differencesin DNA sequences by Kenneth Petren and colleagues (2005), shows the sometimes complex relationships among the major groups. Thephotos, from Petren et al. (1999) and Grant and Grant (1997), show the extensive variation among species in beak size and shape.


to a single species.The next deepest split separates two lineages of sharp-beakedground finches that are likewise considered a single species. Consistent with theirclose kinship, all species of Darwin’s finches are similar in size and coloration.They range from 4 to 6 inches in length and from brown to black in color.Theydo, however, show remarkable variation the size and shape of their beaks.

The beak is the primary tool used by birds in feeding, and the enormousrange of beak morphologies among the Galápagos finches reflects the diversity offoods they eat.The warbler finches (Certhidea olivacea and Certhidea fusca) feed oninsects, spiders, and nectar; woodpecker and mangrove finches (C. pallida andC. heliobates) use twigs or cactus spines as tools to pry insect larvae or termitesfrom dead wood; several ground finches in the genus Geospiza pluck ticks fromiguanas and tortoises in addition to eating seeds; the vegetarian finch (Platyspizacrassirostris) eats leaves and fruit.

For a test of the Theory of Evolution by Natural Selection, we focus on dataGrant and Grant and colleagues have gathered on the medium ground finch,Geospiza fortis, on Isla Daphne Major (Figure 3.7).

Daphne Major’s size and location make it a superb natural laboratory. Like allof the islands in the Galápagos, it is the top of a volcano (Figure 3.8).The islandis tiny. It rises from the sea to a maximum elevation of just 120 meters. It has one

Figure 3.7 The mediumground finch, Geospiza fortis(top) An adult male; (bottom) anadult female.

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Figure 3.8 The Galápagos Archipelago and Isla Daphne Major (a) Cocos Island and the Galapágos Archipelago, home of Darwin’sfinches. Isla Daphne Major is a tiny speck between Santa Cruz and Santiago. (b) Isla Daphne Major, seen from a boat approaching the is-land.Visible as a faint white line running upward from left to right is the footpath that runs from the boat landing (at the waterline) to thecampsite (on the rim of the crater). (c) A map of Daphne Major. Note the island’s tiny size. Rerendered from Boag and Grant (1984a).


main crater, with a small secondary crater adjacent to it.There is only one spoton the island that is both flat enough and large enough to pitch a camp. It takesjust 20 minutes to walk from the campsite all the way around the main crater’srim and back to camp.The climate is seasonal even though the location is equa-torial.A warmer, wetter season from January through May alternates with a cool-er, drier season from June through December. The vegetation consists of dryforest and scrub, with several species of cactus.

The medium ground finches on Daphne Major make an ideal study popula-tion. Few finches migrate onto or off of the island, and the population is smallenough to be studied exhaustively. In an average year, there are about 1,200 indi-vidual finches on the island. By 1977, Grant and Grant’s team had captured andmarked more than half of them; since 1980, virtually 100% of the population hasbeen marked. Medium ground finches live up to 16 years (Grant and Grant2000).Their generation time is 4.5 years (Grant and Grant 2002).

Medium ground finches are primarily seed eaters. The birds crack seeds bygrasping them at the base of the bill and then applying force.Grant and Grant andtheir colleagues have shown that both within and across finch species, beak size iscorrelated with the size of seeds harvested. In general, birds with bigger beaks eatlarger seeds, and birds with smaller beaks eat smaller seeds.This is because birdswith different beak sizes are able to handle different sizes of seeds more efficient-ly (Bowman 1961; Grant et al. 1976;Abbott et al. 1977; Grant 1981b).

Testing Postulate 1: Is the Finch Population Variable?The researchers mark every finch they catch by placing on its legs one num-bered aluminum band and three colored plastic bands.This allows them to iden-tify individual birds in the field.The scientists also weigh each finch and measureits wing length, tail length, beak width, beak depth, and beak length. All of thetraits they have investigated are variable. For example, when Grant and Grantplotted measurements of beak depth in the Isla Daphne Major population ofmedium ground finches, the data indicated that beak depth varies considerably(Figure 3.9). All of the finch characteristics Grant and Grant have measuredclearly conform to Darwin’s first postulate. As we will see in Chapter 4, varia-tion among the individuals within populations is virtually universal.

Some Geospiza fortis havebeaks that are only half as

deep as other individuals.

Numberof

finches

Beak depth (mm)

6 7 8 9 10 11 12 13 14

30

60

90 N = 751

Figure 3.9 Variation in beakdepth in medium ground finchesThis histogram shows the distribu-tion of beak depth in mediumground finches on Daphne Majorin 1976.A few birds have shallowbeaks; a few birds have deepbeaks; most birds have mediumbeaks. (N stands for sample size;the blue arrow along the x-axis in-dicates the mean, oraverage.)Rerendered from Boagand Grant (1984b).


Testing Postulate 2: Is Some of the Variation among IndividualsHeritable?Within the Daphne Major population, individual finches could vary in beakdepth because the environments they have experienced are different or becausetheir genotypes are different, or both.There are several ways that environmentalvariation could cause the variation in beak depth documented in Figure 3.9.Variation in the amount of food that individual birds happened to have receivedas chicks can lead to variation in beak depth among adults. Injuries or abrasionagainst hard seeds or rocks can also affect beak size and shape.

To determine whether at least part of the variation among finch beaks is ge-netically based, and thus passed from parents to offspring, Peter Boag, a colleagueof Peter Grant and Rosemary Grant, estimated the heritability of beak depth.

The heritability of a trait is defined as the proportion of the variation observedin a population that is due to variation in genes. Because it is a proportion, heri-tability varies between 0 and 1. We will develop the theory behind how heri-tability is estimated more fully in Chapter 9. For now, we point out that if thedifferences among individuals are due to differences in the alleles they have in-herited, then offspring will resemble their parents.

Boag compared the average beak depth of families of G. fortis young after theyhad attained adult size to the average beak depth of their mother and father.Boag’s data reveal a strong correspondence between relatives. As the plot inFigure 3.10 shows, parents with shallow beaks tend to have chicks with shallowbeaks, and parents with deep beaks tend to have chicks with deep beaks.This isevidence that a large proportion of the observed variation in beak depth is ge-netically based and can be passed to offspring (Boag and Grant 1978;Boag 1983).

Boag himself would be the first to say that caution is warranted in interpretinghis data. Environments shared by family members, maternal effects, conspecificnest parasitism, and misidentified paternity can cause graphs like the one inFigure 3.10 to exaggerate, or to underplay, the heritability of traits (see Box 3.1).However, Lukas Keller and colleagues (2001) have used modern genetic analysesto eliminate most of these confounding factors (Box 3.1). It is clear that Darwin’ssecond postulate is true for the medium ground finches on Daphne Major: Asubstantial fraction of the variation in beak size is due to variation in genotype.

8.0 9.0 10.0 11.0

8.0

9.0

10.0

11.0

Midparent beak depth (mm)

Midoffspring beakdepth (mm)

19781976

In finches, the beak depths ofparents and offspring aresimilar. This observationsuggests that some allelestend to produce shallowbeaks, while other alleles tendto produce deeper beaks.

Figure 3.10 Heritability ofbeak depth in Geospiza fortisThis graph shows the relationshipbetween the beak depth of par-ents and their offspring. Midparentvalue is the average of the mater-nal and paternal measurements;midoffspring value is the average ofthe offspring measurements.Thelines in the graph are statisticalbest-fit lines.The green line and cir-cles are from 1978 data, and theblue line and circles are from 1976data. Both years show a strong re-lationship between the beak depthof parents and their offspring.Rerendered from Boag (1983).

Heritabilities are estimated by measuring the similar-ity of traits among closely related individuals. Theidea is that genes run in families. If the variation inphenotype among individuals is due in part to varia-tion in genotype, then relatives will tend to resembleone another. But a number of confounding issuescan complicate this approach.We will consider foursuch issues here: misidentified paternity, conspecificnest parasitism, shared environments, and maternaleffects.Misidentified paternity In many species of birds,even socially monogamous birds like mediumground finches, females sometimes have extrapairsex.This means that a chick’s social father is not al-ways its biological father. If researchers simply as-sume that the social father at a nest is the biologicalfather of all the chicks, they may underestimate theheritability. Although it is expensive and time con-suming, misidentified paternity can be avoided byusing genetic paternity tests.Conspecific nest parasitism In some species ofbirds, females sneak into each other’s nests and layextra eggs.This means that even the social mother ata nest might not be the biological parent of all thechicks.Again, researchers may underestimate the her-itability.As with misidentified paternity, this problemcan be avoided by using genetic tests.Shared environments Relatives share their envi-ronment as well as their genes, and any correlationthat is due to their shared environment inflates theestimate of heritability. For example, it is well knownthat birds tend to grow larger when they have abun-dant food as chicks. But the most food-rich breedingterritories are often claimed and defended by thelargest adults in the population. Young from theseterritories will tend to become the largest adults inthe next generation. As a result, a researcher mightmeasure a strong relationship between parent andoffspring beak and body size, and claim a high heri-tability for these traits, when in reality there is none.In this case, the real relationship is between the envi-ronments that parents and their young each experi-enced as chicks.

In many species, this problem can be circumvent-ed by performing what are called cross-fostering,common garden, or reciprocal-transplant experi-ments. In birds, these experiments involve taking

eggs out of their original nest and placing them inthe nests of randomly assigned foster parents. Mea-surements in the young, taken when they are fullygrown, are then compared with the data from theirbiological parents. This experimental treatment re-moves any bias in the analysis created by the fact thatparents and offspring share environments.

Maternal effects Even cross-fostering experimentscannot remove environmental effects that are due todifferences in the nutrient stores or hormonal con-tents of eggs.These are called maternal effects.Theycan be largely avoided by estimating heritabilitiesfrom the resemblance between offspring and theirfathers only.

Lukas Keller and colleagues (2001) have made themost painstaking estimates to date of the heritability ofmorphological traits in Daphne Major’s mediumground finches. The researchers performed geneticanalyses to confirm the parentage of all the chicks intheir sample. They found no evidence of conspecificnest parasitism,but they did find that 20% of the chickshad been fathered by extrapair males. Excluding thesechicks from their data set, Keller and colleagues esti-mated that the heritability of beak depth is 0.65 (witha standard error of 0.15). In other words, about 65% ofthe variation among finches in beak depth appears tobe due to differences in genes.This estimate is uncont-aminated by extrapair paternity, conspecific nest para-sitism, and maternal effects. It might, however, containsome error due to shared environments.

It has not been possible for the Galápagos re-searchers to perform a cross-fostering experiment onDarwin’s finches. Because the Galápagos are a nationalpark, experiments that manipulate individuals beyondcatching and marking are forbidden. But the finchesthemselves have conducted a sort of cross-fostering ex-periment: As we mentioned above, about 20% of thechicks have been raised by males who are not their bi-ological fathers. If some of the resemblance betweenparents and offspring is due to shared environments,then these chicks should resemble their social fathers.Using data on the social fathers and their foster off-spring, Keller and colleagues calculated the “heritabili-ty” of beak depth. It was less than 0.2 and was notstatistically distinguishable from zero.This suggests thatshared environments have little influence on the re-semblance among relatives’ beaks.

Issues that complicate how heritabilities are estimatedBox 3.1

84


We do not know the identity of the specific genes reponsible for variation inbeak size in medium ground finches. However, Arhat Abzhanov and colleagues(2004), working in the laboratory of Clifford Tabin, discovered a tantalizing clue.These researchers focussed on growth factors known to be active during embry-onic development.Among them was bone morphogenic protein 4, or BMP4, asignalling molecule that helps sculpt the shape of bird beaks (Wu et al. 2004). Forall six species of ground finches,Abzhanov and colleagues treated embryos of dif-ferent ages with a probe that stains messenger RNA made by the gene that en-codes BMP4.As the photos in Figure 3.11 show, ground finch species with largerbeaks make BMP4 mRNA (and presumably BMP4) earlier and in larger quanti-ties than species with smaller beaks.The large ground finch, Geospiza magnirostris,for example, has by far the biggest beak; it is also the only species that beginsmaking BMP4 mRNA at stage 26 of development. Abzhanov and colleaguessuggest that the different species of ground finches harbor alternate versions ofone or more of the genes that determine when, where, and how strongly theBMP4 gene is activated.A reasonable hypothesis would be that a similar geneticmechanism is responsible for some of the variation among individuals in themedium ground finch population on Daphne Major.

Geospizafuliginosa

Geospizafortis

Geospizamagnirostris

Geospizascandens

Geospizaconirostris

Geospizadifficilis

Small ground finch

Medium ground finch

Large ground finch

Cactus ground finch

Large cactus ground finch


mRNA from BMP4 geneAt stage 26 At stage 29

Figure 3.11 Bone morphogenic protein 4 and beak de-velopment in Darwin’s ground finches The first column il-lustrates the differences in beak size and shape among thesix species of ground finches.The second and third columnsshow cross sections of the upper beak bud in embryos ofeach species at two stages of development.The cross sec-tions have been treated with a probe that stains mRNAmade from the gene for bone morphogenic protein 4, orBMP4.The stained mRNA appears as dark areas indicatedby arrowheads. Adult finch photos from Petren et al.(1999); embryos from Abzhanov et al. (2004).


Testing Postulate 3: Do Individuals Vary inTheir Success at Surviving or Reproducing?Because Grant and Grant and their colleagues have beenmonitoring the finches on Daphne Major every yearsince 1973, two members of the research team, PeterBoag and Laurene Ratcliffe, were on the island in 1977to witness a terrible drought (Boag and Grant 1981;Grant 1999). Instead of the normal 130 mm of rainfallduring the wet season, the island got only 24 mm.Theplants made few flowers and few seeds. The mediumground finches did not even try to breed. Over thecourse of 20 months, 84% of the Geospiza fortis onDaphne Major disappeared (Figure 3.12a). The re-searchers inferred that most died of starvation.The de-cline in population size was simultaneous with a declinein the availability of the seeds the birds depend on forfood (Figure 3.12b); 38 emaciated birds were actuallyfound dead,and none of the missing birds reappeared thefollowing year. It is clear that only a fraction of the pop-ulation survived to reproduce. This sort of mortality isnot unusual. For example, Rosemary Grant has shownthat 89% of Geospiza conirostris individuals die beforethey breed (Grant 1985). Trevor Price and coworkers(1984) determined that an additional 19% and 25% ofthe G. fortis on Daphne Major died during subsequentdrought events in 1980 and 1982, respectively.

In fact, in every natural population studied, moreoffspring are produced each generation than survive tobreed. If a population is not increasing in size, theneach parent will, in the course of its lifetime, leave anaverage of one offspring that survives to breed. But thereproductive capacity (or biotic potential) of organ-isms is astonishing. Darwin (1859) picked the elephantto illustrate this point, because it was the slowestbreeder then known among animals. He calculatedthat if all the descendants of a single pair survived andreproduced, then after just 750 years there would be19 million of them. The numbers are even more star-tling for rapid breeders. Dodson (1960) calculated thatif all the descendents of a pair of starfish survived andreproduced, then after just 16 years they would exceed

, the estimated number of electrons in the visibleuniverse.1079

Jan Apr Jul Oct Jan Apr Jul Oct Jan Apr Jul Oct JanJul Oct

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Figure 3.12 Decline of ground finch population and available seeds during the 1977 drought (a) This graph shows the number ofground finches found on Daphne Major before, during, and after the drought.The vertical lines through each data point represent a quanti-ty called the standard error, which indicates the amount of variation in census estimates.The lines in this graph are simply drawn from pointto point to make the trend easier to see. (b) This graph shows the abundance of seeds on Daphne Major before, during, and after thedrought. (c) This graph shows the characteristics of the average seed available as food to medium ground finches before, during, and afterthe drought.The hardness index plotted on the y-axis is a special measure created by Boag and Grant (1981).


Similarly, data show that in most populations some of the individuals that sur-vive to breed are more successful at mating and producing offspring than others.Just as variation in survival does, variation in reproductive success represents se-lection. Darwin’s third postulate is universally true.

Testing Postulate 4:Are Survival and Reproduction Nonrandom?Darwin’s fourth claim was that the individuals who survive and go on to repro-duce, or who reproduce the most, are those with certain, favorable variations.Dida nonrandom, or selected, subset of the medium ground finch population survivethe 1977 drought? The answer is yes.

As the drought wore on, not only the number, but also the types of seeds avail-able changed dramatically (Figure 3.12c).The finches on Daphne Major eat seedsfrom a variety of plants.The seeds range from small and soft to large and hard.The small, soft seeds, easy to crack, are the birds’ favorites. During the drought, asat other times, the finches ate the small, soft seeds first. Once most of the small,soft seeds were gone, the large, hard fruits of an annual plant called Tribulus cis-toides became a key food item. Only large birds with deep, narrow beaks cancrack and eat Tribulus fruits successfully.The rest of the finches were left to turnover rocks and scratch the soil in search of the few remaining smaller seeds.

The top graph in Figure 3.13 is from Figure 3.9 on page 82. It shows the beaksizes of a large and random sample of the birds living on Daphne Major the yearbefore the drought.The bottom graph in Figure 3.13 shows the beak sizes of arandom sample of 90 birds who survived the drought.The average survivor had adeeper beak than the average nonsurvivor. Because deep beaks and large bodysizes are positively correlated, and because large birds tend to win fights overfood, the average survivor had a larger body size too.

During the drought, fincheswith larger, deeper beaks hadan advantage in feeding, andthus in surviving.

Numberof

finches

6 7 8 9 10 11 12 13 14

30

60

90N = 751

Numberof

finches

Beak depth (mm)6 7 8 9 10 11 12 13 14

N = 90

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1976 all Daphne birds

1978 survivors

Figure 3.13 Beak depth be-fore and after natural selectionThese histograms show the distri-bution of beak depth in mediumground finches on Daphne Major,before and after the drought of1977.The blue triangles indicatethe population means. Reren-dered from Boag and Grant(1984b).


The 1977 selection event, as dramatic as it was, was not an isolated occurrence.In 1980 and 1982 there were similar droughts, and selection again favored individ-uals with large body size and deep beaks (Price et al. 1984).Then, in 1983, an in-flux of warm surface water off the South American coast, called an El Niño event,created a wet season with 1,359 mm of rain on Daphne Major.This dramatic envi-ronmental change (almost 57 times as much rain as in 1977) led to a superabun-dance of small, soft seeds and, subsequently, to strong selection for smaller body size(Gibbs and Grant 1987).After wet years, small birds with shallow beaks survive bet-ter and reproduce more because they harvest small seeds much more efficientlythan large birds with deep beaks. Larger birds were favored in drought conditions,but smaller birds were favored in wet years.Natural selection—as we pointed out inour analysis of HIV evolution in Chapter 1—is dynamic.

Testing Darwin’s Prediction: Did the Population Evolve?All four of Darwin’s postulates are true for the medium ground finch populationon Daphne Major. Darwin’s theory therefore predicts a change in the composi-tion of the population from one generation to the next.When the deep-beakedbirds who survived the drought of 1977 bred to produce a new generation, theyshould have passed their genes for deep beaks to their offspring. Figure 3.14 con-firms that they did.The chicks hatched in 1978, the year after the drought, haddeeper beaks, on average, than the birds hatched in 1976, the year before thedrought.The population evolved.

Peter Grant and Rosemary Grant and their colleagues have continued tomonitor the Daphne Major finch population since the 1970s.As a result of un-predictable changes in the climate and bird community, and consequent changesin the Daphne Major plant community, the researchers have seen selection events

Beak size (depth in mm)

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7.3 7.8 8.3 8.8 9.3 9.8 10.3 10.8 11.3Figure 3.14 Beak depth in thefinches hatched the year beforethe drought versus the year afterthe drought The red trianglesrepresent population means.Redrawn from Grant and Grant(2003).

As a result of the drought,the finch population evolved.

Selection occurs withingenerations; evolution occurs

between generations.


in which deep-beaked birds were more likely to survive and selection events inwhich shallow-beaked birds were more likely to survive.

Figure 3.15 shows the pattern of change in the population averages for threetraits across three decades. Each of the three traits is a statistical composite ofmeasurable traits, like beak depth. For example, “PC1 beak size” (Figure 3.15a)combines beak depth, beak length, and beak width. The evolutionary changesthat occurred as a result of 1977 drought are highlighted in red.

Figure 3.15a shows, first, what we have already seen: During the drought of1977 the finch population evolved a significantly larger average beak size. In ad-dition, the figure shows that the population remained at this large mean beak sizeuntil the mid-1980s, then evolved back to the mean beak size it started with.There the population stayed for many years, until another drought struck.

The drought of 2003 and 2004 was as bad as the drought of 1977 (Grant andGrant 2006).Once again the medium ground finches ran short of food and manyperished. This time, however, the medium ground finches faced an additionalchallenge: competition from a substantial population of large ground finches(Geospiza magnirostris) that had become established on the island. The largeground finches dominated access to, and consumed, the Tribulus fruits on whichthe large-beaked medium ground finches had survived in 1977. As a result, themedium ground finches with large beaks died at higher rates than the ones withsmall beaks did, and the population evolved toward smaller beak size.

In its mean beak shape and mean body size the medium ground finch populationalso showed substantial evolution [Figure 3.15b and (c)].The average bird in 2001 hada significantly sharper beak, and was significantly smaller than the average bird in themid-1970s (Grant and Grant 2002).

Grant and Grant’s long-term study demonstrates that Darwin’s mechanism ofevolution can be documented in natural populations.When all four of Darwin’s

1

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Figure 3.15 Thirty years ofevolution in the medium groundfinch population on Isla DaphneMajor These graphs track theaverage adult values for beak size,beak shape, and body size amongthe Geospiza fortis on DaphneMajor from the early 1970s intothe 2000s.The vertical whiskersrepresent the 95% confidence in-terval for the estimated mean. Ifthere had been no evolution, theconfidence intervals for all dotswould have overlapped the tanband—the 95% confidence inter-val for 1973, the first year withcomplete data.The changes thatoccurred during the drought of1977 are indicated in red. In (a)the change that occurred duringthe drought of 2004 is indicatedin orange. The populationshowed significant evolution in allthree traits. (a) Rerendered fromGrant and Grant (2006). (b andc) Rerendered from Grant andGrant (2002).


postulates are true in a population, the population evolves.The study also showsthat small evolutionary changes over short time spans can accumulate into largerchanges over longer time spans.

3.5 The Nature of Natural SelectionAlthough the Theory of Evolution by Natural Selection can be stated concisely,tested rigorously in natural populations, and validated, it can be difficult to un-derstand thoroughly. One reason is that under Darwin’s theory descent withmodification is essentially a statistical process: a change in the trait distributions ofpopulations. Statistical thinking does not come naturally to most people, andthere are a number of widely shared ideas about natural selection that are incor-rect. Our goal in this section is to cover some key points about how selectiondoes and does not operate.

Natural Selection Acts on Individuals, but Its ConsequencesOccur in PopulationsWhen HIV strains were selected by exposure to AZT, or finch populations wereselected by changes in seed availability, none of the selected individuals (virionsor finches) changed in any way. They simply lived through the selection eventwhile others died or reproduced more than competing virions or birds. Whatchanged after the selection process was the characteristics of the populations ofvirions and finches, not the affected individuals themselves. Specifically, a higherfrequency of HIV virions in the population were able to replicate in the presenceof AZT, and a higher proportion of finches had deep beaks.

To state this point another way, the effort of cracking Tribulus seeds did notmake finch beaks become deeper and their bodies larger, and the effort of tran-scribing RNA in the presence of AZT did not change the amino acid composi-tion of the reverse transcriptase active site. Instead, the average beak depth andbody size in the finch population increased because more smaller finches diedthan larger ones (Figure 3.16), and the average active site sequence in reversetranscriptase changed because certain mutants did a better job of making newvirions.

Natural Selection Acts on Phenotypes, but Evolution Consists ofChanges in Allele FrequenciesFinches with large bodies and deep beaks would have survived at higher ratesduring the drought even if all of the variation in the population had been envi-ronmental in origin (that is, if heritabilities had been zero). But no evolutionwould have occurred. Selection would have altered the frequencies of the phe-notypes in the population, but in the next generation the phenotype distributionmight have gone back to what it was before selection occurred (Figure 3.17).

Only when the survivors of selection pass their successful phenotypes to theiroffspring, via genotypes that help determine phenotypes, does natural selectioncause populations to change from one generation to the next. On DaphneMajor, the variation in finch phenotypes that selection acted on had a geneticbasis.As a result, the new phenotypic distribution seen among the survivors per-sisted into the next generation.

Average beak

Average beak

Before selection

After selection

Figure 3.16 Natural selectionhappens to individuals, but whatchanges is populations Duringthe drought on Daphne Major in-dividuals did not change theirbeak depths; they simply lived ordied.What changed was the aver-age beak depth, a characteristic ofthe population.

If beak depth is heritable

If beak depth is not heritable

x

x

Figure 3.17 Populations evolveonly if traits are heritable If vari-ation is due to differences ingenotype, then the survivors ofselection pass their successfulphenotypes to their offspring.


Natural Selection Is Not Forward LookingEach generation is descended from the survivors of selection by the environ-mental conditions that prevailed in the generation before.The offspring of theHIV virions and finches that experienced selection are better adapted to envi-ronments dominated by AZT and drought conditions, respectively, than theirparents’ generation was. If the environment changed again during the lifetime ofthese offspring, however, they might not be adapted to the new conditions.

There is a common misconception that organisms can be adapted to futureconditions, or that selection can look ahead in the sense of anticipating environ-mental changes during future generations.This is impossible. Evolution is alwaysa generation behind any changes in the environment.

New Traits Can Evolve, Even Though Natural Selection Acts onExisting TraitsDifferences in survival or reproduction—that is, natural selection—can onlyoccur among variants that already exist. Death by starvation of small-beakedfinches, for example, does not instantaneously create birds with big beaks optimalfor cracking Tribulus fruits. It merely winnows the breeding population down tothe largest-beaked of the birds already living.

This may seem to imply that new traits cannot evolve by natural selection. Butthe evolution of new traits is, in fact, possible for two reasons. First, during repro-duction in all species, mutations produce new alleles. Second, during reproductionin sexual species, meiosis and fertilization recombine existing alleles into new geno-types. Mutation and recombination yield new suites of traits for selection to sort.

Consider, for example, an artificial selection study run at the University of Illinois(Moose et al. 2004). Since they started in 1896 with 163 ears of corn, researchershave been sowing for next year’s crop only seeds from the plants with the highest oilcontent in their kernels. In the starting population,oil content ranged from 4–6% byweight.After 100 generations of selection, the average oil content in the populationwas about 20% (Figure 3.18).That is, a typical plant in the present population hasover three times the oil content of the most-oil rich plant in the founding popula-tion. Mutation, recombination, and selection together produced a new phenotype.

Natural selection adaptspopulations to conditionsthat prevailed in the past, notconditions that might occurin the future.

1000

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Original population range

Average oil content of

corn kernels (%)Figure 3.18 Persistent long-term selection can result in dra-matic changes in traits Thesedata, from the Illinois Long-TermSelection Experiment, documentthe increase in oil content in cornkernels during 100 generations ofartificial selection.The average forthe 100th generation lies far out-side the range of the foundinggeneration. Modified from Mooseet al. (2004).


Persistent natural selection can lead to the evolution of entirely new functionsfor existing behaviors, structures, or genes.The giant panda’s thumb provides anexample (Gould 1980; Endo et al. 1999a, 1999b, 2001). Pandas use this structureto get a firm grip on the stalks of their favorite food, bamboo (Figure 3.19a).Anatomically, the “thumb” is actually an enlarged and modified radial sesamoidbone, which in closely related species is part of the wrist (Figure 3.19b). Know-ing how natural selection works in contemporary populations, we surmise thatwhen pandas first began eating bamboo, there was variation among individuals inthe length of the radial sesamoid. Pandas with bigger radial sesamoids had firmergrips, fed more efficiently, and consequently had more offspring. As a result ofcontinued selection over many generations, the average size of the bone in-creased in the population until it reached its present dimensions.

A trait that is used in a novel way and is eventually elaborated by selection intoa completely new structure, like the radial sesamoid of the ancestral panda, isknown as a preadaptation.An important point about preadaptations is that theyrepresent happenstance. A preadaptation improves an individual’s fitness fortu-itously—not because natural selection is conscious or forward looking.

Natural Selection Does Not Lead to PerfectionThe previous paragraphs argue that populations evolving by natural selection be-come better adapted over time. It is equally important, however, to realize thatevolution does not result in organisms that are perfect.

Consider the male mosquito fish (Gambusia affinis), whose anal fin is modifiedto serve as a copulatory organ, or gonopodium. Brian Langerhans and colleages(2005) found that females prefer males with larger gonopodia. But when preda-tors attack, a big gonopodium is literally a drag, slowing a male’s escape.A perfectmale would be irresistable to females and fleet enough to evade any predator.Alas, no male can be both. Instead, each population evolves a phenotype thatstrikes a compromise between opposing agents of selection (Figure 3.20).

(a) (b)

Bamboo stalk

5 Fingers

“Thumb”

“Thumb”

Radial sesamoid

5 mm

Figure 3.20 No guy is perfectThese males sport gonopodiathat attract mates but hinder es-cape.The male at bottom is froma high-predation population.

Figure 3.19 The panda’s thumb (a) Giant pandas can grasp and manipulate bamboo stalks in their paws. (b) These drawings showhow the Panda’s thumb, actually a modified wrist bone, helps clamp a stalk in the animal’s curled fingers. After Endo et al. (1999a, b; 2001).


Natural selection cannot simultaneously optimize all traits. It leads to adapta-tion, not perfection.

Natural Selection Is Nonrandom, but It Is Not ProgressiveEvolution by natural selection is sometimes characterized as a random or chanceprocess, but nothing could be further from the truth. Mutation and recombina-tion, the processes that generate genetic variation, are random with respect to thechanges they produce in phenotypes. But natural selection, the mechanism thatsorts among variant phenotypes and genotypes, is the opposite of random. It is,by definition, the nonrandom superiority at survival and reproduction of somevariants over others.This is why evolution by means of natural selection is non-random, why, instead, it increases adaptation to the environment.

As the HIV, finch, and panda examples show, however, nonrandom selection asit occurs in nature is completely free of any entity’s conscious intent. Darwincame to regret using the phrase “naturally selected,” because people thought itimplied a conscious act or choice by some entity. Nothing of the sort happens.

Also, although evolution has tended toward increases in the complexity, de-gree of organization, and specialization of organisms over time, it is not progres-sive in the sense of leading toward some predetermined goal. Evolution makespopulations “better” only in the sense of increasing their average adaptation totheir environment.There is no inexorable trend toward more advanced forms oflife. For example, contemporary tapeworms have no digestive system and haveactually evolved to be simpler than their ancestors. Snakes evolved from ancestorsthat had limbs.The earliest birds in the fossil record had teeth.

Unfortunately, a progressivist view of evolution dies hard. Even Darwin had toremind himself to “never use the words higher or lower” when discussing evolu-tionary relationships. It is true that some organisms are the descendants of ancientlineages and some are the descendants of more recent lineages, but all organisms inthe fossil record and those living today were adapted to their environments.Theyare all able to survive and reproduce. None is “higher” or “lower” than any other.

Fitness is Not CircularThe Theory of Evolution by Natural Selection is often criticized by nonbiolo-gists as tautological, or circular in its reasoning.That is, after reviewing Darwin’sfour postulates, one could claim,“Of course individuals with favorable variationsare the ones that survive and reproduce because the theory defines favorable asthe ability to survive and reproduce.”

The key to resolving the issue is to realize that the word “favorable,” althougha convenient shorthand, is misleading.The only requirement for natural selectionis for certain heritable variants to do better than others, as opposed to randomones.As long as a nonrandom subset of the population survives better and leavesmore offspring, evolution will result. In the examples we have been analyzing, re-search not only determined that nonrandom groups survived a selection event,but also uncovered why those groups did better than others.

It should also make sense by now that Darwinian fitness is not an abstractquantity. Fitness can be measured in nature. This is done by counting the off-spring that individuals produce, or by observing their ability to survive a selec-tion event, and comparing each individual’s performance to that of others in thepopulation.These are independent and objective criteria for assessing fitness.

There is no such thing as ahigher or lower plant oranimal.


Selection Acts on Individuals, Not for the Good of the SpeciesOne of the most pervasive misconceptions about natural selection, especially se-lection on animal behavior, is that individual organisms will perform actions forthe good of the species. Self-sacrificing, or altruistic, acts do occur in nature.Prairie dogs give alarm calls when predators approach, which draws attention tothemselves. Lion mothers sometimes nurse cubs that are not their own. But traitscannot evolve by natural selection unless they increase the bearer’s fitness relativeto competing individuals. If an allele existed that produced a truly altruistic be-havior—that is, a behavior that reduced the bearer’s fitness and increased the fit-ness of others—it would quickly disappear from the population.As we will see inChapter 12, every altruistic behavior that has been studied in detail has beenfound to increase the altruist’s fitness, either because the beneficiaries of the be-havior are close genetic relatives (as in prairie dogs) or because the beneficiariesreciprocate (as in nursing lions) or both.

The idea that animals will do things for the good of the species is so ingrained,however, that we will make the same point a second way. Consider lions again.Lions live in social groups called prides. Coalitions of males fight to take overprides. If a new group of males defeats the existing pride males in combat, thenewcomers quickly kill all of the pride’s nursing cubs.These cubs are unrelatedto them. Killing the cubs increases the new males’ fitness because pride femalesbecome fertile again sooner and will conceive offspring by the new males (Pack-er and Pusey 1983, 1984). Infanticide is widespread in animals. Clearly, behaviorlike this does not exist for the good of the species. Rather, infanticide exists be-cause, under certain conditions, it enhances the fitness of the individuals whoperform the behavior relative to individuals who do not.

3.6 The Evolution of DarwinismBecause evolution by natural selection is a general organizing feature of living sys-tems, Darwin’s theory ranks as one of the great ideas in intellectual history. Its im-pact on biology is analogous to that of Newton’s laws on physics, Copernicus’sSun-Centered Theory of the Universe on astronomy, and the Theory of Plate Tec-tonics on geology. In the words of evolutionary geneticist Theodosius Dobzhan-sky (1973),“Nothing in biology makes sense except in the light of evolution.”

For all its power, though, the Theory of Evolution by Natural Selection wasnot universally accepted by biologists until some 70 years after it was initiallyproposed.There were three serious problems with the theory, as originally for-mulated by Darwin, that had to be resolved.

1. Because Darwin knew nothing about mutation, he had no ideahow variability was generated in populations. As a result, he could not an-swer critics who maintained that the amount of variability in populations wasstrictly limited and that natural selection would grind to a halt when variabilityran out. It was not until the early 1900s, when geneticists such as Thomas HuntMorgan began experimenting with fruit flies, that biologists began to appreciatethe continuous and universal nature of mutation. Morgan and colleagues showedthat mutations occur in every generation and in every trait.

2. Because Darwin knew nothing about genetics, he had no idea howvariations are passed on to offspring. It was not until Mendel’s experimentswith peas were rediscovered and verified,35 years after their original publication, that

Individuals do not do thingsfor the good of the species.

They behave in a way thatmaximizes their individual

fitness.


biologists understood how parental traits are passed on to offspring. Mendel’s laws ofsegregation and independent assortment confirmed the mechanism behind postulate2,which states that some of the variation observed in populations is heritable.

Until then,many biologists proposed that genes acted like pigments in paint.Ad-vocates of this hypothesis, called blending inheritance, argued that favorable mu-tations would simply merge into existing traits and be lost. In 1867, a Scottishengineer named Fleeming Jenkin published a mathematical treatment of blendinginheritance, along with a famous thought experiment concerning the offspring oflight-skinned and dark-skinned people.For example, if a dark-skinned sailor becamestranded on an equatorial island inhabited by light-skinned people, Jenkins’ modelpredicted that no matter how advantageous dark skin might be (in reducing skincancer, for example), the population would never become dark-skinned becausetraits like skin color blended. If the dark-skinned sailor had children by a light-skinned woman, their children would be brown-skinned. If they, in turn, had chil-dren with light-skinned people, their children would be light-brown-skinned, andso on. Conversely, if a light-skinned sailor became stranded on a northern island in-habited by dark-skinned people, blending inheritance argued that, no matter howadvantageous light skin might be (in facilitating the synthesis of vitamin D with en-ergy from UV light, for example), the population would never become light.Underblending inheritance new variants are swamped, and new mutations diluted, untilthey cease to have a measurable effect. For natural selection to work, favorable newvariations have to be passed on to offspring intact, and remain discrete.

We understand now, of course, that phenotypes blend in some traits, like skincolor, but genotypes never do. Jenkins’s hypothetical population would, in fact, be-come increasingly darker or lighter skinned if selection were strong and mutationcontinually added darker- or lighter-skinned variants to the population via changesin the genes involved in regulating the production of melanin (Figure 3.21).

Darwin himself struggled with the problem of inheritance, and eventuallyadopted an entirely incorrect view based on the work of Jean-Baptiste Lamarck.Lamarck was a great French biologist of the early 19th century who proposedthat species evolve through the inheritance of changes wrought in individuals.Lamarck’s idea was a breakthrough: It recognized that species have changedthrough time and proposed a mechanism to explain how. His theory waswrong, however, because offspring do not inherit phenotypic changes acquiredby their parents. If people build up muscles lifting weights, their offspring arenot more powerful; if giraffes stretch their necks reaching for leaves in treetops,it has no consequence for the neck length of their offspring.

Melanocyte

Pigment-containingmelanosomes

Dysfunctional MC1-R

MSH receptor(MC1-R)

Agouti signallingprotein (ASP)

�-MSH

Eumelanin

Pheomelanin

(a)

(b)

(c)

Figure 3.21 Why blending inheritance does not occur (a) Skin (and hair) color in mammalsis largely determined by the production of pigments in cells called melanocytes. (b)When alphamelanocyte-stimulating hormone binds to the melanocortin 1 receptor (MC1-R), itstimulates melanocytes to make eumelanin, which is brownish black. (c)When MC1-R is dysfunc-tional, or when it is blocked by agouti signalling protein (ASP), melanocytes make pheomelanin,which is reddish yellow.

Variation in human coloration has been tied to allelic variation in both the gene for MC1-R andthe gene for ASP (Harding et al. 2000; Schaffer and Bolognia 2001; Kanetsky et al. 2002). For exam-ple, homozygotes for the Arg151Cys allele of the MC1-R gene almost always have red hair and fairskin (Smith et al. 1998).The effects of alleles may blend in determining the phenotype.An individualwith just one copy of the Arg151Cys allele, for instance, may have intermediate coloration. But thealleles themselves are passed on intact to offspring, and two Arg151Cys heterozygotes can have ahomozygous red-haired offspring.Thus inheritance is particulate, not blending. After Schaffer andBolognia 2001.

(a–MSH)


3. Lord Kelvin, the foremost physicist of the 19th century, publishedan important series of papers in the early 1860s estimating the age ofEarth at 15–20 million years. Kelvin’s analyses were based on measurementsof the Sun’s heat and the temperature of Earth. Because fire was the only knownsource of heat at the time, Kelvin assumed that the Sun was combusting like anenormous lump of coal. This had to mean that the Sun was gradually burningdown, releasing progressively less heat with each passing millennium. Likewise,both geologists and physicists believed that the surface of Earth was graduallycooling.This was based on the assumption that Earth was changing from a moltenstate to a solid one by radiating heat to the atmosphere, a view apparently sup-ported by measurements of progressively higher temperatures deeper down in mine-shafts.These data allowed Kelvin to calculate the rate of radiant cooling.

The bottom line from Kelvin’s calculations was that the transition from a hotto cold Sun and hot to cold Earth created a narrow window of time when life onEarth was possible. The window was clearly too narrow to allow the gradualchanges of Darwinism to accumulate, and thus strongly supported a role for in-stantaneous and special creation in explaining adaptation and diversity.

The discovery of radioactive isotopes early in the 20th century changed allthat. Kelvin’s calculations were correct, but his assumptions were wrong. Scien-tists confirmed that Earth’s heat is a by-product of radioactive decay, not radiantcooling, and that the Sun’s heat is from nuclear fusion, not combustion.

The Modern SynthesisUnderstanding variability, inheritance, and time was so difficult that the first 70years of evolutionary biology were characterized by turmoil (see Provine 1971;Mayr 1980, 1991). But between 1932 and 1953 a series of landmark books werepublished that successfully integrated genetics with Darwin’s four postulates andled to a reformulation of the Theory of Evolution.This restatement, known asthe Modern Synthesis or the Evolutionary Synthesis, was a consensus groundedin two propositions:

• Gradual evolution results from small genetic changes that are acted upon bynatural selection.

• The origin of species and higher taxa, or macroevolution, can be explained interms of natural selection acting on individuals, or microevolution.

With the synthesis, Darwin’s original four postulates and their outcome could berestated along the following lines:

1. As a result of mutation creating new alleles, and segregation and independentassortment shuffling alleles into new combinations, individuals within popula-tions are variable for many traits.

2. Individuals pass their alleles on to their offspring intact.3. In every generation, some individuals are more successful at surviving and re-

producing than others.4. The individuals that survive and reproduce, or who reproduce the most, are

those with the alleles and allelic combinations that best adapt them to theirenvironment.

The outcome is that alleles associated with higher fitness increase in frequencyfrom one generation to the next.

The Modern Synthesisresolved decades of

controversy over the validityof evolution by natural

selection.


This View of LifeDarwin ended the introduction to the first edition of On the Origin of Species witha statement that still represents the consensus view of evolutionary biologists(Darwin 1859,p. 6):“Natural Selection has been the main but not exclusive meansof modification.”We now think of modification in terms of changes in the fre-quencies of the alleles responsible for traits like beak depth and AZT resistance.Weare more keenly aware of other processes that cause evolutionary change in addi-tion to natural selection. (Chapters 6 and 7 explore these processes in detail.) Butthe Darwinian view of life, as a competition between individuals with varyingabilities to survive and reproduce, has proven correct in almost every detail.

As Darwin wrote in his concluding sentence (1859, p. 490): “There isgrandeur in this view of life, with its several powers, having been originallybreathed into a few forms or into one; and that, whilst this planet has gone cy-cling on according to the fixed law of gravity, from so simple a beginning endlessforms most beautiful and most wonderful have been, and are being, evolved.”

3.7 The Debate over “Scientific Creationism” and Intelligent Design Creationism

Scientific controversy over the fact of evolution ended in the late 1800s, whenthe evidence reviewed in Chapter 2 simply overwhelmed the critics. Whethernatural selection was the primary process responsible for both adaptation and di-versity was still being challenged until the 1930s, when the works of the ModernSynthesis provided a mechanistic basis for Darwin’s four postulates and unifiedmicro- and macroevolution. Evolution by natural selection is now considered thegreat unifying idea in biology.Although scientific discourse about the validity ofevolution by natural selection ended well over a half-century ago, a political andphilosophical controversy in the United States and Europe still continues (Hold-en 1995; Kaiser 1995).What is this debate, and why is it occurring?

History of the ControversyThe Scopes Trial of 1925, popularly known as the Monkey Trial, is perhaps themost celebrated event in a religious debate that has raged since Darwin firstpublished On the Origin of Species (see Gould 1983, essay 20; Larson 1997). JohnScopes (Figure 3.22) was a biology teacher who gave his students a reading as-signment about Darwinian evolution.This was a clear violation of the State ofTennessee’s Butler Act, which prohibited the teaching of evolution in publicschools.William Jennings Bryan, a famous politician and a fundamentalist orator,was the lawyer for the prosecution; Clarence Darrow, the most renowned defenseattorney of his generation, led Scopes’s defense.Although Scopes was convictedand fined $100, the trial was widely perceived as a triumph for evolution becauseBryan had suggested, while on the stand as a witness, that the six days of creationdescribed in Genesis 1:1–2:4 may each have lasted far longer than 24 hours.Thiswas considered a grave inconsistency, and therefore a blow to the integrity of thecreationist viewpoint. But far from ending the debate over teaching evolution inU.S. schools, the Scopes trial was merely a way station.

The Butler Act, in fact, stayed on the books until 1967; it was not until 1968,in Epperson v. Arkansas, that the U.S. Supreme Court struck down laws that

Creationists want the Theoryof Special Creation to betaught in public schools, eventhough it was dismissed as aviable alternative to theTheory of Evolution by NaturalSelection over a century ago.

Figure 3.22 Scopes on TrialJohn Scopes, right, confers with amember of his defense team.


prohibit the teaching of evolution.The court’s ruling was made on the basis ofthe U.S. Constitution’s separation of church and state. In response, fundamen-talist religious groups in the United States reformulated their arguments as“creation science” and demanded equal time for what they insisted was an al-ternative theory for the origin of species. By the late 1970s, 26 state legislatureswere debating equal-time legislation (Scott 1994). Arkansas and Louisianapassed such laws only to have them struck down in state courts.The Louisianalaw was then appealed all the way to the U.S. Supreme Court, which decidedin 1987 (Edwards v. Aquillard) that because creationism is essentially a religiousidea, teaching it in the public schools was a violation of the first amendment.Two justices, however, formally wrote that it would still be acceptable forteachers to present alternative theories to evolution (Scott 1994).

One response from opponents of evolution has been to drop the words cre-ation and creator from their literature and call either for equal time for teachingthat no evolution has occurred, or for teaching a proposal called Intelligent De-sign Theory, which infers the presence of a designer from the perfection of adap-tation in contemporary organisms (Scott 1994; Schmidt 1996). In the fall of 2005the case of Kitzmiller et al. v. Dover Area School District was tried in Dover, Penn-sylvania.The school district had enacted a policy requiring that students in biol-ogy classes “be made aware of gaps/problems in Darwin’s Theory and of othertheories of evolution including, but not limited to, intelligent design.”A group ofparents sued the school district on the grounds, again, that the policy violates thefirst ammendment.The court agreed (Goodstein 2005; Jones 2005).

The complexity and perfection of organisms is a time-worn objection to evo-lution by natural selection. Darwin was aware of it; in his Origin he devoted a sec-tion of the chapter titled “Difficulties on Theory” to “Organs of extremeperfection.” How can natural selection, by sorting random changes in thegenome, produce elaborate and integrated traits like the vertebrate eye?

Perfection and Complexity in NatureThe English cleric William Paley, writing in 1802, promoted the Theory of Spe-cial Creation with a now-classic argument. If a person found a watch and discov-ered that it was an especially complex and accurate instrument, they wouldnaturally infer that it had been made by a highly skilled watchmaker. Paley thendrew a parallel between the watch and the perfection of the vertebrate eye andasked his readers to infer the existence of a purposeful and perfect Creator. Hecontended that organisms are so well-engineered that they have to be the workof a conscious designer.This logic, still used by creationists today, is called the Ar-gument from Design (Dawkins 1986).

Because we perceive perfection and complexity in the natural world, evolu-tion by natural selection seems to defy credulity.There are actually two concernshere.The first is how random changes can lead to order. Mutations are chanceevents, so the generation of variation in a population is random. But the selectionof those variants, or mutants, is nonrandom: It is directed in the sense of increas-ing fitness. And adaptations—structures or behaviors that increase fitness—arewhat we perceive as highly ordered, complex, or even perfect in the naturalworld. But there is nothing conscious or intelligent about the process.The biol-ogist Richard Dawkins captured this point by referring to natural selection as ablind watchmaker.

The Argument from Designcontends that adaptations

must result from the actionsof a conscious entity.


A second, and closely related, concern is: How can complex, highly integratedstructures, like the vertebrate eye, evolve through the Darwinian process of grad-ual accumulation of small changes? Each evolutionary step would have to in-crease the fitness of individuals in the population. Darwinism predicts thatcomplex structures have evolved through a series of intermediate stages, or grad-ed forms. Is this true? For example, when we consider a structure like the eye, dowe find a diversity of forms, some of which are more complex than others?

The answer to these questions is yes. In some unicellular species there are ac-tually subcellular organelles with functions analogous to the eye.The eyespots ofa group of protozoans called euglenoids, for example, contain light-absorbingmolecules that are shaded on one side by a patch of pigment.When these mole-cules absorb light, they undergo structural changes. Because light can reach themfrom one side only, a change in the light-absorbing molecule contains useful in-formation about where light is coming from. Some dinoflagellates even have asubcellular, lenslike organelle that can concentrate light on a pigment cup. It isunlikely that these single-celled protists can form an image, however, becausethey are not capable of neural processing. Rather, their eye probably functions intransmitting information about the cell’s depth in the water column, helping thecell orient itself and swim toward light.

More complex eyes have a basic unit called the photoreceptor.This is a cellthat contains a pigment capable of absorbing light.The simplest type of mul-ticellular eye, consisting of a few photoreceptor cells in a cup or cuplikearrangement, is shown in Figures 3.23a and 3.23b.This type of eye is foundin a wide diversity of taxa, including flatworms, polychaetes (segmentedworms in the phylum Annelida), some crustaceans (the shrimps, crabs, and al-lies), and some vertebrates. These organs are used in orientation and day-length monitoring (Willson 1984; Brusca and Brusca 1990). Slightly morecomplex eyes, like those illustrated in Figure 3.23c, have optic cups with anarrow aperture acting as a lens and may be capable of forming images in atleast some species.These are found in a few nemerteans (ribbon worms) andannelids (segmented worms), copepod crustaceans, and abalone and nau-tiloids (members of the phylum Mollusca). The most complex eyes (Figure3.23d) fall into two functional categories based on whether the photorecep-tor cells are arrayed on a retina that is concave, like the eyes of vertebrates andoctopuses, or convex, like the compound eyes of insects and other arthropods(Goldsmith 1990). These eyes have lenses, and in most cases are capable offorming images.

It is important to recognize that the simpler eyes we have just reviewed donot themselves represent intermediate forms on the way to more advancedstructures.The eyespots, pigment cups, and optic cups found in living organismsare contemporary adaptations to the problem of sensing light.They are not an-cestral forms. It is, however, sensible to argue that the types of eyes discussedhere form an evolutionary pathway (Gould 1983, essay 1).That is, it is conceiv-able that eyes like these formed intermediate stages in the evolution of the com-plex eyes found in vertebrates, octopuses, and insects. This is exactly whatDarwin argued in his section on organs of extreme perfection. (To learn moreabout the evolution of the eye, see Salvini-Plawen and Mayr 1977; Nilsson andPelger 1994; Quiring et al. 1994; Dawkins 1994; Donner and Maas 2004;Gehring 2004; Fernald 2004.)

Pigmented cells

Epithelial cells

Nerve fibers

Pigmentedcells

Water-filledcavity

Pigmentedlayer(retina)

Epithelium

Optic nerve

(c)

(b)

(d)

(a)

Nerve fibers

LensCornea

Lens

Iris

Cornea

Retina

Optic nerve

Figure 3.23 Variation in mol-lusc eyes (a) A pigment spot;(b) a simple pigment cup; (c) thesimple optic cup found inabalone; (d) the complex lensedeyes of a marine snail calledLittorina and the octopus. Pig-mented cells are shown in color.From Brusca and Brusca 1990.


The Argument from Biochemical “Design”

Summarizing his views on perfection and complexity in nature, Darwin wrote(1859, p. 189):

If it could be demonstrated that any complex organ existed, which couldnot possibly have been formed by numerous, successive, slight modifica-tions, my theory would absolutely break down. But I can find out nosuch case.

Creationist Michael Behe (1996), believes he has found a profusion of suchcases. Behe claims that many of the molecular machines found inside cells are ir-reducibly complex, and could not have been built by natural selection. Behewrites (p. 39):

By irreducibly complex I mean a single system composed of several well-matched, interacting parts that contribute to the basic function, where-in the removal of any one of the parts causes the system to effectivelycease functioning.

Among the examples Behe offers is the eukaryotic cilium (also known, when itis long, as a flagellum).

Figures 3.24a and 3.24b show a cross section of the stalk, or axoneme, of oneof these cellular appendages. Its main structural components are microtubules,made of proteins called and At the core of the axoneme aretwo singlet microtubules, held together by a protein bridge. Surrounding thecentral pair are nine doublet microtubules. The doublet microtubules are con-nected to the central pair by protein spokes. Neighboring doublets are also con-nected to each other by an elastic protein called nexin.The cilium is powered bythe dynein motors on the doublet microtubules.As the motors on each doubletcrawl up their neighboring doublet, they cause the entire axoneme to bend.

Here is Behe again (1998):

Cilia are composed of at least a half dozen proteins: alpha-tubulin, beta-tubulin,dynein, nexin, spoke protein, and a central bridge protein.These combine toperform one task, ciliary motion, and all of these proteins must be present forthe cilium to function. If the tubulins are absent, then there are no filaments to

b-tubulin.a-tubulin

(a) (b) (c)Outer row dynein

Inner row dyneins

B-tubule

A-tubule

Radial spoke

Central pair complex

Figure 3.24 Eukaryotic flagella (a) An electron micrograph showing a cross section througha flagellum of the single-celled alga Chlamydomonas. Scale (b) An interpretive draw-ing showing the individual components of the flagellum in (a). (c) A cross section through the fla-gellum of an eel sperm. See text for explanation. Parts (a) and (b) are from Mitchell (2000); (c) isfrom Woolley (1997).

bar = 100 nm.


slide; if the dynein is missing, then the cilium remains rigid and motionless; ifnexin or the other connecting proteins are missing, then the axoneme fallsapart when the filaments slide.

Behe finds it implausible that the cilium could have arisen by natural selection, astepwise process in which each step involves an incremental improvement overwhat came before:

[S]ince the complexity of the cilium is irreducible, then it can not have func-tional precursors. Since the irreducibly complex cilium can not have func-tional precursors it can not be produced by natural selection, which requires acontinuum of function to work. Natural selection is powerless when there isno function to select.

Once he has concluded that the cilium cannot have arisen by natural selection,Behe infers that it must have been designed.

The first thing we can say about Behe’s argument is that the eukaryotic ciliumis not, in fact, irreducibly complex. It is certainly not irreducibly complex in anevolutionary sense.This is demonstrated by organisms with cilia that are simplerin structure than the one pictured in Figure 3.24a and (b) (see Miller 1999).Figure 3.24c, for example, shows a cross section of an eel sperm’s flagellum. It isfully functional, even though it lacks the central pair of singlet microtubules, thespokes, and the outer row of dynein motors.The cilium is not even irreduciblycomplex in a mechanical sense.This is shown by a mutation in the single-celledalga Chlamydomonas known as pf14.The flagella of cells carrying this mutationlack spokes. Although the pf in pf14 stands for paralyzed flagella, the flagella ofmutant cells do still function under the right chemical conditions or on the rightgenetic backgrounds (Frey et al. 1997).

The second thing we can say about Behe’s argument is that even if the ciliumwere irreducibly complex, he would still be wrong to conclude that it cannothave functional precursors and cannot have been built by natural selection.Behe’s argument assumes that evolution by natural selection builds molecularmachines and their components from scratch, and that the individual componentproteins are useless until the entire structure has been assembled in its final form.In fact, evolution by natural selection cobbles molecular machines together frompreexisting and functional component proteins that it co-opts for new roles(True and Carrol 2002). If the components of complex molecular machines arerecruited from other jobs, then we no longer have to explain how the compo-nents were maintained by selection while the machine evolved from scratch.

Richard Lenski and colleagues (2003) showed that evolution by natural selec-tion can, in fact, build complex machines in just this way by studying populationsof digital organisms. A digital organism is a self-replicating computer program.Each of the organisms in Lenski et al.’s virtual world has a genome composed ofa series of simple instructions—low-level scraps of computer code. There aresome two dozen possible instructions in all, which can be strung together in anyorder and repeated any number of times. Most possible sequences of instructionsdo nothing. Some allow an organism to copy itself. Still others allow an organismto take numbers as inputs, perform logical functions on them, and producemeaningful outputs.The researchers started with a large population of identicalorganisms whose modest-sized genomes allowed them to replicate themselves

Intelligent Design Theory is amodern version of the Argu-ment from Design.


but not to perform logical functions. Replication was imperfect, meaning thatoccasionally one or more of the instructions in the genome was replaced withanother chosen at random, or an instruction was inserted or deleted at random.The organisms had to compete for the chance to run their instructions and re-produce. If an organism appeared that could correctly perform one or more log-ical functions, it was rewarded with additional running time.

The capacity to perform simple logical functions evolved first. Complex func-tions evolved later, building on the simple ones and co-opting them for new pur-poses. In genomes capable of performing the most complex function, many ofthe individual instructions were crucial; deleting them destroyed the organism’sability to perform the function. Intriguingly, some of the mutations on the pathto the most complex function were initially harmful.That is, they disrupted themachinery for one or more simple functions. But they set the stage for later mu-tations that helped assemble new and more complex functions from old.

A striking demonstration of gene co-option in real organisms comes from thecrystallins of animal eye lenses (True and Carrol 2002). Crystallins are water-solubleproteins that form densely packed, transparent, light-refracting arrays constitutingabout a third of the mass of the lens.Animal eyes contain an astonishing diversity ofcrystallins (Figure 3.25). Some, such as the and crystallins, are widely distrib-uted across the vertebrates and must have evolved early. These ancient crystallinsevolved from duplicate copies of genes for proteins with other functions. Othercrystallins are unique to particular taxa and must have evolved recently. Most ofthese recently evolved crystallins are similar or identical to enzymes that functionoutside the eye. Some, in fact, are enzymes that function outside the eye.That is, insome cases a single gene encodes a single protein that functions as an enzyme insome tissues and as a crystallin in the lens.The crystallin in chickens, for instance,is a metabolic enzyme called lactate dehydrogenase B.The antifreeze proteins in theblood of Arctic and Antarctic marine fishes provide additional examples of proteinsco-opted for new functions (Baardsnes and Davies 2001; Fletcher et al. 2001).

Crystallins and antifreeze proteins have simple jobs as proteins go.They haveswitched roles during their evolutionary history, but have not been incorporatedinto complex molecular machines. However, most of the components of themolecular machines Behe cites are homologous to proteins with other cellularfunctions.The microtubules and dyneins of the eukaryotic cilium, for example,are similar to components of the spindle apparatus employed in cell division.Andwork on simple examples such as crystallins and antifreeze proteins has paved theway for progress on more challenging problems. Researchers have begun recon-structing the evolutionary origins of complex molecular machines and metabol-ic pathways. Examples include the Krebs citric acid cycle (Meléndez-Hevia, et al.1996; Huynen, et al. 1999), the cytochrome c oxidase proton pump (Musser andChan 1998), the blood-clotting cascade (Krem and Di Cera 2002), and variousbacterial flagella (Pallen and Matzke 2006).

Behe is right that we have not yet worked out in detail the evolutionary historiesof the molecular machines he takes as examples of irreducible complexity.He wouldhave us give up and attribute them all to miracles. But that is no way to makeprogress. Ironically, Behe began claiming that the origins of cellular biochemistrywould never be deciphered just as the techniques and data required to do so werebecoming available.Among these are automated DNA sequencers and the whole-genome sequences they are providing.We predict that in the coming decades all ofBehe’s examples of irreducible complexity will yield to evolutionary analysis.

H

bga


Other ObjectionsHere are four additional arguments that creationists use regularly, with responsesfrom an evolutionary perspective (see Gish 1978; Kitcher 1982; Futuyma 1983;Gould 1983 essays 19, 20, 21; Dawkins 1986; Swinney 1994):

1. Evolution by natural selection is unscientific because it is not falsifi-able and because it makes no testable predictions. Each of Darwin’s fourpostulates is independently testable, so the theory meets the classical criterion thatideas must be falsifiable to be considered scientific.Also, the claim that evolutionarybiologists do not make predictions is not true. Paleontologists routinely (and cor-rectly) predict which strata will bear fossils of certain types (a spectacular example

ancestral protein function

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� small heat shock proteins � related to bacterial stress protein � NADPH-dependent reductase � arginosuccinate lyase � � enolase � glyceraldehyde phosphate dehydrogenase � lactate dehydrogenase � similar to bacterial ornithine deaminase � aldehyde dehydrogenase alcohol dehydrogenase � hydroxyacyl-CoA dehydrogenase L aldehyde dehydrogenase S glutathione S-transferase � aldehyde dehydrogenase O similar to yeast TSFIdrosocrystalin insect cuticle protein J1 similar to chaperonin/60 kd hsp

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Figure 3.25 Gene co-option in the crystallins of animal eye lenses Crystallin proteins are major components of the lensesin animal eyes.All are derived from proteins with other functions. In some cases crystallins are encoded by duplicates of thegenes for the proteins they are derived from; in other cases crystallins are encoded by the same genes.This phylogeny shows theevolutionary relationships among a variety of animals.The color-coded Greek letters indicate the crystallins found in the lensesof each animal.The table lists the proteins the various crystallins are derived from. Redrawn from True and Carroll 2002.


was that fossil marsupial mammals would be found in Antarctica); Peter Grant andRosemary Grant have used statistical techniques based on evolutionary theory tocorrectly predict the amount and direction of change in finch characteristics duringselection events in the late 1980s and early 1990s (Grant and Grant 1993,1995).Sci-entific creationism, on the other hand, amounts to an oxymoron; in the words ofone of its leading advocates, Dr. Duane Gish (1978, p. 42):“We cannot discover byscientific investigations anything about the creative processes used by God.”

2. Because Earth was created as little as 6,000–8,000 years ago, therehas not been enough time for Darwinian evolution to produce the adap-tation and diversity observed in living organisms. Creation scientists presentshort-Earth theories and argue that most geological landforms and strata resultedfrom the flood during the time of Noah. (For example, see Gish 1978 and Swinney1994.) Most simply disbelieve the assumptions behind radiometric dating and denythe validity of the data.The assumption of uniformitarianism in the evolution of lifeand landforms is also rejected by creation scientists.Again, we quote Gish (1978, p.42): “We do not know how God created, what processes He used, for God usedprocesses which are not now operating anywhere in the natural universe”(emphasis original).

The assumptions of radiometric dating have been tested, however, anddemonstrated to be correct. Radiometric dating has demonstrated that rock stra-ta differ in age, and that Earth is about 4.6 billion years old.

3. Because organisms progress from simpler to more complex forms,evolution violates the Second Law of Thermodynamics. Although theSecond Law has been stated in a variety of ways since its formulation in the late19th century, the most general version is:“Natural processes tend to move toward astate of greater disorder” (Giancoli 1995).The Second Law is focused on the con-cept of entropy.This is a quantity that measures the state of disorder in a system.TheSecond Law, restated in terms of entropy, is “The entropy of an isolated systemnever decreases. It can only stay the same or increase” (Giancoli 1995).

The key to understanding the Second Law’s relevance to evolution is the word“isolated.”The Second Law is true only for closed systems. Organisms, however,live in an open system: Earth, where photosynthetic life-forms capture the radi-ant energy of the Sun and convert it to chemical energy that they and other or-ganisms can use. Because energy is constantly being added to living systems, theSecond Law does not apply to their evolution.

A similar objection is William Dembski’s (2002) assertion that natural selec-tion cannot lead the evolution of complex genetic information because it is nobetter than a random search. He stakes this claim on a set of results in theoreticalcomputer science called the No Free Lunch Theorems.These show that averagedover all possible problems, no set of rules for finding a solution is better than anyother, including random trial and error. But as Allen Orr (2002) points out, theNo Free Lunch Theorems do not apply to Darwinian evolution, because Dar-winian evolution is not a search for a predefined target. It is, instead,“sheer colddemographics.” Genomes that make more copies of themselves become morecommon; genomes that make fewer copies disappear.

4. No one has ever seen a new species formed, so evolution is un-proven. And because evolutionists say that speciation is too slow to bedirectly observed, evolution is unprovable and thus based on faith.Although speciation is a slow process, it is ongoing and can be studied. InChapter 2 we discussed an example: Eastern versus western greenish warblershave diverged as they expanded their range around the Tibetan Plateau, to the


point that the two forms act like different species where they meet in the north.Chapter 16 will cover other experimental and observational studies of speciationin action.

Also, it is simply incorrect to claim that the only way to prove something hap-pened is to observe it directly. Here is a rather contrived example: Imagine thatyou and two friends are stranded on an otherwise deserted island.You find onefriend face down with a knife in his back, and you know that you did not do it.Although you did not directly observe the murder, you can infer the identity ofthe guilty party.We make inferences of this sort all the time in everyday life.Theyare common in science as well.We cannot observe atoms directly, for example,but there is considerable evidence on which to infer that they exist.

What Motivates the Controversy?For decades, evolution by natural selection has been considered one of the best-documented and most successful theories in the biological sciences. Many scien-tists see no conflict between evolution and religious faith (Easterbrook 1997;Scott 1998), and many Christians agree. In 1996, for example, Pope John Paul IIacknowledged that Darwinian evolution was a firmly established scientific resultand stated that accepting Darwinism was compatible with traditional Christianunderstandings of God.

If the fact of evolution and the validity of natural selection are utterly uncon-troversial, and if belief in evolution is compatible with belief in God, then whydoes the creationist debate continue?

During a discussion about whether material on evolution should be included inhigh school textbooks, a member of the Alabama State School Board named DavidByers said, “It’s foolish and naive to believe that what children are taught aboutwho they are, how they got here, doesn’t have anything to do with what they con-clude about why they are here and what their obligations are, if, in fact, they haveany obligations, and how they should live” (National Public Radio 1995). Thisstatement suggests that, for some creationists, the controversy is not about the va-lidity of the scientific evidence or its compatibility with religion. Instead, the con-cern is about what evolution means for human morality and behavior.

Creationists and evolutionists, it is safe to say, share the desire that childrenshould grow up to become morally responsible adults. Creationists fight evolu-tion because they believe it is morally dangerous. Evolutionary biologists, onthe other hand, tend to believe that morality and moral guidance derive fromsources outside of biology, and that children should learn what science showsus about how we and Earth’s other living things came to be.

Before Darwin began to work on the origin of species,many scientists had become convinced that specieschange through time. The unique contribution madeby Darwin and Wallace was to realize that the process ofnatural selection provided a mechanism for this pattern,which Darwin termed descent with modification.

Evolution by natural selection is the logical out-come of four facts: (1) Individuals vary in most or all

traits; (2) some of this variation is genetically based andcan be passed on to offspring; (3) more offspring areborn than can survive to breed, and of those that dobreed, some are more successful than others; and (4)the individuals that reproduce the most are a nonran-dom, or more fit, subset of the general population.This selection process causes changes in the geneticmakeup of populations over time, or evolution.

Summary


Questions1. In everyday English, the word “adaptation” means an

adjustment to environmental conditions. How is theevolutionary definition of adaptation different from theeveryday English sense?

2. a. Describe Darwin’s four postulates in your ownwords. What would have happened in the snapdrag-on experiment if any of the four had not been true?

b. If Darwin’s four postulates are true for a given pop-ulation, is there any way that evolution can not hap-pen? What does this imply about whether evolutionis or is not occurring in most populations today?

3. Think about how the finch bill data demonstrate Dar-win’s postulates.a. What would Figure 3.9 have looked like if bill

depth was not variable?b. What would Figure 3.14 look like if bill depth was

variable but the variation was not heritable?c. In Figure 3.10, why is the line drawn from 1978

data, after the drought, higher on the y-axis than theline drawn from 1976 data, before the drought?

4. According to the text, it is legitimate to claim that mostfinches died from starvation during the 1977 droughtbecause “there was a strong correspondence betweenpopulation size and seed availability.” Do you acceptthis hypothesis? If so, why don’t the data in Figure 3.12show a perfect correspondence between when seedavailability started declining and when population sizestarted declining?

5. A common creationist criticism of the finch study is,“But it’s just a little change in beak shape. Nothing re-ally new has evolved.” Or put a different way, “It’s justmicroevolution and not macroevolution.” The finchteam continues to spend a great deal of effort on theirproject—traveling thousands of miles to the remoteGalápagos every year, just to try to band an entire pop-ulation of birds and all their nestlings and measure theirbills. How would you respond to the creationists’ criti-cisms? Do you think the ongoing 30-year-effort of thefinch bill project has been worthwhile? Is it useful totry to document microevolution, and does it tell usanything about how macroevolution might work?

6. Suppose that you are starting a long-term study of apopulation of annual, flowering plants isolated on asmall island. Reading some recent papers has convincedyou that global warming will probably cause long-termchanges in the amount of rain the island receives. Out-line the observations and experiments you would needto do in order to document whether natural selectionoccurs in your study population over the course ofyour research. What traits would you measure, andwhy?

7. At the end of an article on how mutations in variablenumber tandem repeat (VNTR) sequences of DNAare associated with disease, Krontiris (1995, p. 1683)writes:“the VNTR mutational process may actually bepositively selected; by culling those of us in middle ageand beyond, evolution brings our species into fightingtrim.”This researcher proposes that natural selection onhumans favors individuals who die relatively early inlife. His logic is that the trait of dying from VNTR mu-tations is beneficial and should spread because the pop-ulation as a whole becomes younger and healthier as aresult. Can this hypothesis be true, given that selectionacts on individuals? Explain.

8. Describe three major objections to Darwin’s theory inthe 19th century that were eventually resolved by dis-coveries by other scientists in the 20th century. Whatdoes this tell us about the utility of a theory that cannotyet answer all questions but that appears to be betterthan all alternative theories?

9. Many working scientists are relatively uninterested inthe history of their fields. Did the historical develop-ment of Darwinism, reviewed in Section 3.6, help youunderstand the theory better? Why or why not? Doyou think it is important for practicing scientists tospend time studying history?

10. a. Describe Behe’s argument of “irreducible complex-ity.” Is it a logical argument? How does it apply tothe bacterial flagellum or the vertebrate eye?

b. Opponents of intelligent design refer to irreduciblecomplexity as an “argument from personal in-credulity” (i.e.,“I personally can’t imagine how thiscould have evolved, so it must not have evolved.”).What is the logical flaw of an argument from per-sonal incredulity? Do you think it is fair to charac-terize irreducible complexity in this way?

11. In 1995, the Alabama School Board, after reviewinghigh school biology texts, voted to require that this dis-claimer be posted on the inside front cover of the ap-proved book (National Public Radio 1995):

This textbook discussed evolution, a controversialtheory some scientists present as a scientific explana-tion for the origin of living things, such as plants, an-imals, and humans.No one was present when life firstappeared on Earth; therefore, any statement aboutlife’s origins should be considered as theory, not fact.

Do you accept the last sentence in this statement?Does the insert’s point of view pertain to other scientif-ic theories, such as the Cell Theory, the Atomic Theory,the Theory of Plate Tectonics, and the Germ Theory ofDisease?


Exploring the Literature

14. During the past 50 years, hundreds of viruses, bacteria,fungi, and insects have evolved resistance to drugs, her-bicides, fungicides, or pesticides.These are outstandingexamples of evolution in action. In several of thesecases, we know the molecular mechanisms of the evo-lutionary changes involved. To explore this topic fur-ther, look up the following papers. Think about howthe evidence from these studies compares with the evi-dence for evolution in Darwin’s finches and HIV.Anthony, R. G.,T. R.Waldin, J.A. Ray, S.W. J. Bright, and P. J. Hussey.

1998. Herbicide resistance caused by spontaneous mutation of thecytoskeletal protein tubulin. Nature 393: 260–263.

Cohen, M. L. 1992. Epidemiology of drug resistance: Implicationsfor a post-antimicrobial era. Science 257: 1050–1055.

Davies, J. 1994. Inactivation of antibiotics and the dissemination of re-sistance genes. Science 264: 375–382.

Van Rie, J.,W. H. McGaughey, D. E. Johnson, B. D. Barnett, and H.VanMelleart. 1990. Mechanism of insect resistance to the microbial in-secticide Bacillus thuringiensis. Science 247: 72–74.

15. It seems unlikely that selection of traits “for the good ofthe species” can occur. However, it now appears thatunder certain conditions, such as small group size andvery low migration,group selection of altruistic behaviorsmay in fact be possible. Look up the following papers tolearn more about this topic:Avilés, L., and P. Tufino. 1998. Colony size and individual fitness in

the social spider Anelosimus eximius. American Naturalist 152:403–418.

Borrello, M.E. 2005.The rise, fall, and resurrection of group selection.Endeavour 29 (1):43–47.

Ono, S., and K. Misawa, and K.Tsuji. 2003. Effect of group selectionon the evolution of altruistic behavior. J.Theor. Biol. 220 (1):55–66.

16. For detailed critical discussions of Intelligent DesignCreationism, see:Miller, K. R. 1999. Finding Darwin’s God:A Scientist’s Search for Com-

mon Ground Between God and Evolution. New York: Cliff StreetBooks.

Pennock, R.T., ed. 2001. Intelligent Design Creationism and Its Crit-ics. Cambridge, MA:The MIT Press. (See especially Chapter 10by M. J. Behe, Chapter 11 by Philip Kitcher, and Chapter 12 byM. J. Brauer and D. R. Brumbaugh.)

Young, M., and T. Edis (editors). 2004. Why Intelligent Design Fails:AScientific Critique of the New Creationism. New Jersey: Rutgers Uni-versity Press.

17. For new hypotheses about the evolution of Behe's twomost famous examples of "irreducibly complex" sys-tems, the flagellum and the blood clotting cascade, see:Aird, W.C. 2003. Hemostasis and irreducible complexity. J. Thromb.

Haemost. 1 (2): 227–230.

Hanumanthaiah, R., K. Day, and P. Jagadeeswaran. 2002. Comprehen-sive analysis of blood coagulation pathways in teleostei: evolution ofcoagulation factor genes and identification of zebrafish factor VIIi.Blood Cells Mol. Dis. 29 (1): 57–68.

Davidson, C.J., R.P. Hirt, K. Lal, P. Snell, G. Elgar, E.G.Tuddenham,and J.H. McVey. 2003. Molecular evolution of the vertebrate bloodcoagulation network. Thromb. Haemost. 89 (3): 420–428.

Li, J.Y., and C.F.Wu. 2005. New symbiotic hypothesis on the originof eukaryotic flagella. Naturwissenschaften 92 (7): 305–309.

Mitchell, D.R. 2004. Speculations on the evolution of 9+2 organellesand the role of central pair microtubules. Biol. Cell 96 (9): 691–696.

18. For the full court decision of the 2005 Dover SchoolBoard intelligent design case (Kitzmiller vs. DoverSchool District), see:www.pamd.uscourts.gov/kitzmiller/kitzmiller_342.pdf

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12. In the final opinion on the Dover School Board intelli-gent design trial of 2005 (Kitzmiller v. Dover), DistrictCourt Judge John E. Jones wrote (in part):“To be sure,Darwin’s theory of evolution is imperfect.However, thefact that a scientific theory cannot yet render an expla-nation on every point should not be used as a pretext tothrust an untestable alternative hypothesis grounded inreligion into the science classroom or to misrepresentwell-established scientific propositions.”

Do you agree with Judge Jones? Why or why not?[See #18 for more information on this trial.]

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