and studied in intact cells and in mem-branes from various tissues (S); bind-ing can be altered or destroyed bytreating cells with free or agarose-boundenzymes (5); the receptors are notdetectable in intracellular membranes(S); adenylate cyclase activity in iso-lated membranes can be perturbed di-rectly by physiological concentrationsof insulin (6); and insulin receptorshave now been extracted and purifiedfrom cell membranes (7). Althoughthese studies are consistent with andfurther expand the observations madewith insulin-agarose, it is very mislead-ing to suggest (as Katzen and Vlahakesdo in their first paragraph) that anysuch studies are based on a "basicpremise" which is "justified" by the in-sulin-agarose studies. By analogy, thegrowing number of important studiesconcerning receptors for many peptide,cholinergic, and adrenergic hormones,and their localization to cytoplasmicmembranes, are not based on studieswith insoluble hormones.A "unitary concept" of insulin ac-

tion should in principle be viewed inthe same way we evaluate the actionof other hormones. In this respect thebasic but still unanswered question iswhether all of the metabolic effects ofinsulin can be explained on the basisof a single, unique, and fundamentalbiochemical event. This question is de-pendent not on interpretations of exist-ing insulin-agarose studies, but on abetter understanding of the detailedbiochemical processes which follow theinitial insulin-receptor interaction.

I take this opportunity to presentadditional evidence for the inherentactivity of new and interesting insulin-agarose derivatives recently prepared inthis laboratory. Insulin attached toagarose through very large macro-molecular "arms," which consist ofbranched copolymers of poly-L-lysine-L-alanine can be demonstrated to bebiologically active under conditionswhere no significant free insulin is re-leased into the medium (Table 1).These derivatives may be especially use-ful because of the large distance whichseparates the insulin from the agarosebackbone, and because of -the greatstability of the coupled insulin whichresults from the multipoint linkage ofthe copolymer to the agarose backbone.

PEDRO CUATRECASASDepartment of Pharmacology andExperimental Therapeutics, JohnsHopkins University School ofMedicine, Baltimore, Maryland 21205

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References

1. P. C'uatrecasas, Proc. Nat. Acad. Sci. U.S.A.63, 450 (1969).

2. T. Oka and Y. J. Topper, ibit. 68, 2066 (1971);Nature New Biol. 239, 216 (1972); L. M.Blatt and K. H. Kim, J. Biol. Chern. 246,4895 (1971): R. W. TLirkington, Biochein.Biophys. Res. Commun. 41, 1362 (1970).

3. K. J. Armstrong, M. W. Noall, J. E. Stouffer,Bioclhem. Biop/hys. Res. Comin)un. 47, 354(1972); F. Suzuki, Y. Daikuhara, M. Ono,Endlocrinology 90, 1220 (1972).

4. P. Cuatrecasas, Fed. Proc. SY)lp., in press.5. , Proc. Nat. Acad. Sci. U.S.A. 68, 1264

(1971); J. Biol. Chem. 246, 6522, 6532, 7265(1971); P. Freychet, J. Roth, D. M. Neville,Biochemn. Biophys. Res. Co,ztnun. 43, 400 (1971);

Proc. Nat. Acad. Sci. U.S.A. 68, 1833 (1971); P.D. R. House and M. J. Weidemann, Biochem.Biophys. Res. Commun. 41, 541 (1970); T.Kono and F. W. Barham, J. Biol. Chem. 246,6210 (1971); I. D. Goldfine, J. D. Gardner,D. M. Neville, ibid. 247, 6919 (1972); R. M.M. El-Allany and J. Gliemann, Biochim. Bio-phys. Acta 273, 97 (1972); J. M. Hammond, L.Jarett, I. K. Mariz, W. H. Daughaday, Bio-cheit. Biophys. Res. Conmiiiun. 49, 1122 (1972).

6. G. Illiano and P. Cuatrecasas, Science 175, 906(1972); K. D. Hepp, Fed. Eur. Biochein. Soc.FEBS Lett. 12, 263 (1971); ibid. 20, 191 (1972).

7. P. Cuatrecasas, Proc. Nat. Acad. Sci. U.S.A.69, 318 (1972); ibid., p. 1277; J. Biol. Cheni.247, 1980 (1972).

20) January 1973 .

Generation Time and Genomic Evolution in Primates

It is widely accepted among thosewho study evolution at the molecularlevel that time is a major factor deter-mining the degree of sequence differ-ence among the homologous macro-molecules of different species. Whetherdone on the globins (I), cytochromes c(2), fibrinopeptides (3), albumins (4-7),lysozymes (8), or DNA's (9, 10),such studies have generally shown astrong correlation between the degree ofsequence difference and the time thathas elapsed since the two species beingcompared last shared a common ances-tor. Substantial disagreement persists,though, on the question of whether thetime factor should be measured in termsof astronomical time or generationlength (9-12). These conflicting hypoth-eses have been subjected to directtest, and we here review evidence de-veloped in such tests which stronglysupports the astronomical time hypoth-esis.

It is important at the outset to makeclear the distinction between measuringabsolute and relative rates of macro-molecular evolution. We believe thatthe failure to make that distinction hasled others (9-12) unwittingly to favorthe generation time hypothesis. To mea-sure absolute rates of macromolecularevolution requires known times of diver-gence between living species and isthus completely dependent on a de-tailed and properly interpreted fossilrecord. The method is illustrated bythe following example. If it is knownthat the albumins of two species A andB differ in sequence by x amino acidreplacements and that the A and Blineages diverged t million years ago,the average rate of albumin evolution inthis case is x/t amino acid replacementsper million years of separation. Al-though t is sometimes known precisely,this will not be true for most absoluterate measurements. It is relatively easy

107~ , - . Tree shrews

16.7b { , ; < > r Other prosimlons

6.5 i -C Old World monkeys3.3

c Apes and man

Time 65 50 40 30 20 10 0TIme Millions of years ago

Fig. 1 (left). Phylogenetic relationships among three hypothetical living species, A, B,and C. The most recent common ancestor of A and B lived at time T2, and the most re-cent common ancestor of all three species lived at time T1; a and b are the amounts ofsequence change (measured in amino acid replacements, immunological distance units,or nucleotide replacements) along the A and B lineages from T. until the present. Theexperimental A-B difference is assumed to be a + b; a and b can then be calculated ifthe A-C and B-C distances are known (5). Fig. 2 (right). Number of generations(x 100) along various primate lineages according to the model of Lovejoy et al. (12).The divergence times are those used in (12); thus, we do not denote a specific diver-gence time for the tree shrews. For our calculations we have used the relationshipbetween generations per year [X(t)] and time in millions of years (t) given in (12).However, one of their equations, X2(t) = 0.216tr'5, is incorrect and should readX2(t) = 0.358r'"; we have used the latter in our calculations.

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to date fossils, but far more difficultto date divergence events.To measure relative rates of molecu-

lar evolution, on the other hand, re-quires only a knowledge of the cladistic(branching order) relationships amongthe lineages in question. Even when thefossil record has many gaps and uncer-tainties, cladistic relationships canusually be determined unambiguously.The basic strategy of the relative rate

method is outlined in Fig. 1 in terms ofthree living species (A, B, C) whose re-lationships are known from nonmolec-ular evidence. If the time of divergenceof A and B is more recent than that ofA and C or B and C, the relativeamounts of change along the A and Blineages (a, b), may then be estimatedby comparing the A-C and B-C molec-ular differences. Thus, if A is desig-nated as a primate species whose timebetween generations is long (for ex-ample, man) compared to that of an-other primate species B (for example,tree shrew or other prosimian), the gen-eration time hypothesis predicts thatmore change should have occurredalong the B lineage than along the Alineage. Thus, the critical issue can betested without any attempts at absoluterate measurements, and therefore with-out any dependence on the primate fos-sil record. Assuming, then, a mono-phyly of the modern primates relativeto any nonprimate mammal (13), wemay let C represent a modern carnivorespecies. The generation time hypothesispredicts that we should observe a great-er molecular difference between prosim-ian and carnivore than between carni-vore and human. This prediction hasbeen tested (7) by using a series ofantiserums to the albumins of severalof the Carnivora to measure the im-munological distances to various primatealbumins. We found (Table 1) that theprediction was not fulfilled. Indeed, theimmunological distance to human al-bumin (162 units) was greater than thatto any prosimian albumin: slow loris,125; lemur, 135; tarsier, 137; tree shrew,156. Thus, there is no correlation be-tween the amount of primate albuminevolution and generation length, thetwo species with the strongest contrastin generation length (man and treeshrew) having albumins very nearlyequidistant from our carnivore refer-ence points.The logical inference that must be

drawn from these data in the context ofthe particular primate-carnivore rela-tionship is that human albumin, along16 MARCH 1973

with those of the Old World monkeys(Table IA), has changed somewhatmore from the ancestral primate al-bumin sequence than have those of theprosimians, in spite of the undoubtedincrease in generation length amongthe higher primates. A more recent andhitherto unpublished study involving thequantitative precipitin technique and alarger variety of antiserums leads to asimilar conclusion (Table 1B). Andfinally, antiserums to a series of NewWorld monkey albumins indicate thatthe albumin of man or gibbon is noless changed from the ancestral catar-rhine sequence than those of the OldWorld monkeys (Table IC) (14).Now neither the above arguments

nor much of the supporting data arenew, and this puts into a curious lightthe statement of Lovejoy et al. (12):

Table 1. Three tests for the occurrence of anevolutionary slowdown in the hominoid line-age. Abbreviations: ID, immunological dis-tance; MC'F, micro-complement fixation.Primate albumin tested Mean ID

A. MC'F test with antiserums to thealbumins of four carnivore species*t

Homo sapiens 162Macaca mulatta (rhesus monkey) 166Ateles geofiroyi (spider monkey) 149Nycticebus coucang (slow loris) 125Lemur fulvus (brown lemur) 135Tarsius spectrum (tarsier) 137Tupaia glis (tree shrew) 156

B. Precipitin test with antiserums to thealbumins of seven nonprimate speciest

Homo sapiens 169Hylobates lar (gibbon) 169Macaca mulatta 169Aotus trivirgatus (owl monkey) 150Cebus capucinus (capucin monkey) 169Nycticebus coucang 143Lemur fulvus 150Tupaia glis 163

C. MC'F test with antiserums to thealbumins of five New World monkey speciest§Homo sapiens 55Hylobates lar 53Macaca mulatta 53Presbytis entellus (langur) 52

* The four carnivores were Hyaena, Genetta,Ursus, and Arctogalida. t Each purified albu-min from a carnivore, bat, or New Worldmonkey was injected into a different group offour or five rabbits, and the antiserums wereobtained after a 3-month immunization period (5).Antiserums were mixed in reciprocal proportionto their micro-complement fixation titers and usedas described elsewhere (11). The term inununo-logical distance is used in the sense described bySarich (5). For albumins, ID units are now knownto be approximately equivalent to the number ofamino acid differences. t The seven nonpri-mates were Hyaena, Genetta, Ursus, Pteropus,Tadarida, Antrozous, and Hipposideros. Percent-age cross-reaction in the precipitin test was con-verted to ID by means of a calibration curveestablished in (I1) and by Sarch (unpublishedresults obtained with albumin immune systems).§ The five New World monkeys were Cebus,Ateles, Aotus, Saguinus, and Pithecia. Resultsconsistent with this, but obtained with otherantiserums, were published in (4).

"Recalculation of the time of diver-gence of the Pongidae and Hominidaeafter correction of immunological dis-tance by inclusion of generation lengthyields minimum dates of approximately14 million years ago." Its relevance de-pends on a demonstration that genera-tion length does indeed affect rates ofprotein or DNA evolution. Lovejoyet al. did not even attempt such ademonstration and, further, ignored ex-tensive data (such as those in Table1, A and C) which we previously pre-sented (4-7) and which seem to showno generation length effect. However, amore quantitative assessment of themodel of Lovejoy et al. suggests thatthe matter is not all that simple.The equations of Lovejoy et al. can

be used to calculate the number of gen-erations that have accrued along variousprimate lineages (Fig. 2). Such ananalysis demonstrates that the particularassumptions about generation lengthmade by Lovejoy et al. result in a largeproportion of the total number of gen-erations along any primate lineage(other than that of the tree shrews)being seen as having accumulated in itsearly history. A hominoid lineage, forexample, would have gone through 10.5X 106 generations in its first 15 millionyears and only 7.8 X 106 generations inthe subsequent 50 million years. Yetany influence of generation length onthe amounts of amino acid or nucleo-tide substitution among the nontupaiidprimate lineages would be limited tothis latter period. The effect of thesestrictures on our rate tests can be il-lustrated by considering the averageimmunological distance of 122 units(7) from prosimian albumin to higherprimate albumin; according to thefigures of Lovejoy et al., this should bedistributed with 71 units along theprosimian lineage and 51 along thehigher primate lineage (15). This dis-tribution is within 1 standard deviationof the 61 units along each lineagepredicted by the astronomical timemodel; thus, even for the most ex-treme generation length contrast amongthe nontupaiid primates, the predictionsof the two hypotheses are virtually in-distinguishable statistically.However, the same assumptions about

generation length that produce thisseeming impasse also require the treeshrew lineage to have gone through fivetimes as many generations in the last 65million years as has the average higherprimate lineage [107 X 106 compared to19.3 x 106 (see Fig. 2)] and, therefore,

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to have accumulated at least five timesas many albumin amino acid substitu-tions. Now it has already been shownthat since lemurs and higher primateslast shared a common ancestor about 75immunological distance units of changehave occurred along an average higherprimate albumin lineage (7, 16). In thatsame time span, though, the tree shrewalbumin lineage should then have ac-

cumulated more than 350 units ofchange. Yet the carnivore and bat dataof Table 1, along with the mean im-munological distance of 128 units (7),from tree shrew albumin to higher pri-mate albumin allow no more than 60units of change along the tree shrewalbumin lineage (17).

In addition, a similar study has shownthe albumins of species with short gen-

eration lengths, such as rats and mice,to be no more distinct from those of a

series of carnivore albumins than are

those of man and chimpanzee (18).If no effect of generation length on

rates of genomic evolution can be seen

in cases where it should have been most

evident, then it would appear futile to

further pursue the generation lengthhypothesis. We conclude that this hy-pothesis, along with the placentationhypothesis of Goodman (19), has beenput forward to explain a phenomenonnot yet shown to have an existence in-dependent of certain assumptions con-

cerning the primate fossil record. Thebasic problem would appear to be an

unnecessary reliance on the absoluterate approach, for it is only if we ac-

cept current interpretations of the pri-mate fossil record, which suggest a di-vergence time of at least 15 to 20 mil-lion years between man and the Africanapes (14, 20), that the conclusion of a

marked slowdown in rates of albumin,hemoglobin, and DNA evolution in theevolution of the ape and human line-ages since that divergence inevitablyfollows. Any number of selective var-

iables are then available to explain this"'slowdown," for example, generationlength (10, 12) or increased placenta-tion in the higher primates (19). Wheth-er or not the slowdown actually oc-

curred, however, is a matter subject torelative rate tests-and these have con-

sistently failed to show it.The obvious corollary is that the

starting assumption of a time of diver-gence of at least 15 to 20 million years

between man and the African apes isin error, as has been pointed out on

numerous occasions (6, 7), and it re-

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mains difficult if not impossible to rec-

oncile the growing body of protein andnucleic acid data with a divergencetime of more than about 5 million years

ago between man and African apes.

Why generation length does not seem

to affect rates of protein and DNAevolution is a question that currentlyadmits of no unequivocal answer. Wedo, however, call into question the as-

sumption that mutations are, in themain, errors of DNA replication, andpropose the following hypothesis: most

protein and nucleic acid evolution isdue to the random fixation of nucleotidesubstitutions which occur as a result ofprocesses other than DNA replication,that is, presumably continuous ones

such as DNA repair (21). We furthersuggest that selective control of any

such processes must be very finelytuned indeed, for it provides a positiveregulation of the input of variabilityand, therefore, of the scope of popula-tional response to changing environ-mental conditions.

VINCENT M. SARICHDepartments of Anthropology andBiochemistry, University ofCalifornia, Berkeley 94720

ALLAN C. WILSON*Department of Biochemistry,University of California, Berkeley

References and Notes

1. E. Zuckerkandl and L. Pauling, in Horizonsin Biochemistry, M. Kasha and B. Pullman,Eds. (Academic Press, New York, 1962), p.

189; in Evolving Genes and Proteins, V.Bryson and H. J. Vogel, Eds. (AcademicPress, New York, 1965), p. 97; G. Air, E. 0.

P. Thompson, B. J. Richardson, G. B. Shar-man, Nature 229, 391 (1971); M. Kimuraand T. Ohta, J. Mol. Evol. 1, 1 (1971).

2. W. M. Fitch and E. Margoliash, Science lS5,279 (1967); W. M. Fitch, J. Mol. Evol. 1,84 (1971).

3. R. F. Doolittle and B. Blomback, Nature 202,147 (1964); R. E. Dickerson [V. Mol. EvoL1, 26 (1971)] provides an extensive discussionof rates of evolution in all of the aboveproteins.

4. V. M. Sarich and A. C. Wilson, Proc. Nat.Acad. Sci. U.S.A. S8, 142 (1967); G. C.Gorman, A. C. Wilson, M. Nakanishi, Syst.Zool. 20, 167 (1971); D. G. Wallace, L. R.Maxson, A. C. Wilson, Proc. Nat. Acad. Sci.U.S.A. 68, 3127 (1971).

5. V. M. Sarich, Syst. Zool. 18, 286 (1969); ibid.,p. 418.

6. V. M. Sarich and A. C. Wilson, Science 158,

1200 (1967); Proc. Nat. Acad. Scd. U.S.A. 63,1088 (1969); V. M. Sarich, in Perspectives on

Human Evolution, S. L. Washburn and P. C.Jay, Eds. (Holt, Rinehart, & Winston, NewYork, 1968), p. 94; in Climbing Man's FamilyTree, T. D. McCown and K. A. R. Kennedy,Eds. (Prentice-Hall, Englewood Cliffs, N.J.,1972), p. 450.

7. V. M. Sarich, in Old World Monkeys, J. R.Napier and P. H. Napier, Eds. (AcademicPress, New York, 1970), p. 175.

8. E. M. Prager, N. Arnheim, G. A. Mross,A. C. Wilson, J. Biol. Chem. 247, 2905 (1972).

9. C. D. Laird, B. L. McConaughy, B. J.McCarthy, Nature 224, 149 (1969).

10. D. E. Kohne, Quart. Rev. Biophys. 3, 327(1970).

11. V. M. Sarich and A. C. Wilson, Science 154,1563 (1966); E. M. Prager and A. C. Wilson,J. Biol. Chem. 246, 7010 (1971).

12. C. 0. Lovejoy, A. H. Burstein, K. G. Heiple,Science 176, 803 (1972).

13. It might be argued here that in assumingprimate monophiyly and not specific divergencetimes within the primates we are rejectingone paleontologically based conclusion (thetimes involved) in favor of another (thecladistic relationships of the taxa involved)with no substantive reason for making sucha choice. The answer lies in the knowledgethat cladistic conclusions are generally basedon a summation of difference-similarity judg-ments made on a variety of anatomical char-acters which can, to a large extent, beinterpreted evolutionarily without reference tothe fossil record.

14. T. Uzzell and D. Pilbeam [Evolution 25,615 (1971)1 have criticized this type of ratetest as inherently insensitive. While the pointthey make-that- phenetic underestimation ofphyletic distance would reduce the sensitivityof rate tests-is certainly valid, this does notget at the question of the degree of Insensitiv-ity introduced. We have dealt with this matterand point to the actual data which do indi-cate some albumins as more changed, andsome as less changed, than others and, moreimportant, show such differences in a quan-titatively consistent fashion. For example,Aotus albumin Is less changed than that ofCebus, and by about the same amount,whether the reference albumins be those ofthe catarrhines, prosimians, carnivores, orbats [(7) and this report]. Similarly, Ursusalbumin is less changed than those of othercanoid and pinniped carnivores, and again byabout the same amount, whether the referencealbumin is canoid, pinniped, feloid, or pri-mate (5).

15. In these comparisons we have assumed thatthe number of amino acid substitutions alonga lineage is proportional to the number ofgenerations along it. According to (12), thenumber of generations along a nontupaiidprosimian lineage in the last 65 million yearsis 27.2 X 106 and the corresponding figure foran average higher primate (catarrhine) lineageis 19.3 X 106 (Fig. 2). The "expected" distri-bution is then (27.2 /45.5) X 122 =71 for theprosimian lineage and 122-71 =51 for thecatarrhine lineage.

16. If A represents the set of prosimian species(Nycticebus, Lemur, and Tarsius) in Table 1,B the set of higher primate species, and Cthe set of carnivore and bat species in thetable, then with the logic outlined in Fig. 1one can calculate the amount of albuminevolution that has taken place along theaverage higher primate lineage, as follows.The mean A-B albumin distance is 122 units,the A-C distance is 138 units, and the B-Cdistance is 166 units. Thus a + b = 122 anda-b =-28; therefore a = 47 and b = 75.It is, of course, possible that this evolutionaryconservatism of lemuriform, lorisiform, andtarsier albumins has a selective rather than astatistical basis. One could, for example, notethat nocturnal primates (Nycticebus, Loris,Galago, some Lemur spp., Tarsius, Aotus)tend to have "conservative" albumins, andlook for a selective factor associated withsuch an existence. Or one could argue that,as "higher" primates tend to have somewhatmore changed albumins, the prosimian-anthro-poid transition briefly selected for more rapidalbumin evolution. What one cannot show isany slowdown in anthropoid albumin evolution.

17. In this case A can be the tree shrew, and Band C as in (16); a + b = 128 and a-b =-7(from Table 1). Thus a = 60 and b = 68.

18. The generation time hypothesis was originallyprompted by the very large Rattus-Mus differ-ence shown in DNA hybridization studies,coupled with a presumed recent divergencebetween the two genera (9, 10). The corre-sponding Homo-Pan difference is some tenfoldsmaller, and the albumin differences in thetwo pairs are approximately in the same pro-portion. Nevertheless, if an experimental ap-proach identical to that presented here isused, rat and mouse albumins cannot be seenas more changed than those of man andchimpanzee [V. M. Sarich, Blochem. Genet.7, 205 (1972)1.

19. M. Goodman, Hum. Blol. 33, 131 (1961).

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20. L. S. B. Leakey, Proc. Nat. Acad. Sci. U.S.A.67, 746 (1970); E Simons, Primate Evolution(Macmillan, New York, 1972); B. Kurten,Not From thte Apes (Pantheon, New York,1972).

21. E. M. Witkin, Annu. Rev. Microbiol. 23, 487(1969); J. E. Cleaver, J. Invest. Dermatol. 54,181 (1971).

22. We thank S. L. Washburn, B. N. Ames, andC. 0. Lovejoy for helpful discussions. Sup-

Fragile EcosystemsIn their plea for the preservation of

large areas of tropical rain forest,Gomez-Pompa et al. (1) emphasizethat "if we wait for a generation toprovide abundant evidence [of the vul-nerability of the rain-forest ecosystem],there probably will not be rain forestsleft to prove it." Having been inter-ested for several years in the problemof mass extinctions (2), we shouldlike to verify the soundness of theirview from the paleontologist's perspec-tive. In a sense, the documentationwhich they seek in order to elicitmassive international action towardconserving the tropical biota has beenprovided by the fossil record. We havenoted previously, following Sanders (3),that in its high diversity the tropicalecosystem is analogous to offshoremarine assemblages which underwentradical reorganizations in communitystructure, especially at the end ofDevonian and Permian time. Nearshoreassemblages of lower diversity-perhapsanalogous to the temperate-zone forestswhich have been resilient to intensiveand extensive agricultural exploitation-have been much more stable through-out geologic time.By contrast, as Gomez-Pompa et al.

indicate in their first paragraph, neon-tologists have tended to believe that the

ported in part by NSF grants GB-20750 andGB-13119 and by a fellowship award toA.C.W. from the J. S. Guggenheim MemorialFoundation. Pteroputs and Hipposideros werecollected on the Alpha Helix expedition toNew Guinea in 1969, and Antrozous andTadarida were collected locally by P. Leitner.

* Present address: Department of Zoology, Uni-versity of Nairobi, Kenya.

21 July 1972; revised 4 January 1973

more diverse a community is, the morestable it should be-at least if stabilityis defined in terms of resistance to theeffects of fluctuations in the number ofindividuals of a constituent species(such fluctuations comprehending alsothe total disappearance of a species)(4). We have postulated (2) that massextinctions primarily affecting speciesbelonging to assemblages of high di-versity came about because these taxa,having lived for many millions of yearsin a predictable environment wherethere was little selection for genetic orphysiological flexibility, were vulner-able to changes in the physical environ-ment, such as the shrinking of the seasduring periods of mountain building(5). Our postulate of loss of geneticpolymorphism has recently been chal-lenged by workers who have foundthat species of several different phylafrom the deep sea, one of the mostdiverse ecosystems and apparently oneof the most predictable environmentson the globe, show as high a level ofgenetic variability as do species fromless predictable environments (6).[Other studies, however, indicate thatgenetic variability among species of theClass Bivalvia decreases along a gradi-ent from less predictable to more pre-dictable environments (7).] Among

tropical plants, vulnerability to physicalstress appears to result primarily fromthe loss of adaptations for dispersaland dormancy. Identification of theexact cause of mass extinctions is, how-ever, comparatively unimportant in thepresent context; our primary purposeis to reiterate that, although the activi-ties of man which destroy tropical rainforests are different from the naturalforces that destroyed diverse marinebiotas of the geologic past, the effectsare likely to be the same. We believethat the lesson of earth history is thathighly diverse ecosystems in physicallypredictable environmental regimes arein fact very fragile and require respectand care if they are to be preserved.

PETER W. BRETSKYSARA S. BRETSKY

JEFFREY LEVINTONDepartment of Earth and SpaceSciences, State University of NewYork, Stony Brook 11790

DOUGLAS M. LORENZDepartment of Paleobiology,U.S. National Museum, SmithsonianInstitution, Washington, D.C. 20560

References and Notes

1. A. G6mez-Pompa, C. Vizquez-Yanes, S.Guevara, Science 177, 762 (1972).

2. P. W. Bretsky, ibid. 161, 1231 (1968);and D. M. Lorenz, Geol. Soc. Amer. Bull. 81,2449 (1970); Proc. North Amer. Paleontol. Con-vention, E, 522 (1970).

3. H. L. Sanders, Amer. Natur. 102, 243 (1968).4. R. H. MacArthur, Ecology 36, 533 (1955).5. R. C. Moore, Bull. Mus. Comp. Zool. 112,

259 (1954); N. D. Newell, Geol. Soc. Amer.Spec. Paper 89, 63 (1967); E. G. Kauffman,Proc. North Amer. Paleontol. Convention, F,612 (1970).

6. T. J. M. Schopf and J. L. Gooch, J. Geol.80, 481 (1972).

7. J. Levinton, unpublished data.8. Supported by NSF grants GA-25340 to P.W.B.,

GB-27441 to A. R. Palmer, and GA-32421 toJ.L.

18 October 1972

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Generation Time and Genomic Evolution in PrimatesVincent M. Sarich and Allan C. Wilson

DOI: 10.1126/science.179.4078.1144 (4078), 1144-1147.179Science 

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