INTEGR. CotoP. BIOL., 43:522-530 (2003)

On Homology of Arthropod Compound Eyes'

TODD H. OAKLEY 2

Ecology Evolutioni and Marine Biology, University of California-Santa Barbara, S'anzta Barbara, Califonzia 93106

SyNopsis. Eyes serve as models to understand the evolution of complex traits, with broad implications forthe origins of evolutionary novelty. Discussions of eye evolution are relevant at miany taxonomic levels,especially within arthropods where compound eye distribution is perplexing. Either compound eyes werelost numerous times or very similar eyes evolved separately in multiple lineages. Arthropod compound eyehomology is possible, especially; between crustaceans and hexapods, which have very similar eye facets andmay be sister taxa. However, judging homology only on similarity requires subjective decisions. Regardlessof whether compound eyes were present in a common ancestor of arthropods or crustaceans + hexapods,recent phylogenetic evidence suggests that the compound eyes, today present in myodocopid ostracods (Crus-tacea), may have been absent in ostracod ancestors. This pattern is inconsistent with phylogenetic homology.Multiple losses of ostracod eyes are an alternative hypothesis that is statistically improbable and withoutclear cause. One possible evolutionary process to explain the lack of phylogenetic'homology of ostracodcompound eyes is that eyes may evolve by switchback evolution, where genes for lost structures remaindormant and are re-expressed much later in evolution.

INTRODUCTION

"The eye" has long served as a canonical exampleof a complex trait. In an early design-based argumentfor the existence of God, Paley (1846) used the eye asan example of an intricate and marvelously functionalobject' that he thought must have been designed. Dar-win (1859) devoted an entire section of Tlze Origin ofSpecies to describing how eyes could evolve by a se-ries of small and plausible:steps. Darwin's logic wasthat if he presented a cogent argument for the eyeevolving gradually by natural selection, then other farless complex features surely could do the'same. Over150 years later, eyes still are used as models for un-derstanding the evolution of complex traits. But thecontext of the discussion has expanded beyond de-fending natural selection and now must incorporate-'amodern understanding of phylogeny, morphology, de-velopment, developmental genetics and evolutionarymechanisms. The discussion of eye evolution is rele-vant and siiular at many taxonomic levels and here Ifocus on arthropod compound eyes.

The phylogenetic distribution of conipound eyes inarthropods is perplexing. On one hand, the similarityof all arthropod compound eyes suggests that they mayhave evolved only once. On the other hand, many. ar-thropods lack compound'eyes, in many' instances forno apparent reason. These observations lead to one oftwo seemingly unlikely conclusions. Either compoundeyes with detailed similarities evolved multiple timesin different groups or comPound- eyes were lost in aseemingly inordinate number of lineages. Althoughsome researchers argue for homology, other recent ev-idence suggests multiple origins. Before considering

From the Symposium Comzparati'e and Integrative Visionz Re-searchi presented at the Annual Meeting of the Society for Integra-tive and Comparative Biology, 4-8 January 2003, at Toronto, Can-ada.

2 E-mail: oakley@lifesci.ucsb.edu

'the recent evidence for and implications of a poten-tially non-homologous arthropod compound eye, un-derstanding the case for compound eye homology isimportant.

THE CASE FOR ARTHROPOD COMPOUND EYEHOMOLOGY

Whether or not all arthropod compound eyes arehomologous depends on whether arthropods are mono-phyletic and on which. of the major groups are sister-taxa (Paulus, 2000). Polyphyly of arthropods contra-dicts compound eye homology and this hypothesis hasadvocates (Manton;, 1973; Fryer, 1996, 1998) but most

-authors now consider arthropods to be monophyletic(Wheeler et al., 1993; Brusca, 2000). More problem-atic are the relationships of the four major groups,hexapods (including insects), crustaceans, rnyriapods(including centipedes and millipedes), and. chelicerates(including spiders). There is a growing consensus thathexapods and crustaceans are sister taxa (Friedrich andTautz, 1995; Regier and Shultz, 1997; Boore et al.,1998. Giribet et al., 2001; Hwang et al., 2001), butthe placement of chelicerates and myriapods is con-tentious. For example, Giribet et al. (2001) fOund myr-

hiapods to-be the sister group of (Crustacea + Hexap-oda) while Hwang (2001) found evidence for a myr-iapod + chelicerate clade. Furthermore, -crustaceansmay be paraphyletic with respect to insects; in otherwords some crustaceans may be more closely relatedthan others to insects '(e.g.; Regier and Shultz, 1997;Brusca, 2000; Wilson et al., 2000).

These different possibilities for arthropod phyloge-ny affect conclusions about the homology of'com-pound eyes. For example, although crustacean com-pound eye facets (omnmatidia) are diverse, most aresimilar to insect ommatidia. In contrast, myriapods andchelicerates mostly lack compound eyes'and the om-matidia of the few group's that have compound eyesare very different from insect/crustacean ornmatidia

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ARTHROPOD COMPOUND EYE HOMOLOGY

(Table 1). Therefore, a sister relationship between in-sects and crustaceans leads to a conclusion of homol-ogy of compound eyes in those two groups, but notnecessarily in all arthropods (Richter, 2002). In addi-tion, the potential paraphyly of crustaceans is signifi-cant in this context because if true, some crustaceansare more closely related than others to insects. There-fore, compound eye homology could be restricted toinsects and some-but not all-crustaceans. Theseconsiderations require additional work on arthropodphylogeny, which is still controversial.

Regardless of the inclusiveness of a homology state-ment that depends on arthropod phylogeny, the pri-mary argument for compound eye homology is themorphological similarity of arthropod compound eyes.Intuition tells us that complexity and intricacy shouldalmost never evolve the same way more than once.This argument is often termed Dollo's law (Dollo,1893) and with respect to compound eyes, the idea isthat the similarities among eyes are too specific to beindependently evolved. What are these similarities,and how can we judge if they really are too specificto evolve more than once?

Homology inferred from similar morphology ofcompound eye facets

One major similarity among compound eyes of dif-ferent groups is the number of cells in each ommatid-ium. In particular, two cell types show similarity innumber and arrangement. The first involves the retin-ular or R-cells, which are the photoreceptive cells ofthe eye. In numerous arthropod groups, R-cells num-ber eight per facet. An additional similarity involvesthe crystalline cone or Semper cells, which are trans-parent cells at the distal end of the ommatidia. Conecells number four per facet in many compound eyes.The common occurrence of eight retinular and fourcrystalline cone cells per facet is often cited as evi-dence for compound eye homology; the pattern is con-sidered a similarity too detailed to evolve multipletimes (Paulus, 1979, 2000; Melzer et al., 1997).

A conclusion of homology based on similarity israther subjective and concerns two things. First, onemust consider the level of similarity among all theeyes. Put another way, one must decide how muchvariation is allowed before the trait is considered non-homologous. Second, one must consider the likelihoodof convergent evolution of the trait. For example, func-tional or developmental constraints may increase thechances of convergence. Next, I discuss each of thesetwo considerations for the conclusion of homologybased on cell numbers.

Cell numbers per facet vary in arthropods and thismust be considered when deciding on homology.There are many exceptions to the 8/4 pattern (Table1), and advocates of compound eye homology rarelydiscuss these inconsistencies in detail. The main ex-planation for the differences is that they are simplemodifications of the standard pattern (Paulus, 1979,2000; Richter, 2002). Indeed, the origin of such mod-

ifications is known to occur easily. For example, a mu-tation in the Drosophila gene sevenless is sufficient toreduce R-cell number from eight to seven (Harris etal., 1976; Hafen et al., 1987). However, ease of origindoes not necessarily equate with ease of evolution be-cause if deleterious to fitness, the mutation will be se-lected against. An important line of research would beto quantitatively assess the variation in cell numbers.in a phylogenetic context. For example, one could es-timate the rate of evolution of ommatidial cell numberby comparing the distribution of cell numbers to aphylogenetic tree. These rates could then be used toaddress hypotheses of independent origins, by evalu-ating whether the estimated rates are high enough toexplain changes in cell number in specific lineages.

A second consideration when inferring homologyfrom similarity is the possibility of convergence. Ad-vocates of arthropod polyphyly argue that convergenceis rampant in the group (Manton, 1973; Fryer, 1996).With regard to compound eyes, there may be func-tional constraints caused by the hard exoskeleton,which limits the size of eyes and makes multiple facetsthe most likely solution (Paulus, 2000). Selective pres-sure to evolve compound eyes is probably high (Nils-son, 1989, 1996). Nevertheless, Paulus (2000) arguedthat the ommatidia themselves are not necessarily un-der such evolutionary constraint.

In summary, the homology of compound eyes ofdifferent groups remains a viable hypothesis. The levelof this homology statement depends on our conclu-sions about arthropod phylogeny. Of primary importis the probable sister relationship between hexapodsand crustaceans ("tetraconata" sensu (Dohle, 2001)).The ommatidia of these two groups are the most sim-ilar of the major arthropod groups and compound eyesare common in many hexapods and crustaceans. Thisleaves Limulus, the only living chelicerates with com-pound eyes and Scutigeromorphs, the only living myr-iapods with compound eyes. The phylogenetic distri-bution and different morphological features of theseeyes suggest they may be of independent origin, al-though other interpretations are possible (Paulus,2000). Even though homology is feasible, testing thehypothesis with only morphological data is difficultbecause it requires subjective decisions about whatlevel of similarity and what chance of convergence areacceptable. As described in the next section, a com-plementary approach involves the explicit use of sta-tistical phylogenetic methods.

EVIDENCE AND IMPLICATIONS FOR A NON-HOMOLOGOUSCOMPOUND EYE

Recent evidence suggests that the compound eyesof myodocopid ostracods (Crustacea) may be phylo-gentically non-homologous to those of other arthro-pods. In other words, results are not consistent with ahypothesis of "phylogenetic homology," which assertsthe presence of a trait inf a common ancestor (e.g.,Butler and Saidel, 2000). More specifically, moleculardata (genes coding for 18S and 28S ribosomal RNA)

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TODD H.- OAKLEY

TABLE 1. Cell nuimber of various arthropod ommnatidia (X = lateral eyes absent).

Super-Class Class/Order

Chelicerata Merostomata

ArachnidaPycnogonida

Myriapoda DiplopodaChilopodaChil6podaPauropodaSymphyla

Crustacea Branchiopoda

RemipediaCephalocaridaCopepodaOstracoda

BranchiuraTantulocaridiaThecostracaMystacocaridaMalacostraca

Hexapoda. CollembolaProturaDiplura[nsecta

Scutigeromorpha

Phyl (Notostraca)

Species R-Cell # Cone Cell # Reterence

Limulus polyphee 4 to 20 . 0 (Fahrenbach, 1969)mufs

All living speciesAll living species

Scutigera

TrIops cancrifor-ines

Lepidurus apiusLeptodora kindtii

Anostraca ArtenmiaTanynzastix

Cladocera .Dapihnia

.All living speciesAll living speciesAll living species

Myodocopida 3 species -Vargula tsujii

Halocyprida and.Podocopa

Thoracica.

LeptostracaStomatopodaAnispidacea

Euphausidacea

Pericarida

Decapod

Archaeognatha/Machiloidea

Archaeognatha/Monura

ThysanuraPterygotalColeop

tera

Hemiptera

All living species

ArgulusfoliaceusAll Living SpeciesBalanius crenatusAll Living SpeciesNebaliaSquillaAnaspides tasnman-

iaeParanaspides la-I custris

Meganyctiphanesoson'egica

Neomysis integer(Mysida)

Lophogaster typi-.CUS (Lophogas-trida)

Pontoporeia affinis(Amphipoda)

Dutliclhia porecta(Amphipoda)

Oniscus aselltus(Isopoda)

Procambarus clar-kii

Gennadas sp.Many speciesAll living species'All living speciesMacltlis

Tenebrio molitor'

;Cylindrocauluspatalis

Trilobium casta-nelin

Nicagus japonicusAltica fragariae,

A. ampelophaga70 sp. Heteroptera

and relatives

"ocelli""oXei"ocelli"

;9-23 +,4"ocelli""ocelli" :8

85

668xxx681x

8x6x788

8

7

"ocelli"x"ocelli""ocelli"

* 4 :' "ocelli""ocelli"

* 4

45

4. 44xxx22x

4x3x442 + 2

2 + 2

2 + 2

7 2+2

7 2 + 2

5

5

16

8

6-78xx7 or 8

8

7 to 9-

8

78

-8

2

2

2

4

4xx4

4

4

44

I4

(Paulus, 2000)(Paulus, 1979)(Paulus, 1979)(Diersch et al., 1999)

:(Diersch et al., 1999)(Wolken and Gallik, 1965; Nilsson

'etal., 1983)(Elofsson and Odselius, 1975)(Paulus, 1979) -(Paulus, 1979).(Schram, 1986)(Elofsson and Hessler, 1990)(Huys and Boxshall. 1991)(Andersson, 1979; Huvard, 1990)-(Huvard, 1990)

(Meyer-Rochow et al., 2001)

(Hallberg and Elofsson, 1983)

(Paulus, 1979)(Schonenberger, 1977)(Richter, 1999)

(Richter, 1999)

(Richter, 1999)-

(Richter, 1999)

(Richter, 1999)

(Rosenberg and Langer, 1995)

(Meyer-Rochow et al., 1991)

(Paulus, 1979)

(Hafner End Tokarski, 1998)

(Richter, 1999)(Paulus, 1979)

(Paulus, 1979)

(Lee et al., 1999)

(Gokan, 1998)

(Friedrich et al., 1996)

(Gokan and Masuda, -1998)(Guo Bingqun Li et al., 1996): .

(Fischer et al., 2000)

524

ARTHROPOD COMPOUND EYE HOMOLOGY

TABLE 1. Contitnued.

Super-Class Class/Order Specics R.Cell # Cone Cell # Reference

Homoptera Cicadetta montana 6 (Dey, 1999)Hymenoptera Cataglyphis bicol- 9 (Meyer and Domanico, 1999)

orLepidoptera Parnara guttata 9 (Shimohigashi and Tominaga.

1999)Orgyia postica 8 4 (Ting et al., 2000)Ostriniafirnacalis 10 to 11 (Guo Bingqun Li, 1995)Helicoverpa arnmi- 7 to 8 (Guo Bingqun Li, 1995)

geraNeuroptera Mallada basalis 8 4 (Yang et al., 1998)Orthoptera Grylluts sp. 8 (Blum and Labhart, 2000)

Schistocerca gre- 7 (Homberg and Paech, 2002)'garia

Plecoptera Oyamia lugubris 8 (Nagashima and Meyer-RochowVictor, 1995)

indicate that myodocopids-the only ostracods withcompound eyes-are phylogenetically nestediwithinseveral groups that lack such eyes, a topology that iswell supported by bootstrap analysis (Oakley and Cun-ningham, 2002; Oakley, 2004). Using that topology,reconstruction of ancestral states using maximum like-lihood and maximum parsimony methods allowed fora test of phylogenetic homology. These methods in-dicated and significantly favored the absence of com-pound eyes in ancestral ostracods (Fig. 1A), inconsis-'tent with phylogenetic homology of ostracod com-pound eyes with those of other arthropods. An impor-tant point is that the non-homology of ostracodcompound eyes does not rule out homology of all oth-er arthropod compound eyes. For example, eyes mayhave been lost in early ostracods or near relatives, andsimply regained in myodocopids.

Although phylogenetic tests in ostracods are rela-tively clear, morphological evidence is somewhat am-biguous. If ostracod compound eyes are independentlyderived, one prediction is that the eyes should have adistinctive morphology; indeed they do deviate fromthe conserved 8/4 cell-pattern. Most studies indicatethat ostracod compound eyes, including Cypridinanorvegica, Philonmedes globosa, Macrocypridina cas-tanea, and Skogsbergia lerneri have six R-cells andtwo cone cells per facet (Andersson, 1979; Huvard,1990; Land and Nilsson, 1990). However, Huvard(1990) suggested that Vargula tsujii may contain eightR-cells per facet, an intriguing result that would indi-cate polymorphism of R-cell number within a familyof ostracods. Unfortunately, Huvard (1990) did notpresent photographs illustrating eight R-cells in V. tsu-jii ommatidia, so confirmation of this work is neces-sary. Despite the fact that ostracods deviate from the"conserved" 8/4 cell-number with a 6/2 combination,Richter (2002) felt that this difference was not enoughto support non-homology of ostracod compound eyes,arguing "This arrangement, which is different frombut still similar to the proposed ground pattern of theTetraconata, makes it very improbable that the ostra-cod eyes evolved de novo as proposed by Parker(1995) and Oakley and Cunningham (2002)." Again,

subjectivity comes into play here, forcing us to decidehow different an eye must be before it is consistentwith non-homology.

These results in ostracods lead to a conclusionwhich parallels that in all arthropods: Either ostracodcompound eyes with reasonable similarity to othereyes evolved independently or compound eyes havebeen lost in a seemingly (and statistically quantified)large number of ostracod lineages. Next, I will discussfurther the alternative possibilities of numerous inde-pendent losses or multiple independent origins. Thisdiscussion will focus on ostracods, but is also largelyapplicable to arthropods in general.

Statistical tests of multiple compound eye losses inostracods

'The possibility of multiple independent losses ofcompound eyes is an important consideration. Com-plex characters like eyes are probably more easily lostthan gained, which can cause reconstruction methodsto be misleading since they usually assume equal ratesof character gain and loss (Omland, 1997; Cunning-ham et al., 1998; Oakley and Cunningham, 2000,2002). In other words, because eyes are almost cer-tainly more easily lost than gained, we expect multiplelosses to be more likely than multiple gains. Based onthis consideration, Oakley and Cunningham (2002) de-signed statistical tests using maximum likelihood (ML)to determine the sensitivity of the multiple origins hy-pothesis to the assumption of equal rates of gain andloss of compound eyes.

Maximum likelihood methods of ancestral state re-construction usually employ a simple model of char-acter evolution with only two parameters: 1) rate ofgain and 2) rate of loss of the binary character in ques-tion. Assuming the phylogeny of the organisms isknown, the first step in MIL ancestor reconstruction isto estimate these rates of gain and loss before assessingsupport for the states of each ancestral node. Sinceparameter estimation 'is separate from ancestral stateestimation, the rate parameters can be set to differentvalues, allowing for sensitivity analyses of differenthypotheses (Oakley and Cunningham, 2002).

525

5 TODD1 H. OAKLEY

C- Tigriopus califomnicus

A , rz e~~-Argulus FL------ O Manawa staceyi

0 Bairdioid NZ

Uk' LSeliho v 0 Cypridopsis NC

Azygocypridina lowryi

Vargula hilgendorfii

,- Melavargula japonica

Skogsbergia lemer/

Parasterope pollex

= 1 Rate of gain 2 _ OS b Lw Tetraleberis LI

MYODOCOPIDAg v 0R Rutiderma apex

Euphilomedes JP

Euphilomedes sordida

1 Lateral Eyes Present Eusarsiella BZ

0 Lateral Eyes Absent Harbansus paucichelatus

Polycope NZ,0.1 Substitutions/Site> . . 0~~~~-- Conchoecia BD;

Conchoecia CA

., Tigriopus califomicus

I B . 4e ,Argulus FL_ 3 M awManawa staceyi

Bardioid NZ

Cypridopsis NC

) Azygocypridina lowryi

Vargula hilgendorfii

] Melavargulajaponica

Skogsbergia lerneri,.

. Parasterope pollex

MYODOCOPIDA . Tetraleberis LI

| . : 4 3 Rutiderma apex

Euphiomedes JPSubstitutions/

JX Site I Euphilomedes sordida

Q Median Eye Present Eusarsiella BZ

0 Median Eye Absent Harbansus paucichelatus

Polycope NZ

Conchoecia BD

Conchoecia CA

FIG. 1. Maximum likelihood analysis of eye characters. Molecular phylogeny was published previously (Oakley and Cunningham, 2002;.Oakley, 2004)..A. Presence (black) and absence (white).of lateral eyes mapped on molecular phylogeny with'relative branch lengths estimatedassuming a molecular clock. Pie charts represent relative support for one state versus the other state at a node. Arrows point to two potentialindependent origins of lateral eyes. The inset presents the likelihood surface for lateral eye evolution, the likelihood of different combinationsof rate parameters (darker shades represent higher likelihood values). The 95% confidence interval is also plotted and is the, contour line withwhite behind it. B. Presence (grey) and absence (white) of median eyes mapped on molecular phylogeny with relative branch lengths estimatedassuming a molecular clock. Pie charts represent relative support for one state versus.the other state at a' node.

526

ARTHROPOD COMPOUND EYE HOMOLOGY

For example, it is possible to assume an extremelyhigh and statistically significant rate of compound eyeloss in order to assess the sensitivity of the multipleorigins hypothesis: Assuming higher rates of loss in-creasingly favors the multiple-loss hypothesis over themultiple-origins hypothesis. First, we used ML to es-timate the rate of loss of compound eyes during ostra-cod evolution. We next estimated the 95% confidenceinterval around that loss parameter. Finally, we, as-sumed a value for the loss parameter that was outsidethe 95% confidence interval and reconstructed, ances-tral states using this significantly high value for eyeloss. Even when assuming a significantly high rate (arate outside the 95% confidence interval estimatedfrom the data) of compound eye loss, the multiple or-igins hypothesis was still favored, although not signif-icantly (Oakley and Cunningham, 2002).

Could life history drive loss of compound eyes?

Even though statistically improbable, multiple loss-es of compound eyes in ostracods and relatives arepossible. This is especially true if driven in differentgroups by environmental or life history constraints likesmall size, inactivity, or living in a lightless environ-ment. Under a hypothesis of compound eye hormologyand assuming the phylogenetic tree in Figure 1, thefollowing four lineages must have lost compoundeyes: Copepoda (including Tigriopus californicus), Po-docopa (including Cypridopsis), Manawa staceyi, andHalocyprids (including Conchoecia). These groups dotend to be small, which could make construction ofimage forming eyes relatively expensive. However,there are exceptions to small size in these groups, forexample many Halocyprids and some Podocopa areamong the largest living ostracods. Myodocopid ostra-cods-the only group with compound eyes-tend tobe larger than other ostracod groups (Cohen, 1982).

Besides size, another factor that could lead to lossof image forming eyes is relative inactivity. There isa significant correlation between the presence of im-age-forming eyes and locomotory speed in metazoans(de Queiroz, 1999). However, no clear conclusions canbe made for ostracods and relatives because the activ-ity levels of the groups without compound eyes arehighly variable. Many copepods are parasitic, with lowactivity levels, while many are planktonic with higheractivity levels (e.g., Huys and Boxshall, 1991). Po-docopa are also variable; most are benthic crawlers,but some-especially some freshwater forms-are ac-tive swimmers. Manawa staceyi probably does have arelatively low activity level as the species lives inter-stitially (Swanson, '1991). Finally, Halocyprid ostra-cods have a high activity level as a migratory plank-tonic group (e.g., Angel, 1984; Vannier and Abe,1992). Interestingly, the only ostracods with com-pound eyes (myodocopids) are mostly very activeswimmers; many are scavengers or predators (e.g., Co-hen, 1983; Kornicker, 1985; Keable, 1995; Kornickerand Poore, 1996).

A final and important life history-driven cause of

compound eye loss could be living in a lightless en-vironment. In general, although many groups of ostra-cods and relatives have probably secondarily invadedlightless niches, species living in illuminated environ-ments dominate the groups in question. Possible ex-ceptions include the interstitial Manawa staceyi, whichmay be derived from deep-sea ancestors, even thoughit currently lives in shallow illuminated seas (Swanson,1991). In addition, many Halocyprids live as planktonin the deep-sea.

Taken together, there is no obvious reason to con-clude that life history characters drove multiple inde-pendent losses of compound eyes in ostracods and rel-atives. However, in order to make definitive conclu-sions, we need a reliable and large-scale phylogeny forthe group, because the ancestral states of life historycharacters in the eyeless groups are more importantthan present day habits, which may be secondarily de-rived.

Potential causes of independent origins

If compound eyes were not lost in multiple lineages,then myodocopid compound eyes evolved indepen-dently compared to those of other arthropods. A majorcomplication for the multiple-origins hypothesis is thewidely held belief that complex traits should notevolve the same way more than once. This argument,often termed Dollo's law, is essentially probabilistic:Duplicating all the myriad steps necessary to evolveany complex structure should be exceedingly improb-able. Although well founded, Dollo's law makes animportant assumption that is possible to violate. Name-ly, complex structures like eyes might not evolve denovo every time and many of the steps toward originneed not be repeated. This evolutionary process wastermed switchback evolution by Van Valen (1979). Assuch, genes or even whole developmental pathwaysmay be retained during evolution, even in the absenceof the morphological features where those genes wereonce expressed. As a classic example, the existence ofa latent developmental program was proposed to ex-plain the experimental induction of teeth in chickens(Kollar and Fisher, 1980; Gould, 1983; Chen et al.,2000). In a more recent example, Whiting et al. (2003)suggested, based on phylogenetic distribution, that in-sect wings may be evolving by switchback evolution.

As a mechanism for maintaining latent genetic path-ways, Marshall et al. (1994) suggested that genes orwhole pathways may have multiple functions and aretherefore maintained during evolution, even in the ab-sence of one of those functions. Under such a model,re-evolving a compound eye that was lost during evo-lution may not be so improbable if much of the geneticmachinery was retained for other functions. Impor-tantly, genes involved in vision are already known tohave multiple functions and to be maintained in theabsence of visual function. For, example, visual pig-ment genes (opsins) were maintained in crayfish thatevolved in caves (Crandall and Hillis, 1997) as wellas the subterranean blind mole rat, which has only ves-

527

5TODD H. OAKLEY

tigial eyes (Janssen et al., 2000). In addition, homologsof the eye development genes Pax-6 (or eyeless) andSix (or sine ocuilis) are present in Caenorhabditis ele-gaIls, which lacks eyes and ocelli (though exhibitingphototactic behavior) S (Chisholm and Horvitz, 1995;Zhang and Emmons, 1995; Deininger et al., 2000;Dozier et al., 2001).

These considerations lead to the interesting hypoth-esis that genes that code for myodocopid compoundeyes were maintained during ostracod evolution in the-absence of the eyes themselves. A primary candidatefor the function of such genes could be for use inanother type of eye that is:present in ostracods calledthe median or naupliar eye. Therefore, compound eyescould have been lost'in early ostracods or relatives,but many of the genes used for these eyes could havebeen maintained for use in median eyes, thus facili-tating a re-evolution of compound eyes. In otherwords, homologous median eyes acted as an evolu-.tionary "repository" for genes, allowing a separate or-igin of compound eyes, perhaps even through repli-'cation of median eyes (Oakley, 2003). This hypothesismake's two f testable; predictions 1) median eyes werepresent in ostracod ancestors' and 2) genes involved innewly evolved compound eyes-were recruited frommediaiu eyes. Phylogenetic and morphological evi-dence is consistent with the presence' of median eyesin ostracod ancestors (Oakley and Cunningham, 2002;Oakley, 2004, Fig. IB) and preliminary evidence sug-gests at least one gene-the visual pigment, gene op-sin-was recently duplicated and recruited from me-dian eye to compound eyes (Oakley and Huber, un-published).

The possibility of switchback evolution of eyes un-derscores the importance of a clear use of the termhomology (Abouheif, 1997). Throughout most of this'essay, I have referred to "phylogenetic homology,"which asserts the presence of a character (like com-pound.eyes) in a common ancestor. However, "gen-erative homology" (Butler and Saidel, 2000) may bemore appropriate when considering a process likeswitchback- evolution. Generative homology, or: thesimilar idea "homocracy", (Nielsen and Martinez,2003), refers to traits that are organized by the-ex-pression of the same patterning genes,'regardless ofwhether 'they are phylogenetically homologous. If os-tracod compound eyes are not phylogenetically ho-mologous, as molecular phylogeny suggests, they maystill be generatively homologous or "syngenous,"'meaning that the same genes underlie their develop-ment.

SUMMARYThe phylogenetic distribution of compound eyes in

ostracods and relatives produces a dilermamashared inall of Arthropoda: Either eyes - were lost numeroustimes or they evolved, independently in a very similarway multiple times, perhaps through re-deployment ofconserved developmental genes and processses. De-tailed similarity alone supports homology but'these ar-

guments can be subjective.' Furthermore, evolutionarymechanisms like switchback evolution 'may result insimilarities among structures'that are not phylogenet-ically homologous: Therefore, multiple origins of com-pound eyes (phylogenetic homoplasy) currently cannotbe discounted. Fully . understanding arthropod com-,pound eye evolution is a goal worthy of pursuing be-cause it will contribute to'a better understanding ofevolutionary processes but it will require a diverse per-spective.

ACKNOWLEDGMENTS'

Thanks to Mason Posner and Sonke Johnsen for co-organiizing the symposium 'on integrative and compar-ative vision research. Thanks 'also' to 'the participants.I 'acknowledge C. Cutnningham and his laborato'rymembers for advice during 'the initial stages of my;enquiries into ostracod eye evolution.

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Andersson, A. 1979. Ultrastructure of 'ostracod senso7 y or7gans.University of Lund, Lund.

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