Molecular phylogenetic evidence for the independentevolutionary origin of an arthropod compound eyeTodd H. Oakley†and Clifford W. CunninghamDepartment of Biology, Duke University, Box 90325, Durham, NC 27708-0325Edited by James W. Valentine, University of California, Berkeley, CA, and approved November 30, 2001 (received for review September 12, 2001)Eyes often take a central role in discussions of evolution, withdebate focused on how often such complex organs might haveevolved. One such debate is whether arthropod compound eyesare the product of single or multiple origins. Here we use molecularphylogeny to address this long-standing debate and find resultsfavoring the multiple-origins hypothesis. Our analyses of DNAsequences encoding rRNA unequivocally indicate that myo-docopids—the only Ostracoda (Crustacea) with compound eyes—are nested phylogenetically within several groups that lack com-pound eyes. With our well-supported phylogeny, standardmaximum likelihood (ML) character reconstruction methods sig-nificantly reconstruct ancestral ostracods as lacking compoundeyes. We also introduce a likelihood sensitivity analysis, and showthat the single-origin hypothesis is not significantly favored unlesswe assume a highly asymmetric model of evolution (one favoringeye loss more than 30:1 over gain). These results illustrate exactlywhy arthropod compound eye evolution has remained controver-sial, because one of two seemingly very unlikely evolutionaryhistories must be true. Either compound eyes with detailed simi-larities evolved multiple times in different arthropod groups orcompound eyes have been lost in a seemingly inordinate numberof arthropod lineages.The number of times eyes originated during evolution is oftendebated, including within anthropods (1–3). Many biologistsargue that arthropod compound eyes are the product of a singleorigin because detailed similarities exist among the eyes ofdiverse groups. For example, genes involved in eye developmentsuch as Pax-6 and sine oculis appear functionally conservedacross phyla and may also be conserved within Arthropoda (2).In addition, a highly stereotyped number and arrangement ofcells develop in a similar manner to form the individual eye facetsof different arthropod groups (4–8). Finally, neural circuitry ofthe optic lobe is highly conserved in many arthropods (9).Despite the many similarities, some scientists suggest thatcompound eyes may result from multiple origins. Nilsson (10)argues that the different biophysical properties of some eyesmake homology unlikely. Others postulate, based on phyloge-netic arguments drawn from taxonomy, that compound eyes mayhave multiple origins (11, 12). We have taken advantage of thepower of molecular systematics and the recent advances inmethods for analyzing character evolution to study the questionof compound eye evolution in a phylogenetic framework.Here we use these tools and examine the phylogeny of theOstracoda (Crustacea) to test the hypothesis that one ostracodgroup independently evolved compound eyes with respect to allother arthropods (11, 12). The Ostracoda are a diverse andancient group of bivalved crustaceans with a superb fossil recorddating back at least 500 million years (13). Taxonomically,ostracods are often divided into three major groups: Podocopa,Palaeocopa, and Myodocopa (13). The Myodocopa are furtherdivided into the Halocyprida and Myodocopida. Although mostPodocopa and Myodocopida have a non-image-forming andanterodorsally located eye called the ‘‘median eye,’’ the Myo-docopida (myodocopids) are the only ostracods that also have apair of lateral compound eyes. Our molecular phylogeny clearlyindicates that myodocopids are monophyletic and are nestedwithin several groups lacking compound eyes. Based on thisphylogeny, methods of character reconstruction significantlyfavor the independent origin of myodocopid compound eyes,constituting the strongest phylogenetic evidence to date formultiple origins of arthropod eyes. If this is not an independentorigin, and compound eyes were actually lost many times, thenthis is a case where commonly used methods of historicalinference are positively and significantly misleading.MethodsTaxa. Our analysis contains representatives of the major groupsof Ostracoda (13), with the possible exception of the Platyco-pida, which lack both median and compound eyes and are oftenplaced within the Podocopa (14). We sampled all five taxonomicfamilies of Myodocopida, the only ostracods with compoundeyes, to test for monophyly.As outgroups we chose two maxillopods, crustaceans thoughtto be close relatives of ostracods (e.g., ref. 5). Like mostmaxillopods, both chosen outgroups have a median eye (5).However, only one of these outgroups also has compound eyes(Argulus sp.: Branchyura), the other does not (Tigriopus: Copep-oda). This outgroup choice is conservative with respect to theindependent compound eyes hypothesis, because most maxillo-pods lack compound eyes (5) and the inclusion of additionaloutgroups lacking compound eyes could strengthen but is un-likely to weaken our conclusion of independent origins. Collec-tion details for all taxa are available from T.H.O.Sequences and Phylogenetic Analysis. We used standard primersand methods to obtain a complete sequence for DNA encoding18S rRNA (rDNA) and a partial 28S rDNA sequence includingthe ddff, eemm, and vx regions (15, 16). We aligned sequenceswithCLUSTALX (17) and removed ambiguously aligned regions,although the same maximum likelihood (ML) tree topology wasobtained when including all data (results not shown). Wedetermined the best-fit model of molecular evolution to beTamura–Nei (18) ⫹ gamma ⫹ invariant sites by usingMODEL-TEST (19). We then fixed parameters to their ML estimates(transversions ⫽ 1; A–G ⫽ 3.5081; C–T ⫽ 4.1785; gammashape ⫽ 0.6894; proportion of invariant sites ⫽ 0.3228) for a MLheuristic search and for 500 ML bootstrap pseudoreplicates inPAUP* (20). We estimated relative branch lengths by using theML tree and assuming a molecular clock.Ancestral State Reconstruction. Taxa were scored for presence兾absence of compound eyes and separately for presence兾absenceThis paper was submitted directly (Track II) to the PNAS office.Abbreviations: rDNA, rRNA-encoding DNA; ML, maximum likelihood.Data deposition: The sequences reported in this paper have been deposited in the GenBankdatabase (accession nos. AF363294–AF363360).†To whom reprint requests
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