Molecular phylogenetic evidence for the independent evolutionary origin of an arthropod compound eye Todd H Oakley and Clifford W Cunningham Department of Biology Duke University Box 90325 Durham NC 27708 0325 Edited 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 with debate focused on how often such complex organs might have evolved One such debate is whether arthropod compound eyes are the product of single or multiple origins Here we use molecular phylogeny to address this long standing debate and find results favoring the multiple origins hypothesis Our analyses of DNA sequences encoding rRNA unequivocally indicate that myodocopids the only Ostracoda Crustacea with compound eyes are nested phylogenetically within several groups that lack compound eyes With our well supported phylogeny standard maximum likelihood ML character reconstruction methods significantly reconstruct ancestral ostracods as lacking compound eyes We also introduce a likelihood sensitivity analysis and show that the single origin hypothesis is not significantly favored unless we assume a highly asymmetric model of evolution one favoring eye loss more than 30 1 over gain These results illustrate exactly why arthropod compound eye evolution has remained controversial because one of two seemingly very unlikely evolutionary histories must be true Either compound eyes with detailed similarities evolved multiple times in different arthropod groups or compound eyes have been lost in a seemingly inordinate number of arthropod lineages T he number of times eyes originated during evolution is often debated including within anthropods 1 3 Many biologists argue that arthropod compound eyes are the product of a single origin because detailed similarities exist among the eyes of diverse groups For example genes involved in eye development such as Pax 6 and sine oculis appear functionally conserved across phyla and may also be conserved within Arthropoda 2 In addition a highly stereotyped number and arrangement of cells develop in a similar manner to form the individual eye facets of different arthropod groups 4 8 Finally neural circuitry of the optic lobe is highly conserved in many arthropods 9 Despite the many similarities some scientists suggest that compound eyes may result from multiple origins Nilsson 10 argues that the different biophysical properties of some eyes make homology unlikely Others postulate based on phylogenetic arguments drawn from taxonomy that compound eyes may have multiple origins 11 12 We have taken advantage of the power of molecular systematics and the recent advances in methods for analyzing character evolution to study the question of compound eye evolution in a phylogenetic framework Here we use these tools and examine the phylogeny of the Ostracoda Crustacea to test the hypothesis that one ostracod group independently evolved compound eyes with respect to all other arthropods 11 12 The Ostracoda are a diverse and ancient group of bivalved crustaceans with a superb fossil record dating back at least 500 million years 13 Taxonomically ostracods are often divided into three major groups Podocopa Palaeocopa and Myodocopa 13 The Myodocopa are further divided into the Halocyprida and Myodocopida Although most Podocopa and Myodocopida have a non image forming and anterodorsally located eye called the median eye the Myodocopida myodocopids are the only ostracods that also have a pair of lateral compound eyes Our molecular phylogeny clearly indicates that myodocopids are monophyletic and are nested 1426 1430 PNAS February 5 2002 vol 99 no 3 within several groups lacking compound eyes Based on this phylogeny methods of character reconstruction significantly favor the independent origin of myodocopid compound eyes constituting the strongest phylogenetic evidence to date for multiple origins of arthropod eyes If this is not an independent origin and compound eyes were actually lost many times then this is a case where commonly used methods of historical inference are positively and significantly misleading Methods Taxa Our analysis contains representatives of the major groups of Ostracoda 13 with the possible exception of the Platycopida which lack both median and compound eyes and are often placed within the Podocopa 14 We sampled all five taxonomic families of Myodocopida the only ostracods with compound eyes to test for monophyly As outgroups we chose two maxillopods crustaceans thought to be close relatives of ostracods e g ref 5 Like most maxillopods 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 Copepoda This outgroup choice is conservative with respect to the independent compound eyes hypothesis because most maxillopods lack compound eyes 5 and the inclusion of additional outgroups lacking compound eyes could strengthen but is unlikely to weaken our conclusion of independent origins Collection details for all taxa are available from T H O Sequences and Phylogenetic Analysis We used standard primers and methods to obtain a complete sequence for DNA encoding 18S rRNA rDNA and a partial 28S rDNA sequence including the ddff eemm and vx regions 15 16 We aligned sequences with CLUSTALX 17 and removed ambiguously aligned regions although the same maximum likelihood ML tree topology was obtained when including all data results not shown We determined the best fit model of molecular evolution to be Tamura Nei 18 gamma invariant sites by using MODELTEST 19 We then fixed parameters to their ML estimates transversions 1 A G 3 5081 C T 4 1785 gamma shape 0 6894 proportion of invariant sites 0 3228 for a ML heuristic search and for 500 ML bootstrap pseudoreplicates in PAUP 20 We estimated relative branch lengths by using the ML tree and assuming a molecular clock Ancestral State Reconstruction Taxa were scored for presence absence of compound eyes and separately for presence absence This 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 GenBank database accession nos AF363294 AF363360 To whom reprint requests should be addressed at present address Department of Ecology and Evolution University of Chicago 1101 East 57th
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