2002Proceedings of the National Academy of SciencesOpen access

Molecular phylogenetic evidence for the independent evolutionary origin of an arthropod compound eye

Todd H. Oakley, Cliff Cunningham

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Abstract

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.

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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.

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Available abstract

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.

Key concepts: Arthropod, Phylogenetics, Phylogenetic tree, Biology, Evolutionary biology, Compound eye, Character (mathematics), Zoology

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