Distinct Evolutionary Patterns Between Two Duplicated Color Vision Genes Within Cyprinid Fishes

Abstract

We investigated the molecular evolution of duplicated color vision genes (LWS-1 and SWS2) within cyprinid fish, focusing on the most cavefish-rich genusSinocyclocheilus. Maximum likelihood-based codon substitution approaches were used to analyze the evolution of vision genes. We found that the duplicated color vision genes had unequal evolutionary rates, which may lead to a related function divergence. Divergence of LWS-1 was strongly influenced by positive selection causing an accelerated rate of substitution in the proportion of pocketforming residues. The SWS2 pigment experienced divergent selection between lineages, and no positively selected site was found. A duplicate copy of LWS-1 of some cyprinine species had become a pseudogene, but all SWS2 sequences remained intact in the regions examined in the cyprinid fishes examined in this study. The pseudogenization events did not occur randomly in the two copies of LWS-1 within Sinocyclocheilus species. Some cave species of Sinocyclocheilus with numerous morphological specializations that seem to be highly adapted for caves, retain both intact copies of color vision genes in their genome. We found some novel amino acid substitutions at key sites, which might represent interesting target sites for future mutagenesis experiments. Our data add to the increasing evidence that duplicate genes experience lower selective constraints and in some cases positive selection following gene duplication. Some of these observations are unexpected and may provide insights into the effect of caves on the evolution of color vision genes in fishes.

Complex patterns of divergence among green-sensitive (RH2a) African cichlid opsins revealed by Clade model analyses

“…We note that our study is the first, to our knowledge, to explicitly investigate divergence among both orthologs and paralogs in the same data set. Finally, it is noteworthy that several studies have used the results of Clade model analyses to support arguments of positive selection [101,102], but whether or not the relevant ω estimates significantly exceed ω = 1 has not been explicitly tested, as we have done here; this point, while at first glance technical in nature, is of large importance, as ω estimates larger than ω = 1 may occur due to chance.…”

The future of codon models in studies of molecular function: ancestral reconstruction and clade models of functional divergence

“…Li et al, 2011 Feline cauxins (urinary proteins) Orthologs CmC, CmD Liao et al, 2010 Rhododendron small heat shock proteins Paralogs CmD Liu et al, 2010 Mammalian prestins (auditory motor proteins) Orthologs CmC Wang et al, 2010 Vertebrate plasma membrane transport proteins Paralogs CmC Wei et al, 2010 Feline major-histocompatibility complex peptide binding regions Paralogs CmC Hughes et al, 2009b Mammalian UCP mitochondrial anion carriers Paralogs CmC Hughes et al, 2009a Primate melanocortin receptors Orthologs CmC Li et al, 2009 Cyprinid cone opsins (visual pigment proteins) Paralogs CmC Mondragon-Palomino et al, 2009 Orchid class-B MADS-box transcription factors Paralogs CmC, CmD Zhao et al, 2009 Mammalian rod opsins (visual pigment proteins) Orthologs CmC Des Marais and Rausher, 2008 Morning glory acanthocyanin pigment pathway reductases Paralogs CmC Haudry et al 2008 A variety of gene fragments from selfing and non-selfing grasses Orthologs CmC Summers and Zhu, 2008 Cichlid prolactin hormones Paralogs CmD Alverson, 2007 Diatom silicon transporters Orthologs CmD Hernandez-Hernandez et al, 2007 Eudicot class-B MADS-box transcription factors Paralogs CmD Li et al, 2007 Bat FoxP2 transcription factors Orthologs CmC Balakirev et al, 2006 Drosophila β-esterase enzymes Paralogs CmD Bielawski and Yang, 2004 Primate RNases and globins Paralogs CmD goodness-of-fit of CmC (Weadick and Chang, in press). Briefly, CmC and its typically used null model, M1a, differ not just in whether˘is heterogeneous between among clades, but also in how they model among-site˘variation.…”

Evidence for Repeated Loss of Selective Constraint in Rhodopsin of Amblyopsid Cavefishes (Teleostei: Amblyopsidae)

“…Studies demonstrating that regressive evolution of eyes in subterranean organisms is associated with loss of gene function at the molecular level are limited to subterranean diving beetles (Leys et al 2005), Mexican cavefish (Yokoyama et al 1995), marsupial moles (Springer et al 1997), naked mole rats (Kim et al 2011), and cave-roosting bats (Zhao et al 2009a). Several additional studies found no support for LOF of vision-related genes in a variety of subterranean organisms (Yokoyama and Yokoyama 1990a,b;Crandall and Hillis 1997;Janssen et al 2000;Smulders et al 2002;Jeffery 2005Jeffery , 2009Li and He 2009;Li et al 2009b).…”