Dataset Information

Genomic Environment Impacts Color Vision Evolution in a Family with Visually Based Sexual Selection.

ABSTRACT: Many models of evolution by sexual selection predict a coevolution of sensory systems and mate preferences, but the genomic architecture (number and arrangement of contributing loci) underlying these characters could constrain this coevolution. Here, we examine how the genomic organization and evolution of the opsin genes (responsible for tuning color vision) can influence the evolutionary trajectory of sexually selected traits across 15 species in the family Poeciliidae, which includes classic systems for studies of color-mediated sexual selection such as guppies, swordtails, and mollies. Although male coloration patterns and the importance of this coloration in female mate choice vary widely within and among genera, sequencing revealed low variability at amino acid sites that tune Long Wavelength-Sensitive (LWS) opsins in this speciose family. Although most opsin genes in these species appear to have evolved along traditional mutation-selection dynamics, we identified high rates of gene conversion between two of the LWS loci (LWS-1 and LWS-3), likely due to the inverted tandem repeat nature of these genes. Yet members of the subgenus Lebistes appear to resist LWS gene conversion. The LWS opsins are responsible for detecting and discriminating red and orange coloration-a key sexually selected trait in members of the subgenus Lebistes. Taken together these results suggest selection is acting against the homogenizing effects of gene conversion to maintain LWS-1/LWS-3 differences within this subgenus.

SUBMITTER: Sandkam BA

PROVIDER: S-EPMC5714168 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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Genomic Environment Impacts Color Vision Evolution in a Family with Visually Based Sexual Selection.

Sandkam Benjamin A BA Joy Jeffrey B JB Watson Corey T CT Breden Felix F

Genome biology and evolution 20171101 11

Many models of evolution by sexual selection predict a coevolution of sensory systems and mate preferences, but the genomic architecture (number and arrangement of contributing loci) underlying these characters could constrain this coevolution. Here, we examine how the genomic organization and evolution of the opsin genes (responsible for tuning color vision) can influence the evolutionary trajectory of sexually selected traits across 15 species in the family Poeciliidae, which includes classic ...[more]

PMID: 29121209

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Project description:Comparative genomics has contributed to the growing evidence that sexual selection is an important component of evolutionary divergence and speciation. Divergence by sexual selection is implicated in faster rates of divergence of the X chromosome and of genes thought to underlie sexually selected traits, including genes that are sex biased in expression. However, accurately inferring the relative importance of complex and interacting forms of natural selection, demography, and neutral processes that occurred in the evolutionary past is challenging. Experimental evolution provides an opportunity to apply controlled treatments for multiple generations and examine the consequent genomic divergence. Here, we altered sexual selection intensity, elevating sexual selection in polyandrous lines and eliminating it in monogamous lines, and examined patterns of allele frequency divergence in the genome of Drosophila pseudoobscura after more than 160 generations of experimental evolution. Divergence is not uniform across the genome but concentrated in "islands," many of which contain candidate genes implicated in mating behaviors and other sexually selected phenotypes. These are more often seen on the X chromosome, which also shows greater divergence in F ST than neutral expectations. There are characteristic signatures of selection seen in these regions, with lower diversity on the X chromosome than the autosomes, and differences in diversity on the autosomes between selection regimes. Reduced Tajima's D within some of the divergent regions may imply that selective sweeps have occurred, despite considerable recombination. These changes are associated with both differential gene expression between the lines and sex-biased gene expression within the lines. Our results are very similar to those thought to implicate sexual selection in divergence between species and natural populations, and hence provide experimental support for the likely role of sexual selection in driving such types of genetic divergence, but also illustrate how variable outcomes can be for different genomic regions.

Project description:Color vision in primates is variable across species, and it represents a rare trait in which the genetic mechanisms underlying phenotypic variation are fairly well-understood. Research on primate color vision has largely focused on adaptive explanations for observed variation, but it remains unclear why some species have trichromatic or polymorphic color vision while others are red-green color blind. Lemurs, in particular, are highly variable. While some species are polymorphic, many closely-related species are strictly dichromatic. We provide the first characterization of color vision in a wild population of red-bellied lemurs (Eulemur rubriventer, Ranomafana National Park, Madagascar) with a sample size (87 individuals; NX chromosomes = 134) large enough to detect even rare variants (0.95 probability of detection at ≥ 3% frequency). By sequencing exon 5 of the X-linked opsin gene we identified opsin spectral sensitivity based on known diagnostic sites and found this population to be dichromatic and monomorphic for a long wavelength allele. Apparent fixation of this long allele is in contrast to previously published accounts of Eulemur species, which exhibit either polymorphic color vision or only the medium wavelength opsin. This unexpected result may represent loss of color vision variation, which could occur through selective processes and/or genetic drift (e.g., genetic bottleneck). To indirectly assess the latter scenario, we genotyped 55 adult red-bellied lemurs at seven variable microsatellite loci and used heterozygosity excess and M-ratio tests to assess if this population may have experienced a recent genetic bottleneck. Results of heterozygosity excess but not M-ratio tests suggest a bottleneck might have occurred in this red-bellied lemur population. Therefore, while selection may also play a role, the unique color vision observed in this population might have been influenced by a recent genetic bottleneck. These results emphasize the need to consider adaptive and nonadaptive mechanisms of color vision evolution in primates.

Dataset Information

Genomic Environment Impacts Color Vision Evolution in a Family with Visually Based Sexual Selection.

Publications

Genomic Environment Impacts Color Vision Evolution in a Family with Visually Based Sexual Selection.

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