Evolutionary ecology of opsin gene sequence, expression and repertoire.

Linking molecular evolution to biological function is a long-standing challenge in evolutionary biology. Some of the best examples of this involve opsins, the genes that encode the molecular basis of light reception. In this issue of Molecular Ecology, three studies examine opsin gene sequence, expression and repertoire to determine how natural selection has shaped the visual system. First, Escobar-Camacho et al. () use opsin repertoire and expression in three Amazonian cichlid species to show that a shift in sensitivity towards longer wavelengths is coincident with the long-wavelength-dominated Amazon basin. Second, Stieb et al. () explore opsin sequence and expression in reef-dwelling damselfish and find that UV- and long-wavelength vision are both important, but likely for different ecological functions. Lastly, Suvorov et al. () study an expansive opsin repertoire in the insect order Odonata and find evidence that copy number expansion is consistent with the permanent heterozygote model of gene duplication. Together these studies emphasize the utility of opsin genes for studying both the local adaptation of sensory systems and, more generally, gene family evolution

Genetics of adaptation: Experimental test of a biotic mechanism driving divergence in traits and genes.

The genes underlying adaptations are becoming known, yet the causes of selection on genes-a key step in the study of the genetics of adaptation-remains uncertain. We address this issue experimentally in a threespine stickleback species pair showing exaggerated divergence in bony defensive armor in association with competition-driven character displacement. We used semi-natural ponds to test the role of a native predator in causing divergent evolution of armor and two known underlying genes. Predator presence/absence altered selection on dorsal spines and allele frequencies at the Msx2a gene across a generation. Evolutionary trajectories of alleles at a second gene, Pitx1, and the pelvic spine trait it controls, were more variable. Our experiment demonstrates how manipulation of putative selective agents helps to identify causes of evolutionary divergence at key genes, rule out phenotypic plasticity as a sole determinant of phenotypic differences, and eliminate reliance on fitness surrogates. Divergence of predation regimes in sympatric stickleback is associated with coevolution in response to resource competition, implying a cascade of biotic interactions driving species divergence. We suggest that as divergence proceeds, an increasing number of biotic interactions generate divergent selection, causing more evolution in turn. In this way, biotic adaptation perpetuates species divergence through time during adaptive radiation in an expanding number of traits and genes

The genetic basis of divergent melanic pigmentation in benthic and limnetic threespine stickleback

Pigmentation is an excellent trait to examine patterns of evolutionary change because it is often under natural selection. Benthic and limnetic threespine stickleback (Gasterosteus aculeatus) exhibit distinct pigmentation phenotypes, likely an adaptation to occupation of divergent niches. The genetic architecture of pigmentation in vertebrates appears to be complex. Prior QTL mapping of threespine stickleback pigmentation phenotypes has identified several candidate loci. However-relative to other morphological phenotypes (e.g., spines or lateral plates)-the genetic architecture of threespine stickleback pigmentation remains understudied. Here, we performed QTL mapping for two melanic pigmentation traits (melanophore density and lateral barring) using benthic-limnetic F2 crosses. The two traits mapped to different chromosomes, suggesting a distinct genetic basis. The resulting QTLs were additive, but explained a relatively small fraction of the total variance (~6%). QTLs maps differed by F1 family, suggesting variation in genetic architecture or ability to detect loci of small effect. Functional analysis identified enriched pathways for candidate loci. Several of the resulting candidate loci for pigmentation, including three loci in enriched pathways (bco1, sulf1, and tyms) have been previously indicated to affect pigmentation in other vertebrates. These findings add to a growing body of evidence suggesting pigmentation is often polygenic

Gut Microbiota Uniqueness Is Associated with Lake Size, a Proxy for Diet Diversity, in Stickleback Fish.

AbstractOrganismal divergence can be driven by differential resource use and adaptation to different trophic niches. Variation in diet is a major factor shaping the gut microbiota, which is crucial for many aspects of their hosts' biology. However, it remains largely unknown how host diet diversity affects the gut microbiota, and it could be hypothesized that trophic niche width is positively associated with gut microbiota diversity. To test this idea, we sequenced the 16S ribosomal RNA gene from intestinal tissue of 14 threespine stickleback populations from lakes of varying size on Vancouver Island, Canada, that have been shown to differ in trophic niche width. Using lake size as a proxy for trophic ecology, we found evidence for higher gut microbiota uniqueness among individuals from populations with broader trophic niches. While these results suggest that diet diversity might promote gut microbiota diversity, additional work investigating diet and gut microbiota variation of the same host organisms will be necessary. Yet our results motivate the question of how host population diversity (e.g., ecological, morphological, genetic) might interact with the gut microbiota during the adaptation to ecological niches

Pleiotropy facilitates parallel adaptation in sticklebacks

Highly pleiotropic genes are predicted to be used less often during adaptation, as mutations in these loci are more likely to have negative fitness consequences. Following this logic, we tested whether pleiotropy impacts the probability that a locus will be used repeatedly in adaptation. We used two proxies to estimate pleiotropy: number of phenotypic traits affected by a given genomic region and gene connectivity. We first surveyed 16 independent stream‐lake and three independent benthic‐limnetic ecotype pairs of threespine stickleback to estimate genome‐wide patterns in parallel genomic differentiation. Our analysis revealed parallel divergence across the genome; 30%–37% of outlier regions were shared between at least two independent pairs in either the stream‐lake or benthic‐limnetic comparisons. We then tested whether parallel genomic regions are less pleiotropic than nonparallel regions. Counter to our a priori prediction, parallel genomic regions contained genes with significantly more pleiotropy; that is, influencing a greater number of traits and more highly connected. The increased pleiotropy of parallel regions could not be explained by other genomic factors, as there was no significant difference in mean gene count, mutation or recombination rates between parallel and nonparallel regions. Interestingly, although nonparallel regions contained genes that were less connected and influenced fewer mapped traits on average than parallel regions, they also tended to contain the genes that were predicted to be the most pleiotropic. Taken together, our findings are consistent with the idea that pleiotropy only becomes constraining at high levels and that low or intermediate levels of pleiotropy may be beneficial for adaptation