Parallel changes in gut microbiome composition and function in parallel local adaptation and speciation

The processes of local adaptation and ecological speciation are often strongly shaped by biotic interactions such as competition and predation. One of the strongest lines of evidence that biotic interactions drive evolution comes from repeated divergence of lineages in association with repeated changes in the community of interacting species. Yet, relatively little is known about the repeatability of changes in gut microbial communities and their role in adaptation and divergence of host populations in nature. Here we utilize three cases of rapid, parallel adaptation and speciation in freshwater threespine stickleback to test for parallel changes in associated gut microbiomes. We find that features of the gut microbial communities have shifted repeatedly in the same direction in association with parallel divergence and speciation of stickleback hosts. These results suggest that changes to gut microbiomes can occur rapidly and predictably in conjunction with host evolution, and that host-microbe interactions might play an important role in host adaptation and diversification

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

Opsin expression predicts male nuptial color in threespine stickleback.

Theoretical models of sexual selection suggest that male courtship signals can evolve through the build-up of genetic correlations between the male signal and female preference. When preference is mediated via increased sensitivity of the signal characteristics, correlations between male signal and perception/sensitivity are expected. When signal expression is limited to males, we would expect to find signal-sensitivity correlations in males. Here, we document such a correlation within a breeding population of threespine stickleback mediated by differences in opsin expression. Males with redder nuptial coloration express more long-wavelength-sensitive (LWS) opsin, making them more sensitive to orange and red. This correlation is not an artifact of shared tuning to the optical microhabitat. Such correlations are an essential feature of many models of sexual selection, and our results highlight the potential importance of opsin expression variation as a substrate for signal-preference evolution. Finally, these results suggest a potential sensory mechanism that could drive negative frequency-dependent selection via male-male competition and thus maintain variation in male nuptial color