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

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

Rapid adaptive evolution of colour vision in the threespine stickleback radiation.

Vision is a sensory modality of fundamental importance for many animals, aiding in foraging, detection of predators and mate choice. Adaptation to local ambient light conditions is thought to be commonplace, and a match between spectral sensitivity and light spectrum is predicted. We use opsin gene expression to test for local adaptation and matching of spectral sensitivity in multiple independent lake populations of threespine stickleback populations derived since the last ice age from an ancestral marine form. We show that sensitivity across the visual spectrum is shifted repeatedly towards longer wavelengths in freshwater compared with the ancestral marine form. Laboratory rearing suggests that this shift is largely genetically based. Using a new metric, we found that the magnitude of shift in spectral sensitivity in each population corresponds strongly to the transition in the availability of different wavelengths of light between the marine and lake environments. We also found evidence of local adaptation by sympatric benthic and limnetic ecotypes to different light environments within lakes. Our findings indicate rapid parallel evolution of the visual system to altered light conditions. The changes have not, however, yielded a close matching of spectrum-wide sensitivity to wavelength availability, for reasons we discuss

The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome.

BACKGROUND: Many different environmental and genetic sex-determination mechanisms are found in nature. Closely related species can use different master sex-determination switches, suggesting that these developmental pathways can evolve very rapidly. Previous cytological studies suggest that recently diverged species of stickleback fish have different sex chromosome complements. Here, we investigate the genetic and chromosomal mechanisms that underlie sex determination in the threespine stickleback (Gasterosteus aculeatus). RESULTS: Genome-wide linkage mapping identifies a single chromosome region at the distal end of linkage group (LG) 19, which controls male or female sexual development in threespine sticklebacks. Although sex chromosomes are not cytogenetically visible in this species, several lines of evidence suggest that LG 19 is an evolving sex chromosome system, similar to the XX female/XY male system in many other species: (1) males are consistently heterozygous for unique alleles in this region; (2) recombination between loci linked to the sex-determination region is reduced in male meiosis relative to female meiosis; (3) sequence analysis of X- and Y-specific bacterial artificial chromosome (BAC) clones from the sex-determination region reveals many sequence differences between the X- and Y-specific clones; and (4) the Y chromosome has accumulated transposable elements and local duplications. CONCLUSIONS: Taken together, our data suggest that threespine sticklebacks have a simple chromosomal mechanism for sex determination based on a nascent Y chromosome that is less than 10 million years old. Further analysis of the stickleback system will provide an exciting window into the evolution of sex-determination pathways and sex chromosomes in vertebrates

DNA fragility in the parallel evolution of pelvic reduction in stickleback fish

Evolution generates a remarkable breadth of living forms, but many traits evolve repeatedly, by mechanisms that are still poorly understood. A classic example of repeated evolution is the loss of pelvic hindfins in stickleback fish (Gasterosteus aculeatus). Repeated pelvic loss maps to recurrent deletions of a pelvic enhancer of the Pitx1 gene. Here, we identify molecular features contributing to these recurrent deletions. Pitx1 enhancer sequences form alternative DNA structures in vitro and increase double-strand breaks and deletions in vivo. Enhancer mutability depends on DNA replication direction and is caused by TG-dinucleotide repeats. Modeling shows that elevated mutation rates can influence evolution under demographic conditions relevant for sticklebacks and humans. DNA fragility may thus help explain why the same loci are often used repeatedly during parallel adaptive evolution

Analysis of ancestry heterozygosity suggests that hybrid incompatibilities in threespine stickleback are environment dependent

Hybrid incompatibilities occur when interactions between opposite ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are “intrinsic,” meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis using sequence data are scarce. In this article, we compiled genetic data for F(2) hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatus L.) that were born and raised in either the field (seminatural experimental ponds) or the laboratory (aquaria). Because selection against incompatibilities results in elevated ancestry heterozygosity, we tested the prediction that ancestry heterozygosity will be higher in pond-raised fish compared to those raised in aquaria. We found that ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Additional analyses support a phenotypic basis for incompatibility and suggest that environment-specific single-locus heterozygote advantage is not the cause of selection on ancestry heterozygosity. Our study provides evidence that, in stickleback, a coarse—albeit indirect—signal of environment-dependent hybrid incompatibility is reliably detectable and suggests that extrinsic incompatibilities can evolve before intrinsic incompatibilities