Genetics of adaptation

The rediscovery of Mendel’s work showing that the heredity of phenotypes is controlled by discrete genes was followed by the reconciliation of Mendelian genetics with evolution by natural selection in the middle of the last century with the Modern Synthesis. In the past two decades, dramatic advances in genomic methods have facilitated the identification of the loci, genes, and even individual mutations that underlie phenotypic variants that are the putative targets of natural selection. Moreover, these methods have also changed how we can study adaptation by flipping the problem around, allowing us to first examine what loci show evidence of having been under selection, and then connecting these genetic variants to phenotypic variation. As a result, we now have an expanding list of actual genetic changes that underlie potentially adaptive phenotypic variation. Here, we synthesize how considering the effects of these adaptive loci in the context of cellular environments, genomes, organisms, and populations has provided new insights to the genetic architecture of adaptation

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

Divergence of male courtship displays between sympatric forms of anadromous threespine stickleback

Courtship displays are an important component of animal reproduction, and divergence in these displays can play an integral role in promoting or maintaining reproductive isolation between species. The courtship behaviour of the threespine stickleback (Gasterosteus aculeatus) has been extensively characterized. In Japan, there are two lineages of threespine stickleback that are genetically differentiated and reproductively isolated when found in regions of sympatry. We have previously shown that males of the Pacific Ocean lineage perform the zig-zag dance, while sympatric males of the Japan Sea lineage perform a different dance, which we have termed the rolling dance (Kitano et al., 2007, Biol. J. Linn. Soc. 91: 671-685). As a first step towards understanding the role of the courtship display in female mate choice and sexual isolation between this sympatric pair, we conducted a more detailed analysis of divergence between the courtship displays of the Pacific Ocean and Japan Sea males. Kinematic analysis revealed that the tempo of the zig-zag dance is two times faster than the tempo of the rolling dance. A detailed analysis of head movements during the courtship dance revealed that the Japan Sea males erect their gill covers, extend their red throats, and open their mouths more frequently during the rolling dance than the Pacific Ocean males do during the zig-zag dance. These results demonstrate that there is extensive divergence between sympatric Pacific Ocean and Japan Sea males in both the motor patterns and the tempo of their courtship displays. Thus, the Japanese sympatric stickleback pair provides a good system to study the role of courtship behaviour in speciation, as well as the genetic mechanisms that underlie the divergence of kinematics and motor patterns in courtship behaviour

Are homologies in vertebrate sex determination due to shared ancestry or to limited options?

The bewildering array of different sex-determination systems in vertebrates is built on a common set of genes and chromosomes

Contrasting hybridization rates between sympatric three-spined sticklebacks highlight the fragility of reproductive barriers between evolutionarily young species.

Three-spined sticklebacks (Gasterosteus aculeatus) are a powerful evolutionary model system due to the rapid and repeated phenotypic divergence of freshwater forms from a marine ancestor throughout the Northern Hemisphere. Many of these recently derived populations are found in overlapping habitats, yet are reproductively isolated from each other. This scenario provides excellent opportunities to investigate the mechanisms driving speciation in natural populations. Genetically distinguishing between such recently derived species, however, can create difficulties in exploring the ecological and genetic factors defining species boundaries, an essential component to our understanding of speciation. We overcame these limitations and increased the power of analyses by selecting highly discriminatory markers from the battery of genetic markers now available. Using species diagnostic molecular profiles, we quantified levels of hybridization and introgression within three sympatric species pairs of three-spined stickleback. Sticklebacks within Priest and Paxton lakes exhibit a low level of natural hybridization and provide support for the role of reinforcement in maintaining distinct species in sympatry. In contrast, our study provides further evidence for a continued breakdown of the Enos Lake species pair into a hybrid swarm, with biased introgression of the 'limnetic' species into that of the 'benthic'; a situation that highlights the delicate balance between persistence and breakdown of reproductive barriers between young species. A similar strategy utilizing the stickleback microsatellite resource can also be applied to answer an array of biological questions in other species' pair systems in this geographically widespread and phenotypically diverse model organism

Phenotypic divergence and reproductive isolation between sympatric forms of Japanese threespine sticklebacks

The threespine stickleback (Gasterosteus aculeatus) species complex is well suited for identifying the types of phenotypic divergence and isolating barriers that contribute to reproductive isolation at early stages of speciation. In the present study, we characterize the patterns of genetic and phenotypic divergence as well as the types of isolating barriers that are present between two sympatric pairs of threespine sticklebacks in Hokkaido, Japan. One sympatric pair consists of an anadromous and a resident freshwater form and shows divergence in body size between the forms, despite the lack of genetic differentiation between them. The second sympatric pair consists of two anadromous forms, which originated before the last glacial period and are currently reproductively isolated. These two anadromous forms have diverged in many morphological traits as well as in their reproductive behaviours. Both sexual isolation and hybrid male sterility contribute to reproductive isolation between the anadromous species pair. We discuss the shared and unique aspects of phenotypic divergence and reproductive isolation in the Japanese sympatric pairs compared with postglacial stickleback species pairs. Further studies of these divergent species pairs will provide a deeper understanding of the mechanisms of speciation in sticklebacks. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 671–685

Identification of a candidate sex determination gene in Culaea inconstans suggests convergent recruitment of an Amh duplicate in two lineages of stickleback.

Sex chromosomes vary greatly in their age and levels of differentiation across the tree of life. This variation is largely due to the rates of sex chromosome turnover in different lineages; however, we still lack an explanation for why sex chromosomes are so conserved in some lineages (e.g. mammals, birds) but so labile in others (e.g. teleosts, amphibians). To identify general mechanisms driving transitions in sex determination systems or forces which favour their conservation, we first require empirical data on sex chromosome systems from multiple lineages. Stickleback fishes are a valuable model lineage for the study of sex chromosome evolution due to variation in sex chromosome systems between closely-related species. Here, we identify the sex chromosome and a strong candidate for the master sex determination gene in the brook stickleback, Culaea inconstans. Using whole-genome sequencing of wild-caught samples and a lab cross, we identify AmhY, a male specific duplication of the gene Amh, as the candidate master sex determination gene. AmhY resides on Chromosome 20 in C. inconstans and is likely a recent duplication, as both AmhY and the sex-linked region of Chromosome 20 show little sequence divergence. Importantly, this duplicate AmhY represents the second independent duplication and recruitment of Amh as the sex determination gene in stickleback and the eighth example known across teleosts. We discuss this convergence in the context of sex chromosome turnovers and the role that the Amh/AmhrII pathway, which is crucial for sex determination, may play in the evolution of sex chromosomes in teleosts

Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks.

Experimental work has provided evidence for extrinsic post-zygotic isolation, a phenomenon unique to ecological speciation. The role that ecological components to reduced hybrid fitness play in promoting speciation and maintaining species integrity in the wild, however, is not as well understood. We addressed this problem by testing for selection against naturally occurring hybrids in two sympatric species pairs of benthic and limnetic threespine sticklebacks (Gasterosteus aculeatus). If post-zygotic isolation is a significant reproductive barrier, the relative frequency of hybrids within a population should decline significantly across the life-cycle. Such a trend in a natural population would give independent support to experimental evidence for extrinsic, rather than intrinsic, post-zygotic isolation in this system. Indeed, tracing mean individual hybridity (genetic intermediateness) across three life-history stages spanning four generations revealed just such a decline. This provides compelling evidence that extrinsic selection plays an important role in maintaining species divergence and supports a role for ecological speciation in sticklebacks

Sex Differences in Recombination in Sticklebacks.

Recombination often differs markedly between males and females. Here we present the first analysis of sex-specific recombination in Gasterosteus sticklebacks. Using whole-genome sequencing of 15 crosses between G. aculeatus and G. nipponicus, we localized 698 crossovers with a median resolution of 2.3 kb. We also used a bioinformatic approach to infer historical sex-averaged recombination patterns for both species. Recombination is greater in females than males on all chromosomes, and overall map length is 1.64 times longer in females. The locations of crossovers differ strikingly between sexes. Crossovers cluster toward chromosome ends in males, but are distributed more evenly across chromosomes in females. Suppression of recombination near the centromeres in males causes crossovers to cluster at the ends of long arms in acrocentric chromosomes, and greatly reduces crossing over on short arms. The effect of centromeres on recombination is much weaker in females. Genomic differentiation between G. aculeatus and G. nipponicus is strongly correlated with recombination rate, and patterns of differentiation along chromosomes are strongly influenced by male-specific telomere and centromere effects. We found no evidence for fine-scale correlations between recombination and local gene content in either sex. We discuss hypotheses for the origin of sexual dimorphism in recombination and its consequences for sexually antagonistic selection and sex chromosome evolution

Perspectives on the genetic architecture of divergence in body shape in sticklebacks

Synopsis The body shape of fishes encompasses a number of morphological traits that are intrinsically linked to functional systems and affect various measures of performance, including swimming, feeding, and avoiding predators. Changes in shape can allow a species to exploit a new ecological niche and can lead to ecological speciation. Body shape results from the integration of morphological, behavioral and physiological traits. It has been well established that functional interdependency among traits plays a large role in constraining the evolution of shape, affecting both the speed and the repeated evolution of particular body shapes. However, it is less clear what role genetic or developmental constraints might play in biasing the rate or direction of the evolution of body shape. Here, we suggest that the threespine stickleback (Gasterosteus aculeatus) is a powerful model system in which to address the extent to which genetic or developmental constraints play a role in the evolution of body shape in fishes. We review the existing data that begins to address these issues in sticklebacks and provide suggestions for future areas of research that will be particularly fruitful for illuminating the mechanisms that contribute to the evolution of body shape in fishes