Marius Roesti

Genome divergence during evolutionary diversification as revealed in replicate lake-stream stickleback population pairs.

Evolutionary diversification is often initiated by adaptive divergence between populations occupying ecologically distinct environments while still exchanging genes. The genetic foundations of this divergence process are largely unknown and are here explored through genome scans in multiple independent lake-stream population pairs of threespine stickleback. We find that across the pairs, overall genomic divergence is associated with the magnitude of divergence in phenotypes known to be under divergent selection. Along this same axis of increasing diversification, genomic divergence becomes increasingly biased towards the centre of chromosomes as opposed to the peripheries. We explain this pattern by within-chromosome variation in the physical extent of hitchhiking, as recombination is greatly reduced in chromosome centres. Correcting for this effect suggests that a great number of genes distributed widely across the genome are involved in the divergence into lake vs. stream habitats. Analyzing additional allopatric population pairs, however, reveals that strong divergence in some genomic regions has been driven by selection unrelated to lake-stream ecology. Our study highlights a major contribution of large-scale variation in recombination rate to generating heterogeneous genomic divergence and indicates that elucidating the genetic basis of adaptive divergence might be more challenging than currently recognized.

Recombination in the threespine stickleback genome—patterns and consequences

Heterogeneity in recombination rate may strongly influence genome evolution and entail methodological challenges to genomic investigation. Nevertheless, a solid understanding of these issues awaits detailed information across a broad range of taxa. Based on 282 F2 individuals and 1872 single nucleotide polymorphisms, we characterize recombination in the threespine stickleback fish genome. We find an average genome‐wide recombination rate of 3.11 cm/Mb. Crossover frequencies are dramatically elevated in the chromosome peripheries as compared to the centres, and are consistent with one obligate crossover per chromosome (but not chromosome arm). Along the sex chromosome, we show that recombination is restricted to a small pseudoautosomal domain of c. 2 Mb, spanning only 10% of that chromosome. Comparing female to male RAD sequence coverage allows us to identify two discrete levels of degeneration on the Y chromosome, one of these ‘evolutionary strata’ coinciding with a previously inferred inverted region. Using polymorphism data from two young (<10 000 years old) ecologically diverged lake‐stream population pairs, we demonstrate that recombination rate correlates with both the magnitude of allele frequency shifts between populations and levels of genetic diversity within populations. These associations reflect genome‐wide heterogeneity in the influence of selection on linked sites. We further find a strong relationship between recombination rate and GC content, possibly driven by GC‐biased gene conversion. Overall, we highlight that heterogeneity in recombination rate has profound consequences on genome evolution and deserves wider recognition in marker‐based genomic analyses.

The genomic signature of parallel adaptation from shared genetic variation.

Parallel adaptation is common and may often occur from shared genetic variation, but the genomic consequences of this process remain poorly understood. We first use individual-based simulations to demonstrate that comparisons between populations adapted in parallel to similar environments from shared variation reveal a characteristic genomic signature around a selected locus: a low-divergence valley centred at the locus and flanked by twin peaks of high divergence. This signature is initiated by the hitchhiking of haplotype tracts differing between derived populations in the broader neighbourhood of the selected locus (driving the high-divergence twin peaks) and shared haplotype tracts in the tight neighbourhood of the locus (driving the low-divergence valley). This initial hitchhiking signature is reinforced over time because the selected locus acts as a barrier to gene flow from the source to the derived populations, thus promoting divergence by drift in its close neighbourhood. We next empirically confirm the peak-valley-peak signature by combining targeted and RAD sequence data at three candidate adaptation genes in multiple marine (source) and freshwater (derived) populations of threespine stickleback. Finally, we use a genome-wide screen for the peak-valley-peak signature to discover additional genome regions involved in parallel marine-freshwater divergence. Our findings offer a new explanation for heterogeneous genomic divergence and thus challenge the standard view that peaks in population divergence harbour divergently selected loci and that low-divergence regions result from balancing selection or localized introgression. We anticipate that genome scans for peak-valley-peak divergence signatures will promote the discovery of adaptation genes in other organisms.

Constraints on speciation suggested by comparing lake‐stream stickleback divergence across two continents

Adaptation to ecologically distinct environments can coincide with the emergence of reproductive barriers. The outcome of this process is highly variable and can range along a continuum from weak population differentiation all the way to complete, genome‐wide divergence. The factors determining how far diverging taxa will move along this continuum remain poorly understood but are most profitably investigated in taxa under replicate divergence. Here, we explore determinants of progress towards speciation by comparing phenotypic and molecular divergence within young (<150 years) lake‐stream stickleback pairs from Central Europe to divergence in older (thousands of years) archetypal lake‐stream pairs from Vancouver Island, Canada. We generally find relatively weak divergence in most aspects of foraging morphology (gill raker number, body shape) in the European pairs, although substantial adaptive divergence is seen in gill raker length. Combined with striking overall phenotypic differences between the continents, this argues for genetic and time constraints on adaptive divergence in the European pairs. The European lake‐stream pairs also do not display the strong habitat‐related differentiation in neutral (microsatellite) markers seen in the Canadian watersheds. This indicates either the lack of strong reproductive barriers owing to weak adaptive divergence, or alternatively that neutral markers are poorly suited for detecting reproductive barriers if these emerge rapidly. Overall, our comparative approach suggests constraints on speciation due to genetic architecture and limited time for divergence. The relative importance of these factors remains to be quantified by future investigation.

Uninformative polymorphisms bias genome scans for signatures of selection

BackgroundWith the establishment of high-throughput sequencing technologies and new methods for rapid and extensive single nucleotide (SNP) discovery, marker-based genome scans in search of signatures of divergent selection between populations occupying ecologically distinct environments are becoming increasingly popular.Methods and ResultsOn the basis of genome-wide SNP marker data generated by RAD sequencing of lake and stream stickleback populations, we show that the outcome of such studies can be systematically biased if markers with a low minor allele frequency are included in the analysis. The reason is that these ‘uninformative’ polymorphisms lack the adequate potential to capture signatures of drift and hitchhiking, the focal processes in ecological genome scans. Bias associated with uninformative polymorphisms is not eliminated by just avoiding technical artifacts in the data (PCR and sequencing errors), as a high proportion of SNPs with a low minor allele frequency is a general biological feature of natural populations.ConclusionsWe suggest that uninformative markers should be excluded from genome scans based on empirical criteria derived from careful inspection of the data, and that these criteria should be reported explicitly. Together, this should increase the quality and comparability of genome scans, and hence promote our understanding of the processes driving genomic differentiation.

The genomics of ecological vicariance in threespine stickleback fish.

Populations occurring in similar habitats and displaying similar phenotypes are increasingly used to explore parallel evolution at the molecular level. This generally ignores the possibility that parallel evolution can be mimicked by the fragmentation of an ancestral population followed by genetic exchange with ecologically different populations. Here we demonstrate such an ecological vicariance scenario in multiple stream populations of threespine stickleback fish divergent from a single adjacent lake population. On the basis of demographic and population genomic analyses, we infer the initial spread of a stream-adapted ancestor followed by the emergence of a lake-adapted population, that selective sweeps have occurred mainly in the lake population, that adaptive lake–stream divergence is maintained in the face of gene flow from the lake into the streams, and that this divergence involves major inversion polymorphisms also important to marine-freshwater stickleback divergence. Overall, our study highlights the need for a robust understanding of the demographic and selective history in evolutionary investigations.

Testing the stages model in the adaptive radiation of cichlid fishes in East African Lake Tanganyika

Adaptive radiation (AR) is a key process in the origin of organismal diversity. However, the evolution of trait disparity in connection with ecological specialization is still poorly understood. Available models for vertebrate ARs predict that diversification occurs in the form of temporal stages driven by different selective forces. Here, we investigate the AR of cichlid fishes in East African Lake Tanganyika and use macroevolutionary model fitting to evaluate whether diversification happened in temporal stages. Six trait complexes, for which we also provide evidence of their adaptiveness, are analysed with comparative methods: body shape, pharyngeal jaw shape, gill raker traits, gut length, brain weight and body coloration. Overall, we do not find strong evidence for the ‘stages model’ of AR. However, our results suggest that trophic traits diversify earlier than traits implicated in macrohabitat adaptation and that sexual communication traits (i.e. coloration) diversify late in the radiation.

GENETIC ARCHITECTURE OF SKELETAL EVOLUTION IN EUROPEAN LAKE AND STREAM STICKLEBACK

Advances in genomic techniques are greatly facilitating the study of molecular signatures of selection in diverging natural populations. Connecting these signatures to phenotypes under selection remains challenging, but benefits from dissections of the genetic architecture of adaptive divergence. We here perform quantitative trait locus (QTL) mapping using 488 F2 individuals and 2011 single nucleotide polymorphisms (SNPs) to explore the genetic architecture of skeletal divergence in a lake‐stream stickleback system from Central Europe. We find QTLs for gill raker, snout, and head length, vertebral number, and the extent of lateral plating (plate number and height). Although two large‐effect loci emerge, QTL effect sizes are generally small. Examining the neighborhood of the QTL‐linked SNPs identifies several genes involved in bone formation, which emerge as strong candidate genes for skeletal evolution. Finally, we use SNP data from the natural source populations to demonstrate that some SNPs linked to QTLs in our cross also exhibit striking allele frequency differences in the wild, suggesting a causal role of these QTLs in adaptive population divergence. Our study paves the way for comparative analyses across other (lake‐stream) stickleback populations, and for functional investigations of the candidate genes.

Repeated lake-stream divergence in stickleback life history within a Central European lake basin.

Life history divergence between populations inhabiting ecologically distinct habitats might be a potent source of reproductive isolation, but has received little attention in the context of speciation. We here test for life history divergence between threespine stickleback inhabiting Lake Constance (Central Europe) and multiple tributary streams. Otolith analysis shows that lake fish generally reproduce at two years of age, while their conspecifics in all streams have shifted to a primarily annual life cycle. This divergence is paralleled by a striking and consistent reduction in body size and fecundity in stream fish relative to lake fish. Stomach content analysis suggests that life history divergence might reflect a genetic or plastic response to pelagic versus benthic foraging modes in the lake and the streams. Microsatellite and mitochondrial markers further reveal that life history shifts in the different streams have occurred independently following the colonization by Lake Constance stickleback, and indicate the presence of strong barriers to gene flow across at least some of the lake-stream habitat transitions. Given that body size is known to strongly influence stickleback mating behavior, these barriers might well be related to life history divergence.

Depth-dependent abundance of Midas Cichlid fish (Amphilophus spp.) in two Nicaraguan crater lakes

The Midas Cichlid species complex (Amphilophus spp.) in Central America serves as a prominent model system to study sympatric speciation and parallel adaptive radiation, since small arrays of equivalent ecotype morphs have evolved independently in different crater lakes. While the taxonomy and evolutionary history of the different species are well resolved, little is known about basic ecological parameters of Midas Cichlid assemblages. Here, we use a line transect survey to investigate the depth-dependent abundance of Amphilophus spp. along the shores of two Nicaraguan crater lakes, Apoyo and Xiloá. We find a considerable higher density of Midas cichlids in Lake Xiloá as compared to Lake Apoyo, especially at the shallowest depth level. This might be due to the higher eutrophication level of Lake Xiloá and associated differences in food availability, and/or the presence of a greater diversity of niches in that lake. In any case, convergent forms evolved despite noticeable differences in size, age, eutrophication level, and carrying capacity. Further, our data provide abundance and density estimates for Midas Cichlid fish, which serve as baseline for future surveys of these ecosystems and are also relevant to past and future modeling of ecological speciation.