David Alexander Marques

Genomics and the origin of species

Speciation is a fundamental evolutionary process, the knowledge of which is crucial for understanding the origins of biodiversity. Genomic approaches are an increasingly important aspect of this research field. We review current understanding of genome-wide effects of accumulating reproductive isolation and of genomic properties that influence the process of speciation. Building on this work, we identify emergent trends and gaps in our understanding, propose new approaches to more fully integrate genomics into speciation research, translate speciation theory into hypotheses that are testable using genomic tools and provide an integrative definition of the field of speciation genomics.

Genomics of Rapid Incipient Speciation in Sympatric Threespine Stickleback

Ecological speciation is the process by which reproductively isolated populations emerge as a consequence of divergent natural or ecologically-mediated sexual selection. Most genomic studies of ecological speciation have investigated allopatric populations, making it difficult to infer reproductive isolation. The few studies on sympatric ecotypes have focused on advanced stages of the speciation process after thousands of generations of divergence. As a consequence, we still do not know what genomic signatures of the early onset of ecological speciation look like. Here, we examined genomic differentiation among migratory lake and resident stream ecotypes of threespine stickleback reproducing in sympatry in one stream, and in parapatry in another stream. Importantly, these ecotypes started diverging less than 150 years ago. We obtained 34,756 SNPs with restriction-site associated DNA sequencing and identified genomic islands of differentiation using a Hidden Markov Model approach. Consistent with incipient ecological speciation, we found significant genomic differentiation between ecotypes both in sympatry and parapatry. Of 19 islands of differentiation resisting gene flow in sympatry, all were also differentiated in parapatry and were thus likely driven by divergent selection among habitats. These islands clustered in quantitative trait loci controlling divergent traits among the ecotypes, many of them concentrated in one region with low to intermediate recombination. Our findings suggest that adaptive genomic differentiation at many genetic loci can arise and persist in sympatry at the very early stage of ecotype divergence, and that the genomic architecture of adaptation may facilitate this.

The genetic and molecular architecture of phenotypic diversity in sticklebacks

A major goal of evolutionary biology is to identify the genotypes and phenotypes that underlie adaptation to divergent environments. Stickleback fish, including the threespine stickleback (Gasterosteus aculeatus) and the ninespine stickleback (Pungitius pungitius), have been at the forefront of research to uncover the genetic and molecular architecture that underlies phenotypic diversity and adaptation. A wealth of quantitative trait locus (QTL) mapping studies in sticklebacks have provided insight into long-standing questions about the distribution of effect sizes during adaptation as well as the role of genetic linkage in facilitating adaptation. These QTL mapping studies have also provided a basis for the identification of the genes that underlie phenotypic diversity. These data have revealed that mutations in regulatory elements play an important role in the evolution of phenotypic diversity in sticklebacks. Genetic and molecular studies in sticklebacks have also led to new insights on the genetic basis of repeated evolution and suggest that the same loci are involved about half of the time when the same phenotypes evolve independently. When the same locus is involved, selection on standing variation and repeated mutation of the same genes have both contributed to the evolution of similar phenotypes in independent populations. This article is part of the themed issue ‘Evo-devo in the genomics era, and the origins of morphological diversity’.

Demographic modelling with whole-genome data reveals parallel origin of similar Pundamilia cichlid species after hybridization

Modes and mechanisms of speciation are best studied in young species pairs. In older taxa, it is increasingly difficult to distinguish what happened during speciation from what happened after speciation. Lake Victoria cichlids in the genus Pundamilia encompass a complex of young species and polymorphic populations. One Pundamilia species pair, P. pundamilia and P. nyererei, is particularly well suited to study speciation because sympatric population pairs occur with different levels of phenotypic differentiation and reproductive isolation at different rocky islands within the lake. Genetic distances between allopatric island populations of the same nominal species often exceed those between the sympatric species. It thus remained unresolved whether speciation into P. nyererei and P. pundamilia occurred once, followed by geographical range expansion and interspecific gene flow in local sympatry, or if the species pair arose repeatedly by parallel speciation. Here, we use genomic data and demographic modelling to test these alternative evolutionary scenarios. We demonstrate that gene flow plays a strong role in shaping the observed patterns of genetic similarity, including both gene flow between sympatric species and gene flow between allopatric populations, as well as recent and early gene flow. The best supported model for the origin of P. pundamilia and P. nyererei population pairs at two different islands is one where speciation happened twice, whereby the second speciation event follows shortly after introgression from an allopatric P. nyererei population that arose earlier. Our findings support the hypothesis that very similar species may arise repeatedly, potentially facilitated by introgressed genetic variation.

Divergent Macroparasite Infections in Parapatric Swiss Lake-Stream Pairs of Threespine Stickleback (Gasterosteus aculeatus).

Spatial heterogeneity in diversity and intensity of parasitism is a typical feature of most host-parasite interactions, but understanding of the evolutionary implications of such variation is limited. One possible outcome of infection heterogeneities is parasite-mediated divergent selection between host populations, ecotypes or species which may facilitate the process of ecological speciation. However, very few studies have described infections in population-pairs along the speciation continuum from low to moderate or high degree of genetic differentiation that would address the possibility of parasite-mediated divergent selection in the early stages of the speciation process. Here we provide an example of divergent parasitism in freshwater fish ecotypes by examining macroparasite infections in threespine stickleback (Gasterosteus aculeatus) of four Swiss lake systems each harbouring parapatric lake-stream ecotype pairs. We demonstrate significant differences in infections within and between the pairs that are driven particularly by the parasite taxa transmitted to fish from benthic invertebrates. The magnitude of the differences tended to correlate positively with the extent of neutral genetic differentiation between the parapatric lake and stream populations of stickleback, whereas no such correlation was found among allopatric populations from similar or contrasting habitats. This suggests that genetic differentiation is unrelated to the magnitude of parasite infection contrasts when gene flow is constrained by geographical barriers while in the absence of physical barriers, genetic differentiation and the magnitude of differences in infections tend to be positively correlated.

Genomic landscape of early ecological speciation initiated by selection on nuptial colour

Ecological speciation is the evolution of reproductive isolation as a consequence of direct divergent natural selection or ecologically mediated divergent sexual selection. While the genomic signature of the former has been extensively studied in recent years, only few examples exist for genomic differentiation where environment‐dependent sexual selection has played an important role. Here, we describe a very young (~90 years old) population of threespine sticklebacks exhibiting phenotypic and genomic differentiation between two habitats within the same pond. We show that differentiation among habitats is limited to male throat colour and nest type, traits known to be subject to sexual selection. Divergence in these traits mirrors divergence in much older benthic and limnetic stickleback species pairs from North American west coast lakes, which also occur in sympatry but are strongly reproductively isolated from each other. We demonstrate that in our population, differences in throat colour and breeding have been stable over a decade, but in contrast to North American benthic and limnetic stickleback species, these mating trait differences are not accompanied by divergence in morphology related to feeding, predator defence or swimming performance. Using genomewide SNP data, we find multiple genomic islands with moderate differentiation spread across several chromosomes, whereas the rest of the genome is undifferentiated. The islands contain potential candidate genes involved in visual perception of colour. Our results suggest that phenotypic and multichromosome genomic divergence of these morphs was driven by environment‐dependent sexual selection, demonstrating incipient speciation after only a few decades of divergence in sympatry.

Convergent evolution of SWS2 opsin facilitates adaptive radiation of threespine stickleback into different light environments

Repeated adaptation to a new environment often leads to convergent phenotypic changes whose underlying genetic mechanisms are rarely known. Here, we study adaptation of color vision in threespine stickleback during the repeated postglacial colonization of clearwater and blackwater lakes in the Haida Gwaii archipelago. We use whole genomes from 16 clearwater and 12 blackwater populations, and a selection experiment, in which stickleback were transplanted from a blackwater lake into an uninhabited clearwater pond and resampled after 19 y to test for selection on cone opsin genes. Patterns of haplotype homozygosity, genetic diversity, site frequency spectra, and allele-frequency change support a selective sweep centered on the adjacent blue- and red-light sensitive opsins SWS2 and LWS. The haplotype under selection carries seven amino acid changes in SWS2, including two changes known to cause a red-shift in light absorption, and is favored in blackwater lakes but disfavored in the clearwater habitat of the transplant population. Remarkably, the same red-shifting amino acid changes occurred after the duplication of SWS2 198 million years ago, in the ancestor of most spiny-rayed fish. Two distantly related fish species, bluefin killifish and black bream, express these old paralogs divergently in black- and clearwater habitats, while sticklebacks lost one paralog. Our study thus shows that convergent adaptation to the same environment can involve the same genetic changes on very different evolutionary time scales by reevolving lost mutations and reusing them repeatedly from standing genetic variation.

Genomics of Parallel Ecological Speciation in Lake Victoria Cichlids

Abstract The genetic basis of parallel evolution of similar species is of great interest in evolutionary biology. In the adaptive radiation of Lake Victoria cichlid fishes, sister species with either blue or red‐back male nuptial coloration have evolved repeatedly, often associated with shallower and deeper water, respectively. One such case is blue and red‐backed Pundamilia species, for which we recently showed that a young species pair may have evolved through “hybrid parallel speciation”. Coalescent simulations suggested that the older species P. pundamilia (blue) and P. nyererei (red‐back) admixed in the Mwanza Gulf and that new “nyererei‐like” and “pundamilia‐like” species evolved from the admixed population. Here, we use genome scans to study the genomic architecture of differentiation, and assess the influence of hybridization on the evolution of the younger species pair. For each of the two species pairs, we find over 300 genomic regions, widespread across the genome, which are highly differentiated. A subset of the most strongly differentiated regions of the older pair are also differentiated in the younger pair. These shared differentiated regions often show parallel allele frequency differences, consistent with the hypothesis that admixture‐derived alleles were targeted by divergent selection in the hybrid population. However, two‐thirds of the genomic regions that are highly differentiated between the younger species are not highly differentiated between the older species, suggesting independent evolutionary responses to selection pressures. Our analyses reveal how divergent selection on admixture‐derived genetic variation can facilitate new speciation events.

Experimental evidence for rapid genomic adaptation to a new niche in an adaptive radiation

A substantial part of biodiversity is thought to have arisen from adaptive radiations in which one lineage rapidly diversified into multiple lineages specialized to many different niches. However, selection and drift reduce genetic variation during adaptation to new niches and may thus prevent or slow down further niche shifts. We tested whether rapid adaptation is still possible from a highly derived ecotype in the adaptive radiation of threespine stickleback on the Haida Gwaii archipelago, Western Canada. In a 19-year selection experiment, we let giant sticklebacks from a large blackwater lake evolve in a small clearwater pond without vertebrate predators. A total of 56 whole genomes from the experiment and 26 natural populations revealed that adaptive genomic change was rapid in many small genomic regions and encompassed 75% of the change between 12,000-year-old ecotypes. Genomic change was as fast as phenotypic change in defence and trophic morphology, and both were largely parallel between the short-term selection experiment and long-term natural adaptive radiation. Our results show that functionally relevant standing genetic variation can persist in derived radiation members, allowing adaptive radiations to unfold very rapidly.Adaptation to a new niche results in reduced genetic variation and the ability of derived populations to adapt to new environments is unclear. Here, the authors show rapid adaptive genomic change in a derived ecotype in the adaptive radiation of threespine stickleback.

Adaptation despite gene flow? Low recombination helps

About 15,000 years earlier, the Northern half of Europe and North America was buried under a few kilometres of ice. Since then, many organisms have colonized and rapidly adapted to the new, vacant habitats. Some, like the threespine stickleback fish, have done so more successfully than others: from the sea, stickleback have adapted to a multitude of lake and stream habitats with a vast array of complex phenotypes and life histories. Previous studies showed that most of these “ecotypes” differ in multiple divergently selected genes throughout the genome. But how are well‐adapted ecotypes of one habitat protected from maladaptive gene flow from ecotypes of another, adjacent habitat? According to a From the Cover meta‐analysis in this issue of Molecular Ecology (Samuk et al., 2017), low recombination rate regions in the genome offer such protection. While inversions have often been highlighted as an efficient way to maintain linkage disequilibrium among sets of adaptive variants in the face of gene flow, Samuk et al. (2017) show that variation in recombination rate across the genome may perform a similar role in threespine stickleback. With this study, theoretical predictions for the importance of low recombination regions in adaptation are for the first time tested with a highly replicated population genomic data set. The findings from this study have implications for the adaptability of species, speciation and the evolution of genome architecture.