The ecological and genomic basis of explosive adaptive radiation.

Speciation rates vary considerably among lineages, and our understanding of what drives the rapid succession of speciation events within young adaptive radiations remains incomplete1-11. The cichlid fish family provides a notable example of such variation, with many slowly speciating lineages as well as several exceptionally large and rapid radiations12. Here, by reconstructing a large phylogeny of all currently described cichlid species, we show that explosive speciation is solely concentrated in species flocks of several large young lakes. Increases in the speciation rate are associated with the absence of top predators; however, this does not sufficiently explain explosive speciation. Across lake radiations, we observe a positive relationship between the speciation rate and enrichment of large insertion or deletion polymorphisms. Assembly of 100 cichlid genomes within the most rapidly speciating cichlid radiation, which is found in Lake Victoria, reveals exceptional 'genomic potential'-hundreds of ancient haplotypes bear insertion or deletion polymorphisms, many of which are associated with specific ecologies and shared with ecologically similar species from other older radiations elsewhere in Africa. Network analysis reveals fundamentally non-treelike evolution through recombining old haplotypes, and the origins of ecological guilds are concentrated early in the radiation. Our results suggest that the combination of ecological opportunity, sexual selection and exceptional genomic potential is the key to understanding explosive adaptive radiation.

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 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.

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.

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.

Cycles of fusion and fission enabled rapid parallel adaptive radiations in African cichlids.

Although some lineages of animals and plants have made impressive adaptive radiations when provided with ecological opportunity, the propensities to radiate vary profoundly among lineages for unknown reasons. In Africa's Lake Victoria region, one cichlid lineage radiated in every lake, with the largest radiation taking place in a lake less than 16,000 years old. We show that all of its ecological guilds evolved in situ. Cycles of lineage fusion through admixture and lineage fission through speciation characterize the history of the radiation. It was jump-started when several swamp-dwelling refugial populations, each of which were of older hybrid descent, met in the newly forming lake, where they fused into a single population, resuspending old admixture variation. Each population contributed a different set of ancient alleles from which a new adaptive radiation assembled in record time, involving additional fusion-fission cycles. We argue that repeated fusion-fission cycles in the history of a lineage make adaptive radiation fast and predictable.

Genomic changes underlying repeated niche shifts in an adaptive radiation.

In adaptive radiations, single lineages rapidly diversify by adapting to many new niches. Little is known yet about the genomic mechanisms involved, that is, the source of genetic variation or genomic architecture facilitating or constraining adaptive radiation. Here, we investigate genomic changes associated with repeated invasion of many different freshwater niches by threespine stickleback in the Haida Gwaii archipelago, Canada, by resequencing single genomes from one marine and 28 freshwater populations. We find 89 likely targets of parallel selection in the genome that are enriched for old standing genetic variation. In contrast to theoretical expectations, their genomic architecture is highly dispersed with little clustering. Candidate genes and genotype-environment correlations match the three major environmental axes predation regime, light environment, and ecosystem size. In a niche space with these three dimensions, we find that the more divergent a new niche from the ancestral marine habitat, the more loci show signatures of parallel selection. Our findings suggest that the genomic architecture of parallel adaptation in adaptive radiation depends on the steepness of ecological gradients and the dimensionality of the niche space.

Genomic architecture of adaptive radiation and hybridization in Alpine whitefish.

Adaptive radiations represent some of the most remarkable explosions of diversification across the tree of life. However, the constraints to rapid diversification and how they are sometimes overcome, particularly the relative roles of genetic architecture and hybridization, remain unclear. Here, we address these questions in the Alpine whitefish radiation, using a whole-genome dataset that includes multiple individuals of each of the 22 species belonging to six ecologically distinct ecomorph classes across several lake-systems. We reveal that repeated ecological and morphological diversification along a common environmental axis is associated with both genome-wide allele frequency shifts and a specific, larger effect, locus, associated with the gene edar. Additionally, we highlight the possible role of introgression between species from different lake-systems in facilitating the evolution and persistence of species with unique trait combinations and ecology. These results highlight the importance of both genome architecture and secondary contact with hybridization in fuelling adaptive radiation.

Correlational selection in the age of genomics.

Ecologists and evolutionary biologists are well aware that natural and sexual selection do not operate on traits in isolation, but instead act on combinations of traits. This long-recognized and pervasive phenomenon is known as multivariate selection, or-in the particular case where it favours correlations between interacting traits-correlational selection. Despite broad acknowledgement of correlational selection, the relevant theory has often been overlooked in genomic research. Here, we discuss theory and empirical findings from ecological, quantitative genetic and genomic research, linking key insights from different fields. Correlational selection can operate on both discrete trait combinations and quantitative characters, with profound implications for genomic architecture, linkage, pleiotropy, evolvability, modularity, phenotypic integration and phenotypic plasticity. We synthesize current knowledge and discuss promising research approaches that will enable us to understand how correlational selection shapes genomic architecture, thereby linking quantitative genetic approaches with emerging genomic methods. We suggest that research on correlational selection has great potential to integrate multiple fields in evolutionary biology, including developmental and functional biology, ecology, quantitative genetics, phenotypic polymorphisms, hybrid zones and speciation processes.

A Combinatorial View on Speciation and Adaptive Radiation.

Speciation is often thought of as a slow process due to the waiting times for mutations that cause incompatibilities, and permit ecological differentiation or assortative mating. Cases of rapid speciation and particularly cases of rapid adaptive radiation into multiple sympatric species have remained somewhat mysterious. We review recent findings from speciation genomics that reveal an emerging commonality among such cases: reassembly of old genetic variation into new combinations facilitating rapid speciation and adaptive radiation. The polymorphisms in old variants frequently originated from hybridization at some point in the past. We discuss why old variants are particularly good fuel for rapid speciation, and hypothesize that variation in access to such old variants might contribute to the large variation in speciation rates observed in nature.

Admixture between old lineages facilitated contemporary ecological speciation in Lake Constance stickleback.

Ecological speciation can sometimes rapidly generate reproductively isolated populations coexisting in sympatry, but the origin of genetic variation permitting this is rarely known. We previously explored the genomics of very recent ecological speciation into lake and stream ecotypes in stickleback from Lake Constance. Here, we reconstruct the origin of alleles underlying ecological speciation by combining demographic modelling on genome-wide single nucleotide polymorphisms, phenotypic data and mitochondrial sequence data in the wider European biogeographical context. We find that parallel differentiation between lake and stream ecotypes across replicate lake-stream ecotones resulted from recent secondary contact and admixture between old East and West European lineages. Unexpectedly, West European alleles that introgressed across the hybrid zone at the western end of the lake, were recruited to genomic islands of differentiation between ecotypes at the eastern end of the lake. Our results highlight an overlooked outcome of secondary contact: ecological speciation facilitated by admixture variation.

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.

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'.

Ancient hybridization fuels rapid cichlid fish adaptive radiations.

Understanding why some evolutionary lineages generate exceptionally high species diversity is an important goal in evolutionary biology. Haplochromine cichlid fishes of Africa's Lake Victoria region encompass >700 diverse species that all evolved in the last 150,000 years. How this 'Lake Victoria Region Superflock' could evolve on such rapid timescales is an enduring question. Here, we demonstrate that hybridization between two divergent lineages facilitated this process by providing genetic variation that subsequently became recombined and sorted into many new species. Notably, the hybridization event generated exceptional allelic variation at an opsin gene known to be involved in adaptation and speciation. More generally, differentiation between new species is accentuated around variants that were fixed differences between the parental lineages, and that now appear in many new combinations in the radiation species. We conclude that hybridization between divergent lineages, when coincident with ecological opportunity, may facilitate rapid and extensive adaptive radiation.

Morphometric, Behavioral, and Genomic Evidence for a New Orangutan Species.

Six extant species of non-human great apes are currently recognized: Sumatran and Bornean orangutans, eastern and western gorillas, and chimpanzees and bonobos [1]. However, large gaps remain in our knowledge of fine-scale variation in hominoid morphology, behavior, and genetics, and aspects of great ape taxonomy remain in flux. This is particularly true for orangutans (genus: Pongo), the only Asian great apes and phylogenetically our most distant relatives among extant hominids [1]. Designation of Bornean and Sumatran orangutans, P. pygmaeus (Linnaeus 1760) and P. abelii (Lesson 1827), as distinct species occurred in 2001 [1, 2]. Here, we show that an isolated population from Batang Toru, at the southernmost range limit of extant Sumatran orangutans south of Lake Toba, is distinct from other northern Sumatran and Bornean populations. By comparing cranio-mandibular and dental characters of an orangutan killed in a human-animal conflict to those of 33 adult male orangutans of a similar developmental stage, we found consistent differences between the Batang Toru individual and other extant Ponginae. Our analyses of 37 orangutan genomes provided a second line of evidence. Model-based approaches revealed that the deepest split in the evolutionary history of extant orangutans occurred ∼3.38 mya between the Batang Toru population and those to the north of Lake Toba, whereas both currently recognized species separated much later, about 674 kya. Our combined analyses support a new classification of orangutans into three extant species. The new species, Pongo tapanuliensis, encompasses the Batang Toru population, of which fewer than 800 individuals survive. VIDEO ABSTRACT.

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.