Phylogenomics of the killer whale indicates ecotype divergence in sympatry

For many highly mobile species, the marine environment presents few obvious barriers to gene flow. Even so, there is considerable diversity within and among species, referred to by some as the ‘marine speciation paradox''. The recent and diverse radiation of delphinid cetaceans (dolphins) represents a good example of this. Delphinids are capable of extensive dispersion and yet many show fine-scale genetic differentiation among populations. Proposed mechanisms include the division and isolation of populations based on habitat dependence and resource specializations, and habitat release or changing dispersal corridors during glacial cycles. Here we use a phylogenomic approach to investigate the origin of differentiated sympatric populations of killer whales (Orcinus orca). Killer whales show strong specialization on prey choice in populations of stable matrifocal social groups (ecotypes), associated with genetic and phenotypic differentiation. Our data suggest evolution in sympatry among populations of resource specialists.     

Population genomics and the causes of local differentiation

Exactly 50 years ago, a revolution in empirical population genetics began with the introduction of methods for detecting allelic variation using protein electrophoresis (Throckmorton 1962; Hubby 1963; Lewontin & Hubby 1966). These pioneering scientists showed that populations are chock‐full of genetic variation. This variation was a surprise that required a re‐thinking of evolutionary genetic heuristics. Understanding the causes for the maintenance of this variation became and remains a major area of research. In the process of addressing the causes, this same group of scientists documented geographical genetic structure (Prakash et al. 1969), spawning the continued accumulation of what is now a huge case study catalogue of geographical differentiation (e.g. Loveless & Hamrick 1984; Linhart & Grant 1996). Geographical differentiation is clearly quite common. Yet, a truly general understanding of the patterns in and causes of spatial genetic structure across the genome remains elusive. To what extent is spatial structure driven by drift and phylogeography vs. geographical differences in environmental sources of selection? What proportion of the genome participates? A general understanding requires range‐wide data on spatial patterning of variation across the entire genome. In this issue of Molecular Ecology, Lasky et al. (2012) make important strides towards addressing these issues, taking advantage of three contemporary revolutions in evolutionary biology. Two are technological: high‐throughput sequencing and burgeoning computational power. One is cultural: open access to data from the community of scientists and especially data sets that result from large collaborative efforts. Together, these developments may at last put answers within reach.     

The role of structural genomic variants in population differentiation and ecotype formation in Timema cristinae walking sticks

Theory predicts that structural genomic variants such as inversions can promote adaptive diversification and speciation. Despite increasing empirical evidence that adaptive divergence can be triggered by one or a few large inversions, the degree to which widespread genomic regions under divergent selection are associated with structural variants remains unclear. Here we test for an association between structural variants and genomic regions that underlie parallel host‐plant‐associated ecotype formation in Timema cristinae stick insects. Using mate‐pair resequencing of 20 new whole genomes we find that moderately sized structural variants such as inversions, deletions and duplications are widespread across the genome, being retained as standing variation within and among populations. Using 160 previously published, standard‐orientation whole genome sequences we find little to no evidence that the DNA sequences within inversions exhibit accentuated differentiation between ecotypes. In contrast, a formerly described large region of reduced recombination that harbours genes controlling colour‐pattern exhibits evidence for accentuated differentiation between ecotypes, which is consistent with differences in the frequency of colour‐pattern morphs between host‐associated ecotypes. Our results suggest that some types of structural variants (e.g., large inversions) are more likely to underlie adaptive divergence than others, and that structural variants are not required for subtle yet genome‐wide genetic differentiation with gene flow.     

Population genomic analyses reveal possible drivers of population divergence

Recent advances in sequencing technology and efficiency enable new and improved methods to investigate how populations diverge and species evolve. Fungi have relatively small and simple genomes and can often be cultured in the laboratory. Fungal populations can thus be sequenced for a relatively low cost, which makes them ideal for population genomic analyses. In several recent population genomic studies, wild populations of fungal model organisms and human pathogens have been analysed, for example Neurospora crassa (Ellison et al. 2011 ), Saccharomyces uvarum (Almeida et al. 2014 ), Coccidioides spp. (Neafsey et al. 2010 ) and Cryptococcus gatti (Engelthaler et al. 2014 ). In this issue of Molecular Ecology, Branco et al. ( 2015 ) apply population genomic tools to understand population divergence and adaptation in a symbiotic (mycorrhizal) fungus. This study exemplifies the possibilities of diving deeper into the genomic features involved in population divergence and speciation, also for nonmodel organisms, and how molecular and analytical tools will improve our understanding of the patterns and mechanisms that underlie adaptation to habitats, population divergence and dispersal limitation of fungi.     

The genomics of adaptation,divergence and speciation: a congealing theory

In this issue, Flaxman et al. ( 2014 ) report the results of sophisticated whole‐genome simulations of speciation with gene flow, enhancing our understanding of the process by building on previous single‐locus, multilocus and analytical works. Their findings provide us with new insights about how genomes can diverge and the importance of statistical and chromosomal linkage in facilitating reproductive isolation. The authors characterize the conditions under which, even with high gene flow and weak divergent selection, reproductive isolation between populations can occur due to the emergent stochastic process of genomewide congealing, where numerous statistically or physically linked loci of small effect allow selection to limit effective migration rates. The initial congealing event can occur within a broad range conditions, and once initiated, the self‐reinforcing process leads to rapid divergence and ultimately two reproductively isolated populations. Flaxman et al.'s ( 2014 ) work is a valuable contribution to our understanding of speciation with gene flow and in making a more predictive field of evolutionary genomics and speciation.     

Influence of voltine ecotype and geographic distance on genetic and haplotype variation in the Asian corn borer

Diapause is an adaptive dormancy strategy by which arthropods endure extended periods of adverse climatic conditions. Seasonal variation in larval diapause initiation and duration in Ostrinia furnacalis may influence adult mating generation number (voltinism) across different local environments. The degree to which voltine ecotype, geographic distance, or other ecological factors influence O. furnacalis population genetic structure remains uncertain. Genetic differentiation was estimated between voltine ecotypes collected from 8 locations. Mitochondrial haplotypes were significantly different between historically allopatric univoltine and bivoltine locations, but confounded by a strong correlation with geographic distance. In contrast, single nucleotide polymorphism (SNP) genotypes show low but significant levels of variation and a lack of influence of geographic distance between allopatric voltine locations. Regardless, 11 of 257 SNP loci were predicted to be under selection, suggesting population genetic homogenization except at loci proximal to factors putatively under selection. These findings provide evidence of haplotype divergent voltine ecotypes that may be maintained in allopatric and sympatric areas despite relatively high rates of nuclear gene flow, yet influence of voltinism on maintenance of observed haplotype divergence remains unresolved.     

Between a whale bone and the deep blue sea: the provenance of dwarf males in whale bone-eating tubeworms

When researchers first caught a glimpse of the lush carpet of pink tubeworms covering the scattered bones of a dead grey whale 2900 m below the surface of Monterey Bay, the excitement onboard the Western Flyer (the mother ship of the remotely operated vehicle the Tiburon) must have been electrifying. The discovery of a new genus and several species of whale bone-eating Osedax tubeworms (Annelida, Siboglinidae) a mere 6 years ago from the deep sea was itself noteworthy. But what the researchers peering into the video monitors aboard the Western Flyer could not have known at that moment was that in the gelatinous tubes of those worms clung even more peculiar forms: harems of tiny, paedomorphic males of Osedax, numbering in the hundreds at times. Whereas female tubeworms bore into the marrow of whale bones (possibly via enzymes from their endosymbiotic bacteria), the dwarf males secondarily colonize the tubes of the resident females. The number of males in a female's tube increases over time in a curvilinear fashion. Dwarf males are known from all Osedax species examined to date, yet the origin of the males was an open question. In this issue, Vrijenhoek et al. provide compelling evidence that dwarf males found in the tubes of female Osedax worms are derived from a common larval pool and are unlikely to be the sons of host females or the progeny of females in the local genetic neighbourhood. This study provides an important foundation for future work on the ecology and evolution of extreme male dwarfism in Osedax and sexual size dimorphism more generally.     

Detecting the genomic signal of polygenic adaptation and the role of epistasis in evolution

Over the last decade, the genomic revolution has offered the possibility to generate tremendous amounts of data that contain valuable information on the genetic basis of phenotypic traits, such as those linked to human diseases or those that allow for species to adapt to a changing environment. Most ecologically relevant traits are controlled by a large number of genes with small individual effects on trait variation, but that are connected with one another through complex developmental, metabolic and biochemical networks. As a result, it has recently been suggested that most adaptation events in natural populations are reached via correlated changes at multiple genes at a time, for which the name polygenic adaptation has been coined. The current challenge is to develop methods to extract the relevant information from genomic data to detect the signature of polygenic evolutionary change. The symposium entitled “Detecting the Genomic Signal of Polygenic Adaptation and the Role of Epistasis in Evolution” held in 2017 at the University of Zürich aimed at reviewing our current state of knowledge. In this review, we use the talks of the invited speakers to summarize some of the most recent developments in this field.     

Divergent and linked selection shape patterns of genomic differentiation between European and North American Atlantic salmon (Salmo salar)

As populations diverge many processes can shape genomic patterns of differentiation. Regions of high differentiation can arise due to divergent selection acting on selected loci, genetic hitchhiking of nearby loci, or through repeated selection against deleterious alleles (linked background selection); this divergence may then be further elevated in regions of reduced recombination. Atlantic salmon (Salmo salar) from Europe and North America diverged >600,000 years ago and despite some evidence of secondary contact, the majority of genetic data indicate substantial divergence between lineages. This deep divergence with potential gene flow provides an opportunity to investigate the role of different mechanisms that shape the genomic landscape during early speciation. Here, using 184,295 single nucleotide polymorphisms (SNPs) and 80 populations, we investigate the genomic landscape of differentiation across the Atlantic Ocean with a focus on highly differentiated regions and the processes shaping them. We found evidence of high (mean F_ST = 0.26) and heterogeneous genomic differentiation between continents. Genomic regions associated with high trans‐Atlantic differentiation ranged in size from single loci (SNPs) within important genes to large regions (1–3 Mbp ) on four chromosomes (Ssa06, Ssa13, Ssa16 and Ssa19). These regions showed signatures consistent with selection, including high linkage disequilibrium, despite no significant reduction in recombination. Genes and functional enrichment of processes associated with differentiated regions may highlight continental differences in ocean navigation and parasite resistance. Our results provide insight into potential mechanisms underlying differences between continents, and evidence of near‐fixed and potentially adaptive trans‐Atlantic differences concurrent with a background of high genome‐wide differentiation supports subspecies designation in Atlantic salmon.     

Population genomics of marine fishes: identifying adaptive variation in space and time

Studies of adaptive evolution have experienced a recent revival in population genetics of natural populations and there is currently much focus on identifying genomic signatures of selection in space and time. Insights into local adaptation, adaptive response to global change and evolutionary consequences of selective harvesting can be generated through population genomics studies, allowing the separation of the effects invoked by neutral processes (drift-migration) from those due to selection. Such knowledge is important not only for improving our basic understanding of natural as well as human-induced evolutionary processes, but also for predicting future trajectories of biodiversity and for setting conservation priorities. Marine fishes possess a number of features rendering them well suited for providing general insights into adaptive genomic evolution in natural populations. These include well-described population structures, substantial and rapidly developing genomic resources and abundant archived samples enabling temporal studies. Furthermore, superior possibilities for conducting large-scale experiments under controlled conditions, due to the economic resources provided by the large and growing aquaculture industry, hold great promise for utilizing recent technological developments. Here, we review achievements in marine fish genomics to date and highlight potential avenues for future research, which will provide both general insights into evolution in high gene flow species, as well as specific knowledge which can lead to improved management of marine organisms.     

Butterfly genomics sheds light on the process of hybrid speciation

How common is hybridization between species and what effect does it have on the evolutionary process? Can hybridization generate new species and what indeed is a species? In this issue, Gompert et al. (2014) show how massive, genome‐scale data sets can be used to shed light on these questions. They focus on the Lycaeides butterflies, and in particular, several populations from the western USA, which have characteristics suggesting that they may contain hybrids of two or more different species (Gompert et al. 2006). They demonstrate that these populations do contain mosaic genomes made up of components from different parental species. However, this appears to have been largely driven by historical admixture, with more recent processes appearing to be isolating the populations from each other. Therefore, these populations are on their way to becoming distinct species (if they are not already) but have arisen following extensive hybridization between other distinct populations or species (Fig.  1 ).

Figure 1 Open in figure viewer PowerPoint There has been extensive historical admixture between Lycaeides species with some new species arising from hybrid populations. (Photo credits: Lauren Lucas, Chris Nice, and James Fordyce).

Their data set must be one of the largest outside of humans, with over one and half thousand butterflies genotyped at over 45 thousand variable nucleotide positions. It is this sheer amount of data that has allowed the researchers to distinguish between historical and more recent evolutionary and demographic processes. This is because it has allowed them to partition the data into common and rare genetic variants and perform separate analyses on these. Common genetic variants are likely to be older while rare variants are more likely to be due to recent mutations. Therefore, by splitting the genetic variation into these components, the researchers were able to show more admixture among common variants, while rare variants showed less admixture and clear separation of the populations. The extensive geographic sampling of individuals, including overlapping distributions of several of the putative species, also allowed the authors to rule out the possibility that the separation of the populations was simply due to geographical distance. The authors have developed a new programme for detecting population structure and admixture, which does the same job as STRUCTURE (Pritchard et al. 2000 ), identifying genetically distinct populations and admixture between these populations, but is designed to be used with next generation sequence data. They use the output of this model for another promising new method to distinguish between contemporary and historical admixtures. They fixed the number of source populations in the model at two and estimated the proportion of each individual's genome coming from these two populations. Therefore, an individual can either be purely population 1, or population 2 or some mixture of the two (they call this value q, the same parameter exists in STRUCTURE). They then compared this to the level of heterozygosity coming from the two source populations in the individual's genome. If an individual is an F1 hybrid of two source populations, then it would have a q of 0.5 and also be heterozygous at all loci that distinguish the parental populations. On the other hand, if it is a member of a stable hybrid lineage, it might also have a q of 0.5 but would not be expected to be heterozygous at these loci, because over time the population would become fixed for one or other of the source population states either by drift or selection (Fig.  2 ). This is indeed what they find in the hybrid populations. They tend to have intermediate q values, but the level of heterozygosity coming from the source populations (which they call Q₁₂) was consistently lower than expected.

Figure 2 Open in figure viewer PowerPoint The Q‐matrix analysis used by Gompert et al. ( 2014 ) to distinguish between contemporary (hybrid swarm) and historical (stable hybrid lineage) admixture.

Overall, the results support several of the populations as being stable hybrid lineages. Nevertheless, the strictest definitions of hybrid species specify that the process of hybridization between the parental species must be instrumental in driving the reproductive isolation of the new species from both parental populations (Abbott et al. 2013 ). This is extremely hard to demonstrate conclusively because it requires us to first of all identify the isolating mechanisms that operated in the early evolution of the species and then to show that these were caused by the hybridization event itself. One advantage of the Lycaeides system is that the species appear to be in the early stages of divergence, so barriers to gene flow that are operating currently are likely to be those that are driving the species divergence. While there is some evidence that hybridization gave rise to traits that allowed the new populations to colonize new environments (Gompert et al. 2006 ; Lucas et al. 2008 ), there is clearly further work to be carried out in this direction. One of the rare examples of homoploid hybrid speciation (hybrid speciation without a change in chromosome number) where the reproductive isolation criterion has been demonstrated, comes from the Heliconius butterflies. In this case, hybridization of two species has been shown to give rise to a new colour pattern that instantly becomes reproductively isolated from the parental species due to mate preference for that pattern (Mavárez et al. 2006 ). However, while this has become a widely accepted example (Abbott et al. 2013 ), the naturally occurring ‘hybrid species’ in fact has derived most of its genome from one of the parental species, with largely just the colour pattern controlling locus coming from the other parent, a process that has been termed ‘hybrid trait speciation’ (Salazar et al. 2010 ). This distinction is an important one in terms of our understanding of the organization of biological diversity. While hybrid trait speciation will still largely fit the model of a neatly branching evolutionary tree, with perhaps only the region surrounding the single introgressed gene deviating from this model, hybrid species that end up with mosaic genomes, like Lycaeides, will not fit this model when considering the genome as a whole. This distinction also more broadly applies when comparing the patterns of divergence between Heliconius and Lycaeides. These two butterfly genera have been driving forward our understanding of the prevalence and importance of hybridization at the genomic level, but they reveal different ways in which hybridization can influence the organization of biological diversity. Recent work in Heliconius has shown that admixture is extensive and has been ongoing over a large portion of the evolutionary history of species (Martin et al. 2013 ; Nadeau et al. 2013 ). Nevertheless, this has not obscured the clear and robust pattern of a bifurcating evolutionary tree when considering the genome as a whole (Nadeau et al. 2013 ). In contrast in Lycaeides, the genome‐wide phylogeny clearly does not fit a bifurcating tree, resembling more of a messy shrub, with hybrid taxa falling at intermediate positions on the phylogeny (Gompert et al. 2014 ). The extent to which we need to rethink the way we describe and organize biological diversity will depend on the relative prevalence of these different outcomes of hybridization. We are likely to see many more of these types of large sequence data sets for ecologically interesting organisms. Gompert et al. ( 2014 ) show that these data need not only be a quantitative advance, but can also qualitatively change our understanding of the evolutionary history of these organisms. In particular, analysing common and rare genetic variants separately may provide information that would otherwise be missed. The emerging field of ‘speciation genomics’ (Seehausen et al. 2014 ) should follow this lead in developing new ways of making the most of the flood of genomic data that is being generated, but also improve methods for integrating this with field observations and experiments to identify the sources and targets of selection and divergence.

References

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This article was written and figures prepared by N.N. except as specified in the text (photo credits).

Citing Literature

Number of times cited according to CrossRef: 4

• V. Alex Sotola, David S. Ruppel, Timothy H. Bonner, Chris C. Nice, Noland H. Martin, Asymmetric introgression between fishes in the Red River basin of Texas is associated with variation in water quality, Ecology and Evolution, 10.1002/ece3.4901, 9 , 4, (2083-2095), (2019). Wiley Online Library
• Matej Bocek, Dominik Kusy, Michal Motyka, Ladislav Bocak, Persistence of multiple patterns and intraspecific polymorphism in multi-species Müllerian communities of net-winged beetles, Frontiers in Zoology, 10.1186/s12983-019-0335-8, 16 , 1, (2019). Crossref
• Nicola J. Nadeau, Takeshi Kawakami, Population Genomics of Speciation and Admixture, , 10.1007/13836_2018_24, (2018). Crossref
• Amanda Roe, Julian Dupuis, Felix Sperling, Molecular Dimensions of Insect Taxonomy in the Genomics Era, Insect Biodiversity, 10.1002/9781118945568, (547-573), (2017). Wiley Online Library

Volume 23 , Issue 18 September 2014

Pages 4441-4443     

基于高通量测序的群体基因组学——植物病原真菌研究新方向

群体基因组学能够从全基因组水平揭示种群结构与进化、物种形成、适应性机制等。随着高通量技术的不断发展,基因组测序成本不断降低,大规模测序已成为可能。近几年被全基因组测序的真菌数量迅速增加,极大地促进了真菌群体基因组学的发展,加深了人们对植物病原真菌起源、遗传多样性、选择作用、致病性、毒力因子、杀菌剂抗药性、寄主专化型等生物学特性的认识。本文简要介绍了植物病原真菌的全基因测序以及比较基因组学的研究进展,重点综述了基于高通量测序的病原真菌群体基因组学的最新研究动态。群体基因组学将成为植物病原真菌一个新的研究方向。     

Genetic isolation of fragmented populations is exacerbated by drift and selection

Reduced genetic variation at marker loci in small populations has been well documented, whereas the relationship between quantitative genetic variation and population size has attracted little empirical investigation. Here we demonstrate that both neutral and quantitative genetic variation are reduced in small populations of a fragmented plant metapopulation, and that both drift and selective change are enhanced in small populations. Measures of neutral genetic differentiation (F(ST)) and quantitative genetic differentiation (Q(ST)) in two traits were higher among small demes, and Q(ST) between small populations exceeded that expected from drift alone. This suggests that fragmented populations experience both enhanced genetic drift and divergent selection on phenotypic traits, and that drift affects variation in both neutral markers and quantitative traits. These results highlight the need to integrate natural selection into conservation genetic theory, and suggests that small populations may represent reservoirs of genetic variation adaptive within a wide range of environments.     

Parallel introgression and selection on introduced alleles in a native species

As humans cause the redistribution of species ranges, hybridization between previously allopatric species is on the rise. Such hybridization can have complex effects on overall fitness of native species as new allelic combinations are tested. Widespread species introductions provide a unique opportunity to study selection on introgressed alleles in independent, replicated populations. We examined selection on alleles that repeatedly introgressed from introduced rainbow trout (Oncorhynchus mykiss) into native westslope cutthroat trout (Oncorhynchus clarkii lewisi) populations in western Canada. We found that the degree of introgression of individual single nucleotide polymorphisms from the invasive species into the native is correlated between independent watersheds. A number of rainbow trout alleles have repeatedly swept to high frequency in native populations, suggesting parallel adaptive advantages. Using simulations, we estimated large selection coefficients up to 0.05 favoring several rainbow trout alleles in the native background. Although previous studies have found reduced hybrid fitness and genome‐wide resistance to introgression in westslope cutthroat trout, our results suggest that some introduced genomic regions are strongly favored by selection. Our study demonstrates the utility of replicated introductions as case studies for understanding parallel adaptation and the interactions between selection and introgression across the genome. We suggest that understanding this variation, including consideration of beneficial alleles, can inform management strategies for hybridizing species.     

Population genomics fits the bill: genetics of adaptive beak variation in Darwin's finches

Darwin's finches are an iconic case of adaptive radiation. The size and shape of their beaks are key adaptive traits related to trophic niche that vary among species and evolve rapidly when the food supply changes. Building on recent studies, a paper in this issue of Molecular Ecology (Chaves et al. 2016 ) investigates the genomic basis of beak size variation in sympatric populations of three species of ground finch (Geospiza) by performing a Genome‐wide association study using RAD‐seq data. The authors find that variation in a small number of markers can explain a substantial proportion of variation in beak size. Some of these markers are in genomic regions that have previously been implicated in beak size variation in Darwin's finches, whereas other markers have not, suggesting both conservation and divergence in the genetic basis of morphological evolution. Overall, the study confirms that loci of large effect are involved in beak size variation, which helps to explain the high heritability and rapid response to selection of this trait. The independent identification of regions containing HMGA2 and DLK1 loci in a GWAS makes them prime targets for functional studies. The study also shows that under the right conditions, RAD‐seq can be a viable alternative to genome sequencing for GWAS in wild vertebrate populations.     

Divergent selection and drift shape the genomes of two avian sister species spanning a saline–freshwater ecotone

The role of species divergence due to ecologically based divergent selection—or ecological speciation—in generating and maintaining biodiversity is a central question in evolutionary biology. Comparison of the genomes of phylogenetically related taxa spanning a selective habitat gradient enables discovery of divergent signatures of selection and thereby provides valuable insight into the role of divergent ecological selection in speciation. Tidal marsh ecosystems provide tractable opportunities for studying organisms' adaptations to selective pressures that underlie ecological divergence. Sharp environmental gradients across the saline–freshwater ecotone within tidal marshes present extreme adaptive challenges to terrestrial vertebrates. Here, we sequence 20 whole genomes of two avian sister species endemic to tidal marshes—the saltmarsh sparrow (Ammospiza caudacutus) and Nelson's sparrow (A. nelsoni)—to evaluate the influence of selective and demographic processes in shaping genome‐wide patterns of divergence. Genome‐wide divergence between these two recently diverged sister species was notably high (genome‐wide F_ST = 0.32). Against a background of high genome‐wide divergence, regions of elevated divergence were widespread throughout the genome, as opposed to focused within islands of differentiation. These patterns may be the result of genetic drift resulting from past tidal march colonization events in conjunction with divergent selection to different environments. We identified several candidate genes that exhibited elevated divergence between saltmarsh and Nelson's sparrows, including genes linked to osmotic regulation, circadian rhythm, and plumage melanism—all putative candidates linked to adaptation to tidal marsh environments. These findings provide new insights into the roles of divergent selection and genetic drift in generating and maintaining biodiversity.