Natural selection interacts with recombination to shape the evolution of hybrid genomes

Schumer, Molly; Xu, Chenling; Powell, Daniel L.; Durvasula, Arun; Skov, Laurits; Holland, C. D.; Blazier, John C.; Sankararaman, Sriram; Andolfatto, Peter; Rosenthal, Gil G.; Przeworski, Molly

doi:10.1126/science.aar3684

Cited by 369 publications

(669 citation statements)

References 93 publications

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“…Instead, the source of archaic ancestry tracts in type B2 killer whales is better explained by ancestral population structure. This therefore requires a scenario in which these tracts were the minor component of the ancestry (i.e., the lineage that contributed less to the gene pool, see Schumer et al, ) of an admixed ancestral killer whale population between T Archaic and T Ingroup , and this ancestry was therefore already being broken up by recombination prior to T Ingroup (Figure a).…”

Section: Resultsmentioning

confidence: 99%

Killer whale genomes reveal a complex history of recurrent admixture and vicariance

et al. 2019

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Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree‐like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non‐Antarctic lineages is further driven by ancestry segments with up to four‐fold older coalescence time than the genome‐wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome‐wide data to sample the variation in ancestry within individuals.

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Section: Resultsmentioning

confidence: 99%

Killer whale genomes reveal a complex history of recurrent admixture and vicariance

et al. 2019

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“…In our fixed sliding window size of 50‐kb, we may have missed important patterns of introgression in regions of recombination hotspots, where such patterns are expected to be very localized (Schumer et al. ). Shared variation among species may reflect unsorted polymorphisms from structured ancestral populations rather than hybridization.…”

Section: Discussionmentioning

confidence: 99%

Don't throw out the sympatric speciation with the crater lake water: fine-scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation

2018

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Genomic data has revealed complex histories of colonization and repeated gene flow previously unrecognized in some of the most celebrated examples of sympatric speciation and radiation. However, much of the evidence for secondary gene flow into these radiations comes from summary statistics calculated from sparse genomic sampling without knowledge of which specific genomic regions introgressed. This tells us little about how gene flow potentially influenced sympatric diversification. Here, we investigated whole genomes of Barombi Mbo crater lake cichlids for fine‐scale patterns of introgression with neighboring riverine cichlid populations. We found evidence of secondary gene flow into the radiation scattered across <0.24% of the genome; however, from our analyses, it is not clear if the functional diversity in these regions contributed to the ecological, sexual, and morphological diversity found in the lake. Unlike similar studies, we found no obvious candidate genes for adaptive introgression and we cannot rule out that secondary gene flow was predominantly neutral with respect to the diversification process. We also found evidence for differential assortment of ancestral polymorphisms found in riverine populations between sympatric sister species, suggesting the presence of an ancestral hybrid swarm. Although the history of gene flow and colonization is more complicated than previously assumed, the lack of compelling evidence for secondary gene flow's role in species diversification suggests that we should not yet rule out one of the most celebrated examples of sympatric speciation in nature without a more thorough investigation of the timing and functional role of each introgressed region.

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“…[28,29]) can reduce gene flow between locally adapted populations (reviewed in [30]). More recently, studies have begun to test how selection shapes the distribution of hybrid genotypes found in nature using genome-wide data (e.g., [24,31,32]). By measuring ecologically relevant phenotypes of D. yakuba , D. teissieri , and their hybrids in the lab and the field, our findings extend this knowledge to demonstrate temperature-dependent asymmetries in the strength of RI between reciprocal crosses.…”

Section: Resultsmentioning

confidence: 99%

A Maladaptive Combination of Traits Contributes to the Maintenance of a Drosophila Hybrid Zone

et al. 2018

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Drosophila teissieri and D. yakuba diverged approximately 3 mya and are thought to share a large, ancestral, African range [1-3]. These species now co-occur in parts of continental Africa and in west Africa on the island of Bioko [1, 4]. While D. yakuba is a human commensal, D. teissieri seems to be associated with Parinari fruits, restricting its range to forests [4-6]. Genome data indicate introgression, despite no evidence of contemporary hybridization. Here we report the discovery of D. yakuba-D. teissieri hybrids at the interface of secondary forests and disturbed, open habitats on Bioko. We demonstrate that hybrids are the F progeny of D. yakuba females and D. teissieri males. At high temperatures like those found on Bioko, D. teissieri females are generally less receptive to mating, and in combination with temperature effects on egg lay and egg-to-adult viability, this decreases the potential for gene flow between female D. teissieri and male D. yakuba relative to the reciprocal cross. Field and laboratory experiments demonstrate that F hybrids have a maladaptive combination of D. yakuba behavior and D. teissieri physiology, generating additional barriers to gene flow. Nevertheless, analysis of introgressed and non-introgressed regions of the genome indicate that, while rare, gene flow is relatively recent. Our observations identify precise intrinsic and extrinsic factors that, along with hybrid male sterility, limit gene flow and maintain these species. These data contribute to a growing body of literature that suggests the Gulf of Guinea may be a hotspot for hybridization.

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Natural selection interacts with recombination to shape the evolution of hybrid genomes

Cited by 369 publications

References 93 publications

Killer whale genomes reveal a complex history of recurrent admixture and vicariance

Killer whale genomes reveal a complex history of recurrent admixture and vicariance

Don't throw out the sympatric speciation with the crater lake water: fine-scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation

A Maladaptive Combination of Traits Contributes to the Maintenance of a Drosophila Hybrid Zone

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