scholarly journals Locus-specific introgression in young hybrid swarms: drift dominates selection

2020 ◽  
Author(s):  
S. Eryn McFarlane ◽  
Helen V. Senn ◽  
Stephanie L. Smith ◽  
Josephine M. Pemberton
Keyword(s):  
Reproductive Isolation ◽  
Policy Implications ◽  
Secondary Contact ◽  
Hybrid Zones ◽  
Policy Makers ◽  
Adaptive Introgression ◽  
Allelic Replacement ◽  
Hybrid Swarms ◽  
Genome Wide ◽  
Future Work

AbstractClosely related species that have previously inhabited geographically separated ranges are hybridizing at an increasing rate due to human disruptions. These anthropogenic hybrid zones can be used to study reproductive isolation between species at secondary contact, including examining locus-specific rates of introgression. Introgression is expected to be heterogenous across the genome, reflecting variation in selection. Those loci that introgress especially slowly are good candidates for being involved in reproductive isolation, while those loci that introgress quickly may be involved in adaptive introgression. In the context of conservation, policy makers are especially concerned about introduced alleles moving quickly into the background of a native or endemic species, as these alleles could replace the native alleles in the population, leading to extinction via hybridization. We applied genomic cline analyses to 44997 SNPs to identify loci introgressing at excessive rates when compared to the genome wide expectation in an anthropogenic hybridizing population of red deer and sika in Kintyre Scotland. We found 11.4% of SNPs had cline centers that were significantly different from the genome wide expectation, and 17.6% had excessive rates of introgression. Based on simulations, we believe that many of these markers have diverged from average due to drift, rather than because of selection. Future work could determine the policy implications of allelic-replacement due to drift rather than selection, and could use replicate, geographically distinct hybrid zones to narrow down those loci that are indeed responding to selection in anthropogenic hybrid zones.

scholarly journals Genomic islands of divergence or opportunities for introgression?

2017 ◽  
Vol 284 (1850) ◽  
pp. 20162414 ◽  
Author(s):  
Rachael A. Bay ◽  
Kristen Ruegg
Keyword(s):  
Gene Flow ◽  
Reproductive Isolation ◽  
Genomic Islands ◽  
Secondary Contact ◽  
Catharus Ustulatus ◽  
Adaptive Introgression ◽  
Evolutionary Forces ◽  
Genome Wide ◽  
Isolating Mechanisms ◽  
Migratory Songbird

In animals, introgression between species is often perceived as the breakdown of reproductive isolating mechanisms, but gene flow between incipient species can also represent a source for potentially beneficial alleles. Recently, genome-wide datasets have revealed clusters of differentiated loci (‘genomic islands of divergence’) that are thought to play a role in reproductive isolation and therefore have reduced gene flow. We use simulations to further examine the evolutionary forces that shape and maintain genomic islands of divergence between two subspecies of the migratory songbird, Swainson's thrush ( Catharus ustulatus ), which have come into secondary contact since the last glacial maximum. We find that, contrary to expectation, gene flow is high within islands and is highly asymmetric. In addition, patterns of nucleotide diversity at highly differentiated loci suggest selection was more frequent in a single ecotype. We propose a mechanism whereby beneficial alleles spread via selective sweeps following a post-glacial demographic expansion in one subspecies and move preferentially across the hybrid zone. We find no evidence that genomic islands are the result of divergent selection or reproductive isolation, rather our results suggest that differentiated loci both within and outside islands could provide opportunities for adaptive introgression across porous species boundaries.

scholarly journals Morphologically cryptic Amazonian bird species pairs exhibit strong postzygotic reproductive isolation

2018 ◽  
Vol 285 (1874) ◽  
pp. 20172081 ◽  
Author(s):  
Paola Pulido-Santacruz ◽  
Alexandre Aleixo ◽  
Jason T. Weir
Keyword(s):  
Reproductive Isolation ◽  
Amazon Basin ◽  
Species Recognition ◽  
Bird Species ◽  
Hybrid Zones ◽  
Hybrid Index ◽  
Postzygotic Isolation ◽  
Genome Wide ◽  
Species Pairs ◽  
Hybrid Classes

We possess limited understanding of how speciation unfolds in the most species-rich region of the planet—the Amazon basin. Hybrid zones provide valuable information on the evolution of reproductive isolation, but few studies of Amazonian vertebrate hybrid zones have rigorously examined the genome-wide underpinnings of reproductive isolation. We used genome-wide genetic datasets to show that two deeply diverged, but morphologically cryptic sister species of forest understorey birds show little evidence for prezygotic reproductive isolation, but substantial postzygotic isolation. Patterns of heterozygosity and hybrid index revealed that hybrid classes with heavily recombined genomes are rare and closely match simulations with high levels of selection against hybrids. Genomic and geographical clines exhibit a remarkable similarity across loci in cline centres, and have exceptionally narrow cline widths, suggesting that postzygotic isolation is driven by genetic incompatibilities at many loci, rather than a few loci of strong effect. We propose Amazonian understorey forest birds speciate slowly via gradual accumulation of postzygotic genetic incompatibilities, with prezygotic barriers playing a less important role. Our results suggest old, cryptic Amazonian taxa classified as subspecies could have substantial postzygotic isolation deserving species recognition and that species richness is likely to be substantially underestimated in Amazonia.

scholarly journals Extensive introgression despite Haldane’s rule: insights from grasshopper hybrid zones

2021 ◽  
Author(s):  
Linda Hagberg ◽  
Enrique Celemin ◽  
Iker Irisarri ◽  
Oliver Hawlitschek ◽  
J L Bella ◽  
...  
Keyword(s):  
Gene Flow ◽  
Reproductive Isolation ◽  
Male Sterility ◽  
Secondary Contact ◽  
Hybrid Zones ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Haldane’S Rule ◽  
Haldane's Rule ◽  
Species Formation

Although the process of species formation is notoriously idiosyncratic, the observation of pervasive patterns of reproductive isolation across species pairs suggests that generalities, or “rules”, underlie species formation in all animals. Haldane’s rule states that whenever a sex is absent, rare or sterile in a cross between two taxa, that sex is usually the heterogametic sex. Yet, understanding how Haldane’s rule first evolves and whether it is associated to genome wide barriers to gene flow remains a challenging task because this rule is usually studied in highly divergent taxa that no longer hybridize in nature. Here, we address these questions using the meadow grasshopper Pseudochorthippus parallelus where populations that readily hybridize in two natural hybrid zones show hybrid male sterility in laboratorial crosses. Using mitochondrial data, we infer that such populations have diverged some 100,000 years ago, surviving multiple glacial periods in isolated Pleistocenic refugia. Nuclear data shows that secondary contact has led to extensive introgression throughout the species range, including between populations showing hybrid male sterility. We find repeatable patterns of genomic differentiation across the two hybrid zones, yet such patterns are consistent with shared genomic constraints across taxa rather than their role in reproductive isolation. Together, our results suggest that Haldane’s rule can evolve relatively quickly within species, particularly when associated to strong demographic changes. At such early stages of species formation, hybrid male sterility still permits extensive gene flow, allowing future studies to identify genomic regions associated with reproductive barriers.

scholarly journals Parental population range expansion before secondary contact promotes heterosis

2020 ◽  
Author(s):  
Ailene MacPherson ◽  
Silu Wang ◽  
Ryo Yamaguchi ◽  
Loren H. Riesesberg ◽  
Sarah P. Otto
Keyword(s):  
Reproductive Isolation ◽  
Range Expansion ◽  
Genomic Analysis ◽  
Population Expansion ◽  
Ancestral Population ◽  
Secondary Contact ◽  
Hybrid Zones ◽  
Deleterious Alleles ◽  
Genomic Divergence ◽  
Slightly Deleterious Mutations

AbstractPopulation genomic analysis of hybrid zones is instrumental to our understanding of the evolution of reproductive isolation. Many temperate hybrid zones are formed by the secondary contact between two parental populations that had undergone post-glacial range expansion. Here we show that explicitly accounting for historical parental isolation followed by range expansion prior to secondary contact is fundamental for explaining genetic and fitness patterns in these hybrid zones. Specifically, ancestral population expansion can result in allele surfing, neutral or slightly deleterious mutations drift high frequency at the front of the expansion. If these surfed deleterious alleles are recessive, they can contribute to substantial heterosis in hybrids produced at secondary contact, counteracting negative-epistatic interactions between BDMI loci and hence can deteriorate reproductive isolation. Similarly, surfing at neutral loci can alter the expected pattern of population ancestry and suggests that accounting for historical population expansion is necessary to develop accurate null genomic models in secondary-contact hybrid zones. Furthermore, this process should be incorporated in macroevolutionary models of divergence as well, since such heterosis facilitated by parental-range expansion could dampen genomic divergence established in the past.

scholarly journals Evolution of assortative mating following selective introgression of pigmentation genes between two Drosophila species

2022 ◽  
Author(s):  
Jean R David ◽  
Erina A Ferreira ◽  
Laure Jabaud ◽  
David Ogereau ◽  
Héloïse Bastide ◽  
...  
Keyword(s):  
New Species ◽  
Reproductive Isolation ◽  
Assortative Mating ◽  
Genome Sequencing ◽  
Parental Species ◽  
Phenotypic Change ◽  
Adaptive Introgression ◽  
Genome Wide ◽  
Significant Step ◽  
One Year

Adaptive introgression is ubiquitous in animals but experimental support for its role in driving speciation remains scarce. In the absence of conscious selection, admixed laboratory strains of Drosophila asymmetrically and progressively lose alleles from one parental species and reproductive isolation against the predominant parent ceases after 10 generations. Here, we selectively introgressed during one year light pigmentation genes of D. santomea into the genome of its dark sibling D. yakuba, and vice versa. We found that the pace of phenotypic change differed between the species and the sexes, and identified through genome sequencing common as well as distinct introgressed loci in each species. Mating assays showed that assortative mating between introgressed flies and both parental species persisted even after four years (~ 60 generations) from the end of the selection. Those results indicate that selective introgression of as low as 0.5% of the genome can beget morphologically-distinct and reproductively-isolated strains, two prerequisites for the delimitation of new species. Our findings hence represent a significant step towards understanding the genome-wide dynamics of speciation-through-introgression.

scholarly journals The origin and remolding of genomic islands of differentiation in the European sea bass

2017 ◽  
Author(s):  
Maud Duranton ◽  
François Allal ◽  
Christelle Fraïsse ◽  
Nicolas Bierne ◽  
François Bonhomme ◽  
...  
Keyword(s):  
Reproductive Isolation ◽  
Sea Bass ◽  
Genomic Islands ◽  
Secondary Contact ◽  
European Sea Bass ◽  
Closely Related Species ◽  
Fitness Effects ◽  
Genome Wide ◽  
Complex Process ◽  
Linked Selection

AbstractSpeciation is a complex process that leads to the progressive establishment of reproductive isolation barriers between diverging populations. Genome-wide comparisons between closely related species have revealed the existence of heterogeneous divergence patterns, dominated by genomic islands of increased divergence supposed to contain reproductive isolation loci. However, this divergence landscape only provides a static picture of the dynamic process of speciation, during which confounding mechanisms unlinked to speciation can interfere. Here, we used haplotype-resolved whole-genome sequences to identify the mechanisms responsible for the formation of genomic islands between Atlantic and Mediterranean sea bass lineages. We show that genomic islands first emerged in allopatry through the effect of linked selection acting on a heterogeneous recombination landscape. Upon secondary contact, preexisting islands were strongly remolded by differential introgression, revealing variable fitness effects among regions involved in reproductive isolation. Interestingly, we found that divergent regions containing ancient polymorphisms conferred the strongest resistance to introgression.

scholarly journals Asymmetric Reproductive Barriers and Gene Flow Promote the Rise of a Stable Hybrid Zone in the Mediterranean High Mountain

2021 ◽  
Vol 12 ◽  
Author(s):  
Mohamed Abdelaziz ◽  
A. Jesús Muñoz-Pajares ◽  
Modesto Berbel ◽  
Ana García-Muñoz ◽  
José M. Gómez ◽  
...  
Keyword(s):  
Gene Flow ◽  
Reproductive Isolation ◽  
Sierra Nevada ◽  
Hybrid Zone ◽  
High Elevation ◽  
Secondary Contact ◽  
High Mountain ◽  
Hybrid Zones ◽  
Reproductive Barriers ◽  
Sierra Nevada Mountains

Hybrid zones have the potential to shed light on evolutionary processes driving adaptation and speciation. Secondary contact hybrid zones are particularly powerful natural systems for studying the interaction between divergent genomes to understand the mode and rate at which reproductive isolation accumulates during speciation. We have studied a total of 720 plants belonging to five populations from two Erysimum (Brassicaceae) species presenting a contact zone in the Sierra Nevada mountains (SE Spain). The plants were phenotyped in 2007 and 2017, and most of them were genotyped the first year using 10 microsatellite markers. Plants coming from natural populations were grown in a common garden to evaluate the reproductive barriers between both species by means of controlled crosses. All the plants used for the field and greenhouse study were characterized by measuring traits related to plant size and flower size. We estimated the genetic molecular variances, the genetic differentiation, and the genetic structure by means of the F-statistic and Bayesian inference. We also estimated the amount of recent gene flow between populations. We found a narrow unimodal hybrid zone where the hybrid genotypes appear to have been maintained by significant levels of a unidirectional gene flow coming from parental populations and from weak reproductive isolation between them. Hybrid plants exhibited intermediate or vigorous phenotypes depending on the analyzed trait. The phenotypic differences between the hybrid and the parental plants were highly coherent between the field and controlled cross experiments and through time. The highly coherent results obtained by combining field, experimental, and genetic data demonstrate the existence of a stable and narrow unimodal hybrid zone between Erysimum mediohispanicum and Erysimum nevadense at the high elevation of the Sierra Nevada mountains.

Neutral and adaptive genomic variation in hybrid zones of two ecologically diverged Petunia species (Solanaceae)

2020 ◽  
Author(s):  
Lina Caballero-Villalobos ◽  
Gustavo A Silva-Arias ◽  
Caroline Turchetto ◽  
Giovanna C Giudicelli ◽  
Earl Petzold ◽  
...  
Keyword(s):  
Natural Selection ◽  
Genetic Structure ◽  
Reproductive Isolation ◽  
Genomic Variation ◽  
Secondary Contact ◽  
Pollination Syndrome ◽  
Hybrid Zones ◽  
Environmental Selection ◽  
Species Integrity ◽  
Well Differentiated

Abstract Hybridization between closely related plant species is a widespread phenomenon with significant evolutionary consequences, so natural hybrid zones provide exciting opportunities to study the processes of genetic differentiation and species formation. In Petunia, genetics, ecology and evolution of pollination syndromes have been thoroughly studied and related to the development of prezygotic isolation barriers between species. However, to date, no studies have explored the importance of extrinsic post-zygotic barriers such as environmental selection as drivers of reproductive isolation. In this study, we applied a population genetics approach to understand the speciation of two partially sympatric taxa of Petunia Juss that hybridize in the wild despite having strong differences in pollination syndrome, mating system and environmental requirements. We evaluated 58 individuals from seven allopatric and two contact zones of Petunia axillaris and P. exserta with genomic data to study the population genetic structure and gene exchange between these species and scan for potential loci under natural selection related to the preservation of species barriers. We explicitly evaluated the time, intensity and direction of interspecific migration, testing for alternative demographic scenarios. The genetic structure showed well-differentiated species-level lineages, and poor differentiation among populations of P. axillaris; P. exserta populations were highly structured, with several well-differentiated intraspecific lineages. Our data provide evidence for admixture with low asymmetric gene flow from P. axillaris to P. exserta associated with recent secondary contact, suggesting that pollinator specificity is not the only trait responsible for species integrity in this system. Combining the results from FST outlier and genotype–phenotype association methods, we identified 54 non-synonymous candidate variants under natural selection. Those variants are found in 35 coding sequences from which we found genes related to light-response networks, supporting that extrinsic factors such as habitat preferences can also provide a mechanism of reproductive isolation between Petunia spp. We argue that a set of pre- and post-zygotic barriers in conjunction with demographic processes maintain the species integrity.

scholarly journals Evolutionary dynamics driving continental radiations of Fagaceae forests across the Northern Hemisphere

2021 ◽  
Author(s):  
Biao-Feng Zhou ◽  
Shuai Yuan ◽  
Andrew Crowl ◽  
Yi-Ye Liang ◽  
Yong Shi ◽  
...  
Keyword(s):  
Northern Hemisphere ◽  
Evolutionary Dynamics ◽  
Pollen Dispersal ◽  
Multiple Time Scales ◽  
Secondary Contact ◽  
Multiple Time ◽  
Competitive Edge ◽  
Adaptive Introgression ◽  
Genome Wide ◽  
Rapid Diversification

Abstract Northern Hemisphere forests changed drastically in the early Eocene with the diversification of the oak family (Fagaceae). Cooling climates over the next 20 million years fostered the spread of temperate biomes that became increasingly dominated by oaks and their chestnut relatives. Here we investigate the timing and pattern of major macroevolutionary events and ancient genome-wide signatures of hybridization across Fagaceae. An unparalleled transformation of forest dynamics began with the rapid diversification of major lineages within 15 million years following the K-Pg extinction. Innovations related to seed and pollen dispersal are implicated in triggering waves of continental radiations, while fungal symbioses fortified a competitive edge underground. We detected introgression at multiple time scales, including ancient events predating the origination of genus-level diversity. As oak lineages moved into newly available temperate habitats in the early Miocene, secondary contact between previously isolated species occurred. This resulted in adaptive introgression, further amplifying global proliferation.

scholarly journals Admixture between Ancient Lineages, Selection, and the Formation of Sympatric Stickleback Species-Pairs

2019 ◽  
Vol 36 (11) ◽  
pp. 2481-2497 ◽  
Author(s):  
Laura L Dean ◽  
Isabel S Magalhaes ◽  
Andrew Foote ◽  
Daniele D’Agostino ◽  
Suzanne McGowan ◽  
...  
Keyword(s):  
Reproductive Isolation ◽  
Gasterosteus Aculeatus ◽  
Ecological Speciation ◽  
Morphological Data ◽  
Secondary Contact ◽  
Disruptive Selection ◽  
Implicit Assumption ◽  
Hybridization Rate ◽  
Genome Wide ◽  
Species Pairs

Abstract Ecological speciation has become a popular model for the development and maintenance of reproductive isolation in closely related sympatric pairs of species or ecotypes. An implicit assumption has been that such pairs originate (possibly with gene flow) from a recent, genetically homogeneous ancestor. However, recent genomic data have revealed that currently sympatric taxa are often a result of secondary contact between ancestrally allopatric lineages. This has sparked an interest in the importance of initial hybridization upon secondary contact, with genomic reanalysis of classic examples of ecological speciation often implicating admixture in speciation. We describe a novel occurrence of unusually well-developed reproductive isolation in a model system for ecological speciation: the three-spined stickleback (Gasterosteus aculeatus), breeding sympatrically in multiple lagoons on the Scottish island of North Uist. Using morphological data, targeted genotyping, and genome-wide single-nucleotide polymorphism data, we show that lagoon resident and anadromous ecotypes are strongly reproductively isolated with an estimated hybridization rate of only ∼1%. We use palaeoecological and genetic data to test three hypotheses to explain the existence of these species-pairs. Our results suggest that recent, purely ecological speciation from a genetically homogeneous ancestor is probably not solely responsible for the evolution of species-pairs. Instead, we reveal a complex colonization history with multiple ancestral lineages contributing to the genetic composition of species-pairs, alongside strong disruptive selection. Our results imply a role for admixture upon secondary contact and are consistent with the recent suggestion that the genomic underpinning of ecological speciation often has an older, allopatric origin.

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