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 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 Local adaptation and sexual selection drive intra-island diversification in a songbird lineage: differential divergence in autosomes and sex chromosomes

2018 ◽  
Author(s):  
Yann XC Bourgeois ◽  
Joris AM Bertrand ◽  
Boris Delahaie ◽  
Hélène Holota ◽  
Christophe Thébaud ◽  
...  
Keyword(s):  
Sexual Selection ◽  
Natural Selection ◽  
Reproductive Isolation ◽  
Local Adaptation ◽  
Sex Chromosomes ◽  
Genomic Variation ◽  
Color Variation ◽  
Mating Signals ◽  
Genome Wide

AbstractRecently diverged taxa showing marked phenotypic and ecological diversity are optimal systems to test the relative importance of two major evolutionary mechanisms, adaptation to local ecological conditions by natural selection, or mechanisms of reproductive isolation such as assortative mating mediated by sexually selected mating signals or post-zygotic incompatibilities. Whereas local adaptation is expected to affect many loci throughout the genome, traits acting as mating signals are expected to be located on sex chromosomes and have a simple genetic basis. We used genome-wide markers to test these predictions in Reunion Island’s gray-white eye (Zosterops borbonicus), which has recently diversified into five distinct plumage forms. Two of them correspond to a polymorphic highland population that is separated by a steep ecological gradient from three distinct lowland forms that show narrow contact zones in plumage color traits, yet no association with environmental variables. An analysis of population structure using genome-wide SNP loci revealed two major clades corresponding to highland and lowland forms, respectively, with the latter separated further into three independent lineages corresponding to plumage forms. Coalescent tests of alternative demographic scenarios provided support for divergence of highland and lowland lineages with an intensification of gene flow in the last 60,000 years. Landscapes of genomic variation revealed that signatures of selection associated with elevation are found at multiple regions across the genome, whereas most loci associated with the lowland forms are located on the Z sex chromosome. A gene ontology analysis identified TYRP1, a Z-linked color gene, as a likely candidate locus underlying color variation among lowland forms. Our results are consistent with the role of natural selection in driving the divergence of locally adapted highland populations, and the role of sexual selection in differentiating lowland forms through reproductive isolation mechanisms, showing that both modes of lineage divergence can take place at very small geographic scales in birds.

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.

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 The geography of introgression in a patchy environment and the thorn in the side of ecological speciation

2013 ◽  
Vol 59 (1) ◽  
pp. 72-86 ◽  
Author(s):  
Nicolas Bierne ◽  
Pierre-Alexandre Gagnaire ◽  
Patrice David
Keyword(s):  
Large Scale ◽  
Isolation By Distance ◽  
Alternative Hypothesis ◽  
Ecological Speciation ◽  
Secondary Contact ◽  
Small Scale ◽  
Hybrid Zones ◽  
Patchy Environment ◽  
Environmental Selection ◽  
Selected Traits

Abstract When incompletely isolated taxa coexist in a patchy environment (e.g. mosaic hybrid zones, host-race complexes), patterns of variation may differ between selected traits/genes and neutral markers. While the genetic structure of selected traits/loci tends to coincide with habitat variables (producing Genetic-Environment Association or GEA), genetic differentiation at neutral loci unlinked to any selected locus rather depends on geographic connectivity at a large scale (e.g. Isolation-By-Distance or IBD), although these loci often display GEA at a small scale. This discrepancy has been repeatedly taken as evidence for parallel primary divergence driven by local adaptation. We argue that this interpretation needs to be addressed more thoroughly by considering the alternative hypothesis that speciation was initiated in allopatry and secondary introgression has subsequently erased the signal of past differentiation at neutral loci. We present a model of neutral introgression after secondary contact in a mosaic hybrid zone, which describes how GEAs dissipate with time and how neutral variation self-organizes according to the environmental and geographic structures. We show that although neutral loci can be affected by environmental selection, they are often more affected by history and connectivity: the neutral structure retains the initial geographic separation more than it correlates with the environment during the colonization and introgression phases, and then converges to a migration-drift balance, the most frequent outcome of which is GEA at a local scale but IBD at a large scale. This is the exact pattern usually attributed to parallel ecological speciation. Introgression is heterogeneous in space and depends on the landscape structure (e.g. it is faster in small patches, which are more impacted by immigration). Furthermore, there is no directionality in the association and it is possible to observe reversed GEAs between distant regions. We argue that the history of differentiation should ideally be reconstructed with selected loci or neutral loci linked to them, not neutral ones, and review some case studies for which the hypothesis of a long co-existence of co-adapted genetic backgrounds might have been refuted too hastily.

scholarly journals Genomic variation in the American pika: signatures of geographic isolation and implications for conservation

2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Kelly B. Klingler ◽  
Joshua P. Jahner ◽  
Thomas L. Parchman ◽  
Chris Ray ◽  
Mary M. Peacock
Keyword(s):  
Genetic Variation ◽  
Genetic Structure ◽  
Sierra Nevada ◽  
Spatial Genetic Structure ◽  
Spatial Scales ◽  
Thermal Sensitivity ◽  
Genomic Variation ◽  
Genome Wide ◽  
A Genome ◽  
American Pika

Abstract Background Distributional responses by alpine taxa to repeated, glacial-interglacial cycles throughout the last two million years have significantly influenced the spatial genetic structure of populations. These effects have been exacerbated for the American pika (Ochotona princeps), a small alpine lagomorph constrained by thermal sensitivity and a limited dispersal capacity. As a species of conservation concern, long-term lack of gene flow has important consequences for landscape genetic structure and levels of diversity within populations. Here, we use reduced representation sequencing (ddRADseq) to provide a genome-wide perspective on patterns of genetic variation across pika populations representing distinct subspecies. To investigate how landscape and environmental features shape genetic variation, we collected genetic samples from distinct geographic regions as well as across finer spatial scales in two geographically proximate mountain ranges of eastern Nevada. Results Our genome-wide analyses corroborate range-wide, mitochondrial subspecific designations and reveal pronounced fine-scale population structure between the Ruby Mountains and East Humboldt Range of eastern Nevada. Populations in Nevada were characterized by low genetic diversity (π = 0.0006–0.0009; θW = 0.0005–0.0007) relative to populations in California (π = 0.0014–0.0019; θW = 0.0011–0.0017) and the Rocky Mountains (π = 0.0025–0.0027; θW = 0.0021–0.0024), indicating substantial genetic drift in these isolated populations. Tajima’s D was positive for all sites (D = 0.240–0.811), consistent with recent contraction in population sizes range-wide. Conclusions Substantial influences of geography, elevation and climate variables on genetic differentiation were also detected and may interact with the regional effects of anthropogenic climate change to force the loss of unique genetic lineages through continued population extirpations in the Great Basin and Sierra Nevada.

scholarly journals Multi-model seascape genomics identifies distinct environmental drivers of selection among sympatric marine species

2020 ◽  
Author(s):  
Erica Nielsen ◽  
Romina Henriques ◽  
Maria Beger ◽  
Robert Toonen ◽  
Sophie von der Heyden
Keyword(s):  
Global Change ◽  
Outlier Detection ◽  
Genomic Variation ◽  
Sea Surface ◽  
Environmental Drivers ◽  
Comparative Approach ◽  
Evolutionary Potential ◽  
Environmental Selection ◽  
Outlier Loci ◽  
Isolation By Environment

Abstract Background: As global change and anthropogenic pressures continue to increase, conservation and management increasingly needs to consider species’ potential to adapt to novel environmental conditions. Therefore, it is imperative to characterise the main selective forces acting on ecosystems, and how these may influence the evolutionary potential of populations and species. Using a multi-model seascape genomics approach, we compare putative environmental drivers of selection in three sympatric southern African marine invertebrates with contrasting ecology and life histories: Cape urchin (Parechinus angulosus), Common shore crab (Cyclograpsus punctatus), and Granular limpet (Scutellastra granularis). Results: Using pooled (Pool-seq), restriction-site associated DNA sequencing (RAD-seq), and seven outlier detection methods, we characterise genomic variation between populations along a strong biogeographical gradient. Of the three species, only S. granularis showed significant isolation-by-distance, and isolation-by-environment driven by sea surface temperatures (SST). In contrast, sea surface salinity (SSS) and range in air temperature correlated more strongly with genomic variation in C. punctatus and P. angulosus. Differences were also found in genomic structuring between the three species, with outlier loci contributing to two clusters in the East and West Coasts for S. granularis and P. angulosus, but not for C. punctatus. Conclusion: The findings illustrate distinct evolutionary potential across species, suggesting that species-specific habitat requirements and responses to environmental stresses may be better predictors of evolutionary patterns than the strong environmental gradients within the region. We also found large discrepancies between outlier detection methodologies, and thus offer a novel multi-model approach to identifying the principal environmental selection forces acting on species. Overall, this work highlights how adding a comparative approach to seascape genomics (both with multiple models and species) can elucidate the intricate evolutionary responses of ecosystems to global change.

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