scholarly journals Genome-wide patterns of divergence and introgression after secondary contact between Pungitius sticklebacks

2020 ◽  
Vol 375 (1806) ◽  
pp. 20190548 ◽  
Author(s):  
Yo Y. Yamasaki ◽  
Ryo Kakioka ◽  
Hiroshi Takahashi ◽  
Atsushi Toyoda ◽  
Atsushi J. Nagano ◽  
...  
Keyword(s):  
Gene Flow ◽  
Reproductive Isolation ◽  
Sequence Data ◽  
Continuous Process ◽  
Sympatric Species ◽  
Whole Genome Sequence ◽  
Secondary Contact ◽  
Pungitius Pungitius ◽  
Hybrid Male ◽  
Differential Adaptation

Speciation is a continuous process. Although it is known that differential adaptation can initiate divergence even in the face of gene flow, we know relatively little about the mechanisms driving complete reproductive isolation and the genomic patterns of divergence and introgression at the later stages of speciation. Sticklebacks contain many pairs of sympatric species differing in levels of reproductive isolation and divergence history. Nevertheless, most previous studies have focused on young species pairs. Here, we investigated two sympatric stickleback species, Pungitius pungitius and P. sinensis , whose habitats overlap in eastern Hokkaido; these species show hybrid male sterility, suggesting that they may be at a late stage of speciation. Our demographic analysis using whole-genome sequence data showed that these species split 1.73 Ma and came into secondary contact 37 200 years ago after a period of allopatry. This long period of allopatry might have promoted the evolution of intrinsic incompatibility. Although we detected on-going gene flow and signatures of introgression, overall genomic divergence was high, with considerable heterogeneity across the genome. The heterogeneity was significantly associated with variation in recombination rate. This sympatric pair provides new avenues to investigate the late stages of the stickleback speciation continuum. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

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 Clinal genomic analysis reveals strong reproductive isolation across a steep habitat transition in stickleback fish

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Quiterie Haenel ◽  
Krista B. Oke ◽  
Telma G. Laurentino ◽  
Andrew P. Hendry ◽  
Daniel Berner
Keyword(s):  
Gene Flow ◽  
Reproductive Isolation ◽  
Sequence Data ◽  
Genomic Analysis ◽  
Whole Genome Sequence ◽  
Adaptive Divergence ◽  
Entire Genome ◽  
High Dispersal ◽  
A Genome ◽  
Habitat Transition

AbstractHow ecological divergence causes strong reproductive isolation between populations in close geographic contact remains poorly understood at the genomic level. We here study this question in a stickleback fish population pair adapted to contiguous, ecologically different lake and stream habitats. Clinal whole-genome sequence data reveal numerous genome regions (nearly) fixed for alternative alleles over a distance of just a few hundred meters. This strong polygenic adaptive divergence must constitute a genome-wide barrier to gene flow because a steep cline in allele frequencies is observed across the entire genome, and because the cline center closely matches the habitat transition. Simulations confirm that such strong divergence can be maintained by polygenic selection despite high dispersal and small per-locus selection coefficients. Finally, comparing samples from near the habitat transition before and after an unusual ecological perturbation demonstrates the fragility of the balance between gene flow and selection. Overall, our study highlights the efficacy of divergent selection in maintaining reproductive isolation without physical isolation, and the analytical power of studying speciation at a fine eco-geographic and genomic scale.

scholarly journals Clinal genomic analysis reveals strong reproductive isolation across a steep habitat transition in stickleback fish

2020 ◽  
Author(s):  
Quiterie Haenel ◽  
Krista B. Oke ◽  
Telma G. Laurentino ◽  
Andrew P. Hendry ◽  
Daniel Berner
Keyword(s):  
Gene Flow ◽  
Reproductive Isolation ◽  
Sequence Data ◽  
Genomic Analysis ◽  
Whole Genome Sequence ◽  
Adaptive Divergence ◽  
Entire Genome ◽  
High Dispersal ◽  
A Genome ◽  
Habitat Transition

AbstractHow ecological divergence causes strong reproductive isolation between populations in close geographic contact remains poorly understood at the genomic level. We here study this question in a stickleback population pair adapted to contiguous, ecologically different lake and stream habitats. Dense clinal whole-genome sequence data reveal numerous regions fixed for alternative alleles over a distance of just a few hundred meters. This strong polygenic adaptive divergence must constitute a genome-wide barrier to gene flow because a steep cline in allele frequencies is observed across the entire genome, and because the cline center co-localizes with the habitat transition. Simulations confirm that such strong reproductive isolation can be maintained by polygenic selection despite high dispersal and small per-locus selection coefficients. Finally, comparing samples from the cline center before and after an unusual ecological perturbation demonstrates the fragility of the balance between gene flow and selection. Overall, our study highlights the efficacy of divergent selection in maintaining reproductive isolation without physical isolation, and the analytical power of studying speciation at a fine eco-geographic and genomic scale.

scholarly journals Selective ancestral sorting and de novo evolution in the agricultural invasion of Amaranthus tuberculatus

2021 ◽  
Author(s):  
Julia M. Kreiner ◽  
Amalia Caballero ◽  
Stephen I. Wright ◽  
John R. Stinchcombe
Keyword(s):  
De Novo ◽  
Sequence Data ◽  
Sex Differentiation ◽  
Common Garden ◽  
Whole Genome Sequence ◽  
Secondary Contact ◽  
Natural Environments ◽  
Relative Role ◽  
Standing Variation ◽  
Amaranthus Tuberculatus

The relative role of hybridization, de novo evolution, and standing variation in weed adaptation to agricultural environments is largely unknown. In Amaranthus tuberculatus, a widespread North American agricultural weed, adaptation is likely influenced by recent secondary contact and admixture of two previously isolated subspecies. We characterized the extent of adaptation and phenotypic differentiation accompanying the spread of A. tuberculatus into agricultural environments and the contribution of subspecies divergence. We generated phenotypic and whole-genome sequence data from a manipulative common garden experiment, using paired samples from natural and agricultural populations. We found strong latitudinal, longitudinal, and sex differentiation in phenotypes, and subtle differences among agricultural and natural environments that were further resolved with ancestry-based inference. The transition into agricultural environments has favoured southwestern var. rudis ancestry that leads to higher biomass and environment-specific phenotypes: increased biomass and earlier flowering under reduced water availability, and reduced plasticity in fitness-related traits. We also detected de novo adaptation to agricultural habitats independent of ancestry effects, including marginally higher biomass and later flowering in agricultural populations, and a time to germination home advantage. Therefore, the invasion of A. tuberculatus into agricultural environments has drawn on adaptive variation across multiple timescales—through both preadaptation via the preferential sorting of var. rudis ancestry and de novo local adaptation.

scholarly journals Hybridization drives genetic erosion in sympatric desert fishes of western North America

2019 ◽  
Author(s):  
Tyler K. Chafin ◽  
Marlis R. Douglas ◽  
Bradley T. Martin ◽  
Michael E. Douglas
Keyword(s):  
Reproductive Isolation ◽  
Extinction Risk ◽  
Genetic Erosion ◽  
Sympatric Species ◽  
Habitat Modification ◽  
Genetic Purity ◽  
Hybrid Swarm ◽  
Desert Fishes ◽  
Differential Adaptation ◽  
Anthropogenic Habitat

AbstractMany species have evolved or currently coexist in sympatry due to differential adaptation in a heterogeneous environment. However, anthropogenic habitat modifications can either disrupt reproductive barriers or obscure environmental conditions which underlie fitness gradients. In this study, we evaluated the potential for an anthropogenically-mediated shift in reproductive boundaries that separate two historically sympatric fish species (Gila cypha and G. robusta) endemic to the Colorado River Basin using ddRAD sequencing of 368 individuals. We first examined the integrity of reproductive isolation while in sympatry and allopatry, then characterized hybrid ancestries using genealogical assignment tests. We tested for localized erosion of reproductive isolation by comparing site-wise genomic clines against global patterns and identified a breakdown in the drainage-wide pattern of selection against interspecific heterozygotes. This, in turn, allowed for the formation of a hybrid swarm in one tributary, and asymmetric introgression where species co-occur. We also detected a weak but significant relationship between genetic purity and degree of consumptive water removal, suggesting a role for anthropogenic habitat modifications in undermining species boundaries. In addition, results from basin-wide genomic clines suggested that hybrids and parental forms are adaptively non-equivalent. If so, then a failure to manage for hybridization will exacerbate the long-term extinction risk in parental populations. These results reinforce the role of anthropogenic habitat modification in promoting interspecific introgression in sympatric species by relaxing divergent selection. This, in turn, underscores a broader role for hybridization in decreasing global biodiversity within rapidly deteriorating environments.

scholarly journals Low coverage genomic data resolve the population divergence and gene flow history of an Australian rain forest fig wasp

2020 ◽  
Author(s):  
Lisa Cooper ◽  
Lynsey Bunnefeld ◽  
Jack Hearn ◽  
James M Cook ◽  
Konrad Lohse ◽  
...  
Keyword(s):  
Gene Flow ◽  
Rain Forest ◽  
Sequence Data ◽  
Dry Forest ◽  
Whole Genome Sequence ◽  
Model Organisms ◽  
Eastern Coast ◽  
Population Divergence ◽  
Fig Wasp ◽  
History Of

AbstractPopulation divergence and gene flow are key processes in evolution and ecology. Model-based analysis of genome-wide datasets allows discrimination between alternative scenarios for these processes even in non-model taxa. We used two complementary approaches (one based on the blockwise site frequency spectrum (bSFS), the second on the Pairwise Sequentially Markovian Coalescent (PSMC)) to infer the divergence history of a fig wasp, Pleistodontes nigriventris. Pleistodontes nigriventris and its fig tree mutualist Ficus watkinsiana are restricted to rain forest patches along the eastern coast of Australia, and are separated into northern and southern populations by two dry forest corridors (the Burdekin and St. Lawrence Gaps). We generated whole genome sequence data for two haploid males per population and used the bSFS approach to infer the timing of divergence between northern and southern populations of P. nigriventris, and to discriminate between alternative isolation with migration (IM) and instantaneous admixture (ADM) models of post divergence gene flow. Pleistodontes nigriventris has low genetic diversity (π = 0.0008), to our knowledge one of the lowest estimates reported for a sexually reproducing arthropod. We find strongest support for an ADM model in which the two populations diverged ca. 196kya in the late Pleistocene, with almost 25% of northern lineages introduced from the south during an admixture event ca. 57kya. This divergence history is highly concordant with individual population demographies inferred from each pair of haploid males using PSMC. Our analysis illustrates the inferences possible with genome-level data for small population samples of tiny, non-model organisms and adds to a growing body of knowledge on the population structure of Australian rain forest taxa.

Phylogenomic Data Reveal Widespread Introgression Across the Range of an Alpine and Arctic Specialist

2020 ◽  
Author(s):  
Erik R Funk ◽  
Garth M Spellman ◽  
Kevin Winker ◽  
Jack J Withrow ◽  
Kristen C Ruegg ◽  
...  
Keyword(s):  
Gene Flow ◽  
Genome Sequence ◽  
Population Genetic ◽  
Approximate Bayesian Computation ◽  
Sequence Data ◽  
Species Group ◽  
Whole Genome Sequence ◽  
Whole Genome ◽  
Genome Sequence Data ◽  
Approximate Bayesian

Abstract Understanding how gene flow affects population divergence and speciation remains challenging. Differentiating one evolutionary process from another can be difficult because multiple processes can produce similar patterns, and more than one process can occur simultaneously. Although simple population models produce predictable results, how these processes balance in taxa with patchy distributions and complicated natural histories is less certain. These types of populations might be highly connected through migration (gene flow), but can experience stronger effects of genetic drift and inbreeding, or localized selection. Although different signals can be difficult to separate, the application of high-throughput sequence data can provide the resolution necessary to distinguish many of these processes. We present whole-genome sequence data for an avian species group with an alpine and arctic tundra distribution to examine the role that different population genetic processes have played in their evolutionary history. Rosy-finches inhabit high elevation mountaintop sky islands and high-latitude island and continental tundra. They exhibit extensive plumage variation coupled with low levels of genetic variation. Additionally, the number of species within the complex is debated, making them excellent for studying the forces involved in the process of diversification, as well as an important species group in which to investigate species boundaries. Total genomic variation suggests a broadly continuous pattern of allele frequency changes across the mainland taxa of this group in North America. However, phylogenomic analyses recover multiple distinct, well supported, groups that coincide with previously described morphological variation and current species-level taxonomy. Tests of introgression using D-statistics and approximate Bayesian computation reveal significant levels of introgression between multiple North American taxa. These results provide insight into the balance between divergent and homogenizing population genetic processes and highlight remaining challenges in interpreting conflict between different types of analytical approaches with whole-genome sequence data. [ABBA-BABA; approximate Bayesian computation; gene flow; phylogenomics; speciation; whole-genome sequencing.]

scholarly journals Distinguishing gene flow between malaria parasite populations

PLoS Genetics ◽  
2021 ◽  
Vol 17 (12) ◽  
pp. e1009335
Author(s):  
Tyler S. Brown ◽  
Olufunmilayo Arogbokun ◽  
Caroline O. Buckee ◽  
Hsiao-Han Chang
Keyword(s):  
Gene Flow ◽  
Malaria Parasite ◽  
Sequence Data ◽  
Spatial Scales ◽  
Population Level ◽  
Whole Genome Sequence ◽  
Surveillance Studies ◽  
Migration Rates ◽  
Mobility Data ◽  
Parasite Populations

Measuring gene flow between malaria parasite populations in different geographic locations can provide strategic information for malaria control interventions. Multiple important questions pertaining to the design of such studies remain unanswered, limiting efforts to operationalize genomic surveillance tools for routine public health use. This report examines the use of population-level summaries of genetic divergence (FST) and relatedness (identity-by-descent) to distinguish levels of gene flow between malaria populations, focused on field-relevant questions about data size, sampling, and interpretability of observations from genomic surveillance studies. To do this, we use P. falciparum whole genome sequence data and simulated sequence data approximating malaria populations evolving under different current and historical epidemiological conditions. We employ mobile-phone associated mobility data to estimate parasite migration rates over different spatial scales and use this to inform our analysis. This analysis underscores the complementary nature of divergence- and relatedness-based metrics for distinguishing gene flow over different temporal and spatial scales and characterizes the data requirements for using these metrics in different contexts. Our results have implications for the design and implementation of malaria genomic surveillance studies.

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 Distinguishing gene flow between malaria parasite populations

2021 ◽  
Author(s):  
Tyler Steven Brown ◽  
Aimee R. Taylor ◽  
Olufunmilayo Arogbokun ◽  
Caroline O. Buckee ◽  
Hsiao-Han Chang
Keyword(s):  
Gene Flow ◽  
Malaria Parasite ◽  
Sequence Data ◽  
Simulated Data ◽  
Whole Genome Sequence ◽  
Effective Population ◽  
Migration Rates ◽  
Population Sizes ◽  
And Migration ◽  
Parasite Populations

Measuring gene flow between malaria parasite populations in different geographic locations can provide strategic information for malaria control interventions. Multiple important questions pertaining to the design of such studies remain unanswered, limiting efforts to operationalize genomic surveillance tools for routine public health use. This report evaluates numerically the ability to distinguish different levels of gene flow between malaria populations, using different amounts of real and simulated data, where data are simulated using parameters that approximate different epidemiological conditions. Specifically, using Plasmodium falciparum  whole genome sequence data and sequence data simulated for a metapopulation with different migration rates and effective population sizes, we compare two estimators of gene flow, explore the number of genetic markers and number of individuals required to reliably rank highly connected locations, and describe how these thresholds change given different effective population sizes and migration rates. Our results have implications for the design and implementation of malaria genomic surveillance efforts.

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