scholarly journals Genomic signals of admixture and reinforcement between two closely related species of European sepsid flies

Author(s):  
Athene Giesen ◽  
Wolf Blanckenhorn ◽  
Martin Schäfer ◽  
Kentaro K. Shimizu ◽  
Rie Shimizu-Inatsugi ◽  
...  

Interspecific gene flow by hybridization may weaken species barriers and adaptive divergence, but can also initiate reinforcement of reproductive isolation trough natural and sexual selection. The extent of interspecific gene flow and its consequences for the initiation and maintenance of species barriers in natural systems remain poorly understood, however. To assess genome-wide patterns of gene flow between the two closely related European dung fly species Sepsis cynipsea and Sepsis neocynipsea (Diptera: Sepsidae), we tested for historical gene flow with the aid of ABBA-BABA test using whole-genome resequencing data from pooled DNA of male specimens originating from natural and laboratory populations. We contrasted genome-wide variation in DNA sequence differences between samples from sympatric populations of the two species in France and Switzerland with that of interspecific differences between pairs of samples involving allopatric populations from Estonia and Italy. In the French Cevennes, we detected a relative excess of DNA sequence identity, suggesting interspecific gene flow in sympatry. In contrast, at two sites in Switzerland, we observed a relative depletion of DNA sequence identity compatible with reinforcement of species boundaries in sympatry. Our results suggest that the species boundaries between S. cynipsea and S. neocynipsea in Europe depend on the eco-geographic context.

2020 ◽  
Author(s):  
Athene Giesen ◽  
Wolf U. Blanckenhorn ◽  
Martin A. Schäfer ◽  
Kentaro K. Shimizu ◽  
Rie Shimizu-Inatsugi ◽  
...  

ABSTRACTInterspecific gene flow by hybridization may weaken species barriers and adaptive divergence, but can also initiate reinforcement of reproductive isolation trough natural and sexual selection. The extent of interspecific gene flow and its consequences for the initiation and maintenance of species barriers in natural systems remain poorly understood, however. To assess genome-wide patterns of gene flow between the two closely related European dung fly species Sepsis cynipsea and Sepsis neocynipsea (Diptera: Sepsidae), we tested for historical gene flow with the aid of ABBA-BABA test using whole-genome resequencing data from pooled DNA of male specimens originating from natural and laboratory populations. We contrasted genome-wide variation in DNA sequence differences between samples from sympatric populations of the two species in France and Switzerland with that of interspecific differences between pairs of samples involving allopatric populations from Estonia and Italy. In the French Cevennes, we detected a relative excess of DNA sequence identity, suggesting interspecific gene flow in sympatry. In contrast, at two sites in Switzerland, we observed a relative depletion of DNA sequence identity compatible with reinforcement of species boundaries in sympatry. Our results suggest that the species boundaries between S. cynipsea and S. neocynipsea in Europe depend on the eco-geographic context.


2018 ◽  
Author(s):  
Krzysztof M. Kozak ◽  
W. Owen McMillan ◽  
Mathieu Joron ◽  
Christopher D. Jiggins

ABSTRACTHow frequent is gene flow between species? The pattern of evolution is typically portrayed as a phylogenetic tree, implying that speciation is a series of splits between lineages. Yet gene flow between good species is increasingly recognized as an important mechanism in the diversification of radiations, often spreading adaptive traits and leading to a complex pattern of phylogenetic incongruence. This process has thus far been studied in cases involving few species, or geographically restricted to spaces like islands, but not on the scale of a continental radiation. Previous studies have documented gene flow, adaptive introgression and hybrid speciation in a small subsection of the charismatic Neotropical butterflies Heliconius. Using genome-wide resequencing of 40 out of 45 species in the genus we demonstrate for the first time that admixture has played a role throughout the evolution of Heliconius and the sister genus Eueides. Modelling of phylogenetic networks based on 6848 orthologous autosomal genes (Maximum Pseudo-Likelihood Networks) or 5,483,419 high quality SNPs (Ancestral Recombination Graph) uncovers nine new cases of interspecific gene flow at up to half of the genome. However, f4 statistics of admixture show that the extent of the process has varied between subgenera. Evidence for introgression is found at all five loci controlling the colour and shape of the mimetic wing patterns, including in the putative hybrid species H. hecalesia, characterised by an unusual hindwing. Due to hybridization and incomplete coalescence during rapid speciation, individual gene trees show rampant discordance. Although reduced gene flow and faster coalescence are expected at the Z chromosome, we discover high levels of conflict between the 416 sex-linked loci. Despite this discordant pattern, both concatenation and multispecies coalescent approaches yield surprisingly consistent and fully supported genome-wide phylogenies. We conclude that the imposition of the bifurcating tree model without testing for interspecific gene flow may distort our perception of adaptive radiations and thus the ability to study trait evolution in a comparative framework.


2017 ◽  
Vol 114 (27) ◽  
pp. 7061-7066 ◽  
Author(s):  
Simon Aeschbacher ◽  
Jessica P. Selby ◽  
John H. Willis ◽  
Graham Coop

The interplay of divergent selection and gene flow is key to understanding how populations adapt to local environments and how new species form. Here, we use DNA polymorphism data and genome-wide variation in recombination rate to jointly infer the strength and timing of selection, as well as the baseline level of gene flow under various demographic scenarios. We model how divergent selection leads to a genome-wide negative correlation between recombination rate and genetic differentiation among populations. Our theory shows that the selection density (i.e., the selection coefficient per base pair) is a key parameter underlying this relationship. We then develop a procedure for parameter estimation that accounts for the confounding effect of background selection. Applying this method to two datasets from Mimulus guttatus, we infer a strong signal of adaptive divergence in the face of gene flow between populations growing on and off phytotoxic serpentine soils. However, the genome-wide intensity of this selection is not exceptional compared with what M. guttatus populations may typically experience when adapting to local conditions. We also find that selection against genome-wide introgression from the selfing sister species M. nasutus has acted to maintain a barrier between these two species over at least the last 250 ky. Our study provides a theoretical framework for linking genome-wide patterns of divergence and recombination with the underlying evolutionary mechanisms that drive this differentiation.


Author(s):  
Krzysztof M Kozak ◽  
Mathieu Joron ◽  
W Owen McMillan ◽  
Chris D Jiggins

Abstract How frequent is gene flow between species? The pattern of evolution is typically portrayed as a phylogenetic tree, yet gene flow between good species may be an important mechanism in diversification, spreading adaptive traits and leading to a complex pattern of phylogenetic incongruence. This process has thus far been studied mainly among a few closely related species, or in geographically restricted areas such as islands, but not on the scale of a continental radiation. Using a nearly complete genomic representation of 47 species in the genus, we demonstrate that admixture has played a role throughout the evolution of the charismatic Neotropical butterflies Heliconius. Modeling of phylogenetic networks based on the exome uncovers up to 13 instances of interspecific gene flow. Admixture is detected among the relatives of H. erato, as well as between the ancient lineages leading to modern clades. Interspecific gene flow played a role throughout the evolution of the genus, although the process has been most frequent in the clade of H. melpomene and relatives. We identify H. hecalesia and relatives as putative hybrids, including new evidence for introgression at the loci controlling the mimetic wing patterns. Models accounting for interspecific gene flow yield a more complete picture of the radiation as a network, which will improve our ability to study trait evolution in a realistic comparative framework.


2020 ◽  
Author(s):  
Steven M. Van Belleghem ◽  
Jared M. Cole ◽  
Gabriela Montejo-Kovacevich ◽  
Caroline N. Bacquet ◽  
W. Owen McMillan ◽  
...  

AbstractCharacterizing the genetic architecture of species boundaries remains a difficult task. Hybridizing species provide a powerful system to identify the factors that shape genomic variation and, ultimately, identify the regions of the genome that maintain species boundaries. Unfortunately, complex histories of isolation, admixture and selection can generate heterogenous genomic landscapes of divergence which make inferences about the regions that are responsible for species boundaries problematic. However, as the signal of admixture and selection on genomic loci varies with recombination rate, their relationship can be used to infer their relative importance during speciation. Here, we explore patterns of genomic divergence, admixture and recombination rate among hybridizing lineages across the Heliconius erato radiation. We focus on the incipient species, H. erato and H. himera, and distinguish the processes that drive genomic divergence across three contact zones where they frequently hybridize. Using demographic modeling and simulations, we infer that periods of isolation and selection have been major causes of genome-wide correlation patterns between recombination rate and divergence between these incipient species. Upon secondary contact, we found surprisingly highly asymmetrical introgression between the species pair, with a paucity of H. erato alleles introgressing into the H. himera genomes. We suggest that this signal may result from a current polygenic species boundary between the hybridizing lineages. These results contribute to a growing appreciation for the importance of polygenic architectures of species boundaries and pervasive genome-wide selection during the early stages of speciation with gene flow.


2014 ◽  
Author(s):  
Jared A Grummer ◽  
Martha L. Calderón ◽  
Adrián Nieto Montes-de Oca ◽  
Eric N Smith ◽  
Fausto Méndez-de la Cruz ◽  
...  

Interspecific gene flow is pervasive throughout the tree of life. Although detecting gene flow between populations has been facilitated by new analytical approaches, determining the timing and geography of hybridization has remained difficult, particularly for historical gene flow. A geographically explicit phylogenetic approach is needed to determine the ancestral population overlap. In this study, we performed population genetic analyses, species delimitation, simulations, and a recently developed approach of species tree diffusion to infer the phylogeographic history, timing and geographic extent of gene flow in lizards of the Sceloporus spinosus group. The two species in this group, S. spinosus and S. horridus, are distributed in eastern and western portions of Mexico, respectively, but populations of these species are sympatric in the southern Mexican highlands. We generated data consisting of three mitochondrial genes and eight nuclear loci for 148 and 68 individuals, respectively. We delimited six lineages in this group, but found strong evidence of mito-nuclear discordance in sympatric populations of S. spinosus and S. horridus owing to mitochondrial introgression. We used coalescent simulations to differentiate ancestral gene flow from secondary contact, but found mixed support for these two models. Bayesian phylogeography indicated more than 60% range overlap between ancestral S. spinosus and S. horridus populations since the time of their divergence. Isolation-migration analyses, however, revealed near-zero levels of gene flow between these ancestral populations. Interpreting results from both simulations and empirical data indicate that despite a long history of sympatry among these two species, gene flow in this group has only recently occurred.


2019 ◽  
Vol 192 (4) ◽  
pp. 675-690 ◽  
Author(s):  
Luiza D Hirsch ◽  
Camila M Zanella ◽  
Camila Aguiar-Melo ◽  
Laís M S Costa ◽  
Fernanda Bered

Abstract When related species are distributed in sympatric populations, hybridization may occur. Likewise, one or more of these species may have arisen through historical hybridization between taxa. Here, we aim to elucidate the occurrence of hybridization among three Dyckia spp. (Bromeliaceae) from southern Brazil. We used seven nuclear and six plastid microsatellite loci to assess patterns of genetic diversity, population structure and hybridization in the three species. Furthermore, we performed manual crosses between species to test compatibility and fertility. The results showed that Dyckia julianae has an intermediate molecular profile, low gene flow occurs between Dyckia hebdingii and Dyckia choristaminea and higher gene flow occurs between D. julianae and the other two species. Plastid microsatellites identified 12 haplotypes that are shared among the species. The manual crosses between D. julianae and the other two species produced viable seeds, but no crosses between D. hebdingii and D. choristaminea generated fruits. Our data suggest that the reproductive barrier between D. julianae and the other two species is permeable. Further investigation into the hybrid origin hypothesis of D. julianae should be undertaken, as well as the mechanisms involved in reproductive isolation between D. hebdingii and D. choristaminea.


2020 ◽  
Author(s):  
Heidi Mavengere ◽  
Katlheen Mattox ◽  
Marcus M Teixeira ◽  
Victoria E. Sepúlveda ◽  
Oscar M. Gomez ◽  
...  

ABSTRACTThe fungus Paracoccidioides spp. is a prevalent human pathogen endemic to South America. The genus is composed of five species. In this report, we use 37 whole genome sequences to study the allocation of genetic variation in Paracoccidioides. We tested three genome-wide predictions of advanced speciation, namely, that all species should be reciprocally monophyletic, that species pairs should be highly differentiated along the whole genome, and that there should be low rates of interspecific gene exchange. We find support for these three hypotheses. Species pairs with older divergences show no evidence of gene exchange, while more recently diverged species pairs show evidence of modest rates of introgression. Our results indicate that as divergence progresses, species boundaries become less porous among Paracoccidioides species. Our results suggest that species in Paracoccidioides are at different stages along the divergence continuum.IMPORTANCEParacoccidioides is the causal agent of the most frequent systemic mycosis in Latin America. Most of the inference of the evolutionary history of Paracoccidioides has used only a handful of molecular markers. In this report, we evaluate the extent of genome divergence among Paracoccidioides species and study the possibility of interspecific gene exchange. We find that all species are highly differentiated. We also find that the amount of gene flow between species is low and in some cases even completely absent in spite of geographic overlap. Our study constitutes a systematic effort to identify species boundaries in fungal pathogens, and determine the extent of gene exchange among fungal species.


2016 ◽  
Author(s):  
Simon Aeschbacher ◽  
Jessica P. Selby ◽  
John H. Willis ◽  
Graham Coop

AbstractThe interplay of divergent selection and gene flow is key to understanding how populations adapt to local environments and how new species form. Here, we use DNA polymorphism data and genome-wide variation in recombination rate to jointly infer the strength and timing of selection, as well as the baseline level of gene flow under various demographic scenarios. We model how divergent selection leads to a genome-wide negative correlation between recombination rate and genetic differentiation among populations. Our theory shows that the selection density, i.e. the selection coefficient per base pair, is a key parameter underlying this relationship. We then develop a procedure for parameter estimation that accounts for the confounding effect of background selection. Applying this method to two datasets from Mimulus guttatus, we infer a strong signal of adaptive divergence in the face of gene flow between populations growing on and off phytotoxic serpentine soils. However, the genome-wide intensity of this selection is not exceptional compared to what M. guttatus populations may typically experience when adapting to local conditions. We also find that selection against genome-wide introgression from the selfing sister species M. nasutus has acted to maintain a barrier between these two species over at least the last 250 ky. Our study provides a theoretical framework for linking genome-wide patterns of divergence and recombination with the underlying evolutionary mechanisms that drive this differentiation.


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