scholarly journals Genome-wide admixture is common across the Heliconius radiation

2018 ◽  
Author(s):  
Krzysztof M. Kozak ◽  
W. Owen McMillan ◽  
Mathieu Joron ◽  
Christopher D. Jiggins
Keyword(s):  
Gene Flow ◽  
Phylogenetic Networks ◽  
Z Chromosome ◽  
Putative Hybrid ◽  
Gene Trees ◽  
Tree Model ◽  
Interspecific Gene Flow ◽  
Individual Gene ◽  
Multispecies Coalescent ◽  
Genome Wide

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.

scholarly journals Rampant genome-wide admixture across the Heliconius radiation

2021 ◽  
Author(s):  
Krzysztof M Kozak ◽  
Mathieu Joron ◽  
W Owen McMillan ◽  
Chris D Jiggins
Keyword(s):  
Gene Flow ◽  
Phylogenetic Networks ◽  
Adaptive Traits ◽  
Closely Related Species ◽  
Interspecific Gene Flow ◽  
Genomic Representation ◽  
Genome Wide ◽  
Wing Patterns ◽  
New Evidence ◽  
Complete Genomic

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.

scholarly journals Genome-wide local ancestries discriminate homoploid hybrid speciation from secondary introgression in the red wolf (Canidae: Canis rufus)

2020 ◽  
Author(s):  
Tyler K. Chafin ◽  
Marlis R. Douglas ◽  
Michael E. Douglas
Keyword(s):  
Gene Flow ◽  
X Chromosome ◽  
North American ◽  
Gene Trees ◽  
Canis Rufus ◽  
Red Wolf ◽  
Genome Wide ◽  
Homoploid Hybrid ◽  
Divergence Estimates ◽  
The Impact

AbstractHybridization is well recognized as a driver of speciation, yet it often remains difficult to parse phylogenomically in that post-speciation gene flow frequently supersedes an ancestral signal. Here we examined how interactions between recombination and gene flow shaped the phylogenomic landscape of red wolf to create non-random retention of introgressed ancestry. Our re-analyses of genomic data recapitulate fossil evidence by demonstrating red wolf was indeed extant and isolated prior to more recent admixture with other North American canids. Its more ancient divergence, now sequestered within low-recombinant regions on the X-chromosome (i.e., chromosomal ‘refugia’), is effectively masked by multiple, successive waves of secondary introgression that now dominate its autosomal ancestry. These interpretations are congruent with more theoretical explanations that describe the manner by which introgression can be localized within the genome through recombination and selection. They also tacitly support the large-X effect, i.e., the manner by which loci that contribute to reproductive isolation can be enriched on the X-chromosome. By contrast, similar, high recombinant regions were also found as enriched within very shallow gene trees, thus reflecting post-speciation gene flow and a compression of divergence estimates to 1/20th of that found in recombination ‘cold spots’. Our results effectively reconcile conflicting hypotheses regarding the impact of hybridization on evolution of North American canids and support an emerging framework within which the analysis of a phylogenomic landscape structured by recombination can be used to successfully address the macroevolutionary implications of hybridization.

scholarly journals Ancient and recent introgression shape the evolutionary history of pollinator adaptation and speciation in a model monkeyflower radiation (Mimulus section Erythranthe)

2020 ◽  
Author(s):  
Thomas C. Nelson ◽  
Angela M. Stathos ◽  
Daniel D. Vanderpool ◽  
Findley R. Finseth ◽  
Yao-wu Yuan ◽  
...  
Keyword(s):  
Gene Flow ◽  
Evolutionary History ◽  
Species Tree ◽  
Sister Species ◽  
Pollination Syndrome ◽  
Gene Trees ◽  
Trait Evolution ◽  
Genome Wide ◽  
Hummingbird Pollination ◽  
History Of

AbstractInferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species). Taxa within Erythranthe, particularly the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M. cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M. lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele-sharing (Patterson’s D-statistic and related tests) indicate that gene-tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M. lewisii and M. cardinalis. Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M. lewisii and Southern Californian M. parishii each carrying organelle genomes nested within respective sympatric M. cardinalis clades. A recent organellar transfer from M. cardinalis, an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M. parishii organelles in hybrids with M. lewisii. Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.Author SummaryAdaptive radiations, which involve both divergent evolution of new traits and recurrent trait evolution, provide insight into the processes that generate and maintain organismal diversity. However, rapid radiations also generate particular challenges for inferring the evolutionary history and mechanistic basis of adaptation and speciation, as multiple processes can cause different parts of the genome to have distinct phylogenetic trees. Thus, inferences about the mode and timing of divergence and the causes of parallel trait evolution require a fine-grained understanding of the flow of genomic variation through time. In this study, we used genome-wide sampling of thousands of genes to re-construct the evolutionary histories of a model plant radiation, the monkeyflowers of Mimulus section Erythranthe. Work over the past half-century has established the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated, as are three other species in the section) as textbook examples of both rapid speciation via shifts in pollination syndrome and convergent evolution of floral syndromes. Our phylogenomic analyses re-write both of these stories, placing M. cardinalis in a clade with other hummingbird-pollinated taxa and demonstrating that abundant introgression between ancestral lineages as well as in areas of current sympatry contributes to the real (but misleading) affinities between M. cardinalis and M. lewisii. This work illustrates the pervasive influence of gene flow and introgression during adaptive radiation and speciation, and underlines the necessity of a gene-scale and genome-wide phylogenomics framework for understanding trait divergence, even among well-established species.

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

2020 ◽  
Author(s):  
Athene Giesen ◽  
Wolf U. Blanckenhorn ◽  
Martin A. Schäfer ◽  
Kentaro K. Shimizu ◽  
Rie Shimizu-Inatsugi ◽  
...  
Keyword(s):  
Gene Flow ◽  
Dna Sequence ◽  
Species Boundaries ◽  
Adaptive Divergence ◽  
Sympatric Populations ◽  
Interspecific Gene Flow ◽  
Natural Systems ◽  
Sequence Identity ◽  
Interspecific Differences ◽  
Genome Wide

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.

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

2021 ◽  
Author(s):  
Athene Giesen ◽  
Wolf Blanckenhorn ◽  
Martin Schäfer ◽  
Kentaro K. Shimizu ◽  
Rie Shimizu-Inatsugi ◽  
...  
Keyword(s):  
Gene Flow ◽  
Dna Sequence ◽  
Species Boundaries ◽  
Adaptive Divergence ◽  
Sympatric Populations ◽  
Interspecific Gene Flow ◽  
Natural Systems ◽  
Sequence Identity ◽  
Interspecific Differences ◽  
Genome Wide

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.

scholarly journals Demographic histories and genome-wide patterns of divergence in incipient species of shorebirds

2019 ◽  
Author(s):  
Xuejing Wang ◽  
Kathryn H. Maher ◽  
Nan Zhang ◽  
Pingjia Que ◽  
Chenqing Zheng ◽  
...  
Keyword(s):  
Gene Flow ◽  
Evolutionary Biology ◽  
De Novo ◽  
Secondary Contact ◽  
Z Chromosome ◽  
Phenotypic Traits ◽  
Incipient Species ◽  
Genome Wide ◽  
Genomic Regions ◽  
Kentish Plover

AbstractUnderstanding how incipient species are maintained with gene flow is a fundamental question in evolutionary biology. Whole genome sequencing of multiple individuals holds great potential to illustrate patterns of genomic differentiation as well as the associated evolutionary histories. Kentish (Charadrius alexandrinus) and the white-faced (C. dealbatus) plovers, which differ in their phenotype, ecology and behaviour, are two incipient species and parapatrically distributed in East Asia. Previous studies show evidence of genetic diversification with gene flow between the two plovers. Under this scenario, it is of great importance to explore the patterns of divergence at the genomic level and to determine whether specific regions are involved in reproductive isolation and local adaptation. Here we present the first population genomic analysis of the two incipient species based on the de novo Kentish plover reference genome and resequenced populations. We show that the two plover lineages are distinct in both nuclear and mitochondrial genomes. Using model-based coalescence analysis, we found that population sizes of Kentish plover increased whereas white-faced plovers declined during the Last Glaciation Period. Moreover, the two plovers diverged allopatrically, with gene flow occurring after secondary contact. This has resulted in low levels of genome-wide differentiation, although we found evidence of a few highly differentiated genomic regions in both the autosomes and the Z-chromosome. This study illustrates that incipient shorebird species with gene flow after secondary contact can exhibit discrete divergence at specific genomic regions and provides basis to further exploration on the genetic basis of relevant phenotypic traits.

scholarly journals Inference of Species Phylogenies from Bi-allelic Markers Using Pseudo-likelihood

2018 ◽  
Author(s):  
Jiafan Zhu ◽  
Luay Nakhleh
Keyword(s):  
Network Inference ◽  
Sequence Data ◽  
Phylogenetic Network ◽  
Simulated Data ◽  
Biological Data ◽  
Phylogenetic Networks ◽  
Gene Trees ◽  
Multispecies Coalescent ◽  
Pseudo Likelihood ◽  
Computational Bottleneck

AbstractMotivationPhylogenetic networks represent reticulate evolutionary histories. Statistical methods for their inference under the multispecies coalescent have recently been developed. A particularly powerful approach uses data that consist of bi-allelic markers (e.g., single nucleotide polymorphism data) and allows for exact likelihood computations of phylogenetic networks while numerically integrating over all possible gene trees per marker. While the approach has good accuracy in terms of estimating the network and its parameters, likelihood computations remain a major computational bottleneck and limit the method’s applicability.ResultsIn this paper, we first demonstrate why likelihood computations of networks take orders of magnitude more time when compared to trees. We then propose an approach for inference of phylo-genetic networks based on pseudo-likelihood using bi-allelic markers. We demonstrate the scalability and accuracy of phylogenetic network inference via pseudo-likelihood computations on simulated data. Furthermore, we demonstrate aspects of robustness of the method to violations in the underlying assumptions of the employed statistical model. Finally, we demonstrate the application of the method to biological data. The proposed method allows for analyzing larger data sets in terms of the numbers of taxa and reticulation events. While pseudo-likelihood had been proposed before for data consisting of gene trees, the work here uses sequence data directly, offering several advantages as we discuss.AvailabilityThe methods have been implemented in PhyloNet (http://bioinfocs.rice.edu/phylonet)[email protected], [email protected]

scholarly journals Molecular Signatures of Reticulate Evolution within the Complex of European Pine Taxa

Forests ◽  
2021 ◽  
Vol 12 (4) ◽  
pp. 489
Author(s):  
Bartosz Łabiszak ◽  
Witold Wachowiak
Keyword(s):  
Gene Flow ◽  
Reticulate Evolution ◽  
Modeling Framework ◽  
Closely Related Species ◽  
Interspecific Gene Flow ◽  
Nucleotide Sequence Variation ◽  
History Of ◽  
Best Fitting ◽  
Species Integrity

Speciation mechanisms, including the role of interspecific gene flow and introgression in the emergence of new species, are the major focus of evolutionary studies. Inference of taxonomic relationship between closely related species may be challenged by past hybridization events, but at the same time, it may provide new knowledge about mechanisms responsible for the maintenance of species integrity despite interspecific gene flow. Here, using nucleotide sequence variation and utilizing a coalescent modeling framework, we tested the role of hybridization and introgression in the evolutionary history of closely related pine taxa from the Pinus mugo complex and P. sylvestris. We compared the patterns of polymorphism and divergence between taxa and found a great overlap of neutral variation within the P. mugo complex. Our phylogeny reconstruction indicated multiple instances of reticulation events in the past, suggesting an important role of interspecific gene flow in the species divergence. The best-fitting model revealed P. mugo and P. uncinata as sister species with basal P. uliginosa and asymmetric migration between all investigated species after their divergence. The magnitude of interspecies gene flow differed greatly, and it was consistently stronger from representatives of P. mugo complex to P. sylvestris than in the opposite direction. The results indicate the prominent role of reticulation evolution in those forest trees and provide a genetic framework to study species integrity maintained by selection and local adaptation.

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