scholarly journals Selection and gene flow define polygenic barriers between incipient butterfly species

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.

2019 ◽  
Author(s):  
Xuejing Wang ◽  
Kathryn H. Maher ◽  
Nan Zhang ◽  
Pingjia Que ◽  
Chenqing Zheng ◽  
...  

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.


2019 ◽  
Author(s):  
Lewis G. Spurgin ◽  
Mirte Bosse ◽  
Frank Adriaensen ◽  
Tamer Albayrak ◽  
Christos Barboutis ◽  
...  

AbstractA major aim of evolutionary biology is to understand why patterns of genomic diversity vary among populations and species. Large-scale genomic studies of widespread species are useful for studying how the environment and demographic history shape patterns of genomic divergence, and with the continually decreasing cost of sequencing and genotyping, such studies are now becoming feasible. Here, we carry out one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning almost the entire geographic range of the European great tit subspecies. We found that genome-wide variation was consistent with a recent colonisation across Europe from a single refugium in South-East Europe, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear “islands of differentiation” even among populations with very low levels of genome-wide differentiation. Low local recombination rate in the genome was a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination is a key driver of highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, most likely as a result of recent directional selection at the range edges of this species. Haplotype-based measures of selection were also related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. These regions under positive selection contained candidate genes associated with morphology, thermal adaptation and colouration, providing promising avenues for future investigation. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into evolution.


Nature ◽  
2020 ◽  
Vol 588 (7836) ◽  
pp. 106-111 ◽  
Author(s):  
Andreas F. Kautt ◽  
Claudius F. Kratochwil ◽  
Alexander Nater ◽  
Gonzalo Machado-Schiaffino ◽  
Melisa Olave ◽  
...  

AbstractThe transition from ‘well-marked varieties’ of a single species into ‘well-defined species’—especially in the absence of geographic barriers to gene flow (sympatric speciation)—has puzzled evolutionary biologists ever since Darwin1,2. Gene flow counteracts the buildup of genome-wide differentiation, which is a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that complete the speciation process3. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs4, but empirical tests of this theory are scant because comprehensive data are difficult to collect and synthesize across species, owing to their unique biologies and evolutionary histories5. Here, within a young species complex of neotropical cichlid fishes (Amphilophus spp.), we analysed genomic divergence among populations and species. By generating a new genome assembly and re-sequencing 453 genomes, we uncovered the genetic architecture of traits that have been suggested to be important for divergence. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. By contrast, differentiation among species that have diverged in polygenic traits is genomically widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Thus, we conclude that simple trait architectures are not always as conducive to speciation with gene flow as previously suggested, whereas polygenic architectures can promote rapid and stable speciation in sympatry.


2007 ◽  
Vol 3 (6) ◽  
pp. 660-663 ◽  
Author(s):  
Kanchon K Dasmahapatra ◽  
Armando Silva-Vásquez ◽  
Jae-Woo Chung ◽  
James Mallet

Interspecific hybridization occurs regularly in wild Heliconius butterflies, although hybrid individuals are usually very rare. However, hybridization generally occurs only between the most closely related species. We report a rare naturally occurring hybrid between non-sister species and carry out the first genetic analysis of such distant hybridization. Mitochondrial and nuclear genes indicate that the specimen is an F 1 hybrid between a female Heliconius ethilla and a male Heliconius melpomene , originating from a group of 13 species estimated to have diverged over 2.5 Myr ago. The presence of such distant natural hybrids, together with evidence for backcrossing, suggests that gene flow across species boundaries can take place long after speciation. Adaptive genes such as those involved in wing coloration could thus be widely shared among members of this highly mimetic genus.


2017 ◽  
Author(s):  
Mitra Menon ◽  
Justin C. Bagley ◽  
Christopher Friedline ◽  
Amy V. Whipple ◽  
Anna W. Schoettle ◽  
...  

AbstractInteractions between extrinsic factors, such as disruptive selection, and intrinsic factors, such as genetic incompatibilities among loci, can contribute to the maintenance of species boundaries. The relative roles of these factors in the establishment of reproductive isolation can be examined using species pairs characterized by gene flow throughout their divergence history. We investigated the process of speciation and the maintenance of species boundaries between Pinus strobiformis and P.flexilis. Utilizing ecological niche modeling, demographic modeling, and genomic cline analyses, we illustrated a history of divergence with continuous gene flow between these species. We found an abundance of advanced generation hybrids and a lack of loci exhibiting large allele frequency differences across the hybrid zone. Additionally, we found evidence for climate-associated variation in the hybrid index and niche divergence between parental species and the hybrid zone. Our results are consistent with extrinsic factors, such as climate, being an important isolating mechanism for these species. A buildup of intrinsic incompatibilities and of co-adapted gene complexes is also apparent in our results, although these appear to be in the earliest stages of development. This supports previous work in coniferous species demonstrating the importance of extrinsic factors in creating and enforcing species boundaries. Overall, we lend support to the hypothesis that varying strengths and directions of selection pressures across the long lifespans of conifers, in combination with their life history strategies, delay the evolution of strong intrinsic incompatibilities.


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.


2016 ◽  
Author(s):  
Clément Rougeux ◽  
Louis Bernatchez ◽  
Pierre-Alexandre Gagnaire

AbstractParallel divergence patterns across replicated species pairs occurring in similar environmental contrasts may arise through distinct evolutionary scenarios. Deciphering whether such parallelism actually reflects repeated parallel divergence driven by divergent selection or a single divergence event with subsequent gene flow needs to be ascertained. Reconstructing historical gene flow is therefore of fundamental interest to understand how demography and selection jointly shaped genomic divergence during speciation. Here, we use an extended modeling framework to explore the multiple facets of speciation-with-gene-flow with demo-genetic divergence models that capture both temporal and genomic variation in effective population size and migration rate. We investigate the divergence history of five sympatric Lake Whitefish limnetic (dwarf) and benthic (normal) species pairs characterized by variable degrees of ecological divergence and reproductive isolation. Genome-wide SNPs were used to document the extent of genetic differentiation in each species pair, and 26 divergence models were fitted and compared to the unfolded joint allele frequency spectrum of each pair. We found evidence that a recent (circa 3000-4000 generations) asymmetrical secondary contact between expanding post-glacial populations has accompanied Whitefish diversification. Our results suggest that heterogeneous genomic differentiation patterns have emerged through the combined effects of linked selection generating variable rates of lineage sorting across the genome during geographical isolation, and heterogeneous introgression eroding divergence at different rates across the genome upon secondary contact. This study thus provides a new retrospective insight into the historical demographic and selective processes that shaped a continuum of divergence associated with ecological speciation.


2019 ◽  
Author(s):  
Sarah W. Fitzpatrick ◽  
Gideon S. Bradburd ◽  
Colin T. Kremer ◽  
Patricia E. Salerno ◽  
Lisa M. Angeloni ◽  
...  

AbstractGene flow is an enigmatic evolutionary force because it can limit adaptation but can also help populations escape inbreeding depression. Manipulating gene flow for conservation purposes is a controversial, but potentially powerful management strategy. We use multigenerational pedigrees and genomics to test demographic and evolutionary consequences of manipulating gene flow in two isolated wild Trinidadian guppy populations. We found that on average, hybrids lived longer and reproduced more. Despite overall genome-wide homogenization, alleles potentially associated with local adaptation were not entirely swamped by gene flow. Our results suggest that combining new genomic variation from immigrants with potentially adaptive variation from the recipient population resulted in highly fit hybrids and subsequent increases in population size. Contrary to the prevailing view that gene flow constrains adaptation, our study shows that immigration can produce long-term fitness benefits in small populations without swamping locally adaptive variation.


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.


2017 ◽  
Vol 284 (1850) ◽  
pp. 20162414 ◽  
Author(s):  
Rachael A. Bay ◽  
Kristen Ruegg

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.


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