scholarly journals Genomic islands of divergence or opportunities for introgression?

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.

2017 ◽  
Author(s):  
Maud Duranton ◽  
François Allal ◽  
Christelle Fraïsse ◽  
Nicolas Bierne ◽  
François Bonhomme ◽  
...  

AbstractSpeciation is a complex process that leads to the progressive establishment of reproductive isolation barriers between diverging populations. Genome-wide comparisons between closely related species have revealed the existence of heterogeneous divergence patterns, dominated by genomic islands of increased divergence supposed to contain reproductive isolation loci. However, this divergence landscape only provides a static picture of the dynamic process of speciation, during which confounding mechanisms unlinked to speciation can interfere. Here, we used haplotype-resolved whole-genome sequences to identify the mechanisms responsible for the formation of genomic islands between Atlantic and Mediterranean sea bass lineages. We show that genomic islands first emerged in allopatry through the effect of linked selection acting on a heterogeneous recombination landscape. Upon secondary contact, preexisting islands were strongly remolded by differential introgression, revealing variable fitness effects among regions involved in reproductive isolation. Interestingly, we found that divergent regions containing ancient polymorphisms conferred the strongest resistance to introgression.


Author(s):  
S. Eryn McFarlane ◽  
Helen V. Senn ◽  
Stephanie L. Smith ◽  
Josephine M. Pemberton

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.


Author(s):  
Linda Hagberg ◽  
Enrique Celemin ◽  
Iker Irisarri ◽  
Oliver Hawlitschek ◽  
J L Bella ◽  
...  

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.


2021 ◽  
Author(s):  
Tyler K Chafin ◽  
Binod Regmi ◽  
Marlis R. Douglas ◽  
David R. Edds ◽  
Karma Wangchuk ◽  
...  

Replicated evolutionary patterns are often attributed to recurrent emergence following parallel selective pressures. However, similar genetic patterns (e.g., 'genomic islands') can also emerge following extensive homogenization in secondary contact, as a by-product of heterogeneous introgression. For example, within Himalayan tributaries of the Ganges/Brahmaputra rivers, drainage-specific mtDNA clades of polyploid snowtrout (Cyprinidae: Schizothorax) are partitioned as co-occurring morphological 'ecotypes,' hypothesized to represent parallel divergence among adjacent streams. To evaluate this scenario, we utilized a reduced-representation genomic approach (N=35,319 de-novo and N=10,884 transcriptome-aligned SNPs) applied to high-altitude Nepali/Bhutanese snowtrout (N=48 each). We unambiguously quantified ploidy levels by first deriving genome-wide allelic depths followed by ploidy-aware Bayesian models that produced genotypes statistically consistent with diploid/tetraploid expectations. When genotyped SNPs were clustering within drainages, the convergence of eco-phenotypes was sustained. However, subsequent partitioned analyses of phylogeny and population admixture instead identified subsets of loci under selection which retained genealogical concordance with morphology, with apparent patterns of parallel ecotype emergence instead driven by widespread genomic homogenization. Here, prior isolation is effectively masked by admixture occurring in secondary contact. We note two salient factors:1) Polyploidy has promoted homogenization in tetraploid Himalayan snowtrout; and 2) Homogenization varies across Himalayan tributaries, presumably in lockstep with extent of anthropogenic modification.


2020 ◽  
Vol 10 (9) ◽  
pp. 3147-3163
Author(s):  
Ashley T Sendell-Price ◽  
Kristen C Ruegg ◽  
Eric C Anderson ◽  
Claudio S Quilodrán ◽  
Benjamin M Van Doren ◽  
...  

Abstract Inferring the evolutionary dynamics at play during the process of speciation by analyzing the genomic landscape of divergence is a major pursuit in population genomics. However, empirical assessments of genomic landscapes under varying evolutionary scenarios that are known a priori are few, thereby limiting our ability to achieve this goal. Here we combine RAD-sequencing and individual-based simulations to evaluate the genomic landscape of divergence in the silvereye (Zosterops lateralis). Using pairwise comparisons that differ in divergence timeframe and the presence or absence of gene flow, we document how genomic patterns accumulate along the speciation continuum. In contrast to previous predictions, our results provide limited support for the idea that divergence accumulates around loci under divergent selection or that genomic islands widen with time. While a small number of genomic islands were found in populations diverging with and without gene flow, in few cases were SNPs putatively under selection tightly associated with genomic islands. The transition from localized to genome-wide levels of divergence was captured using individual-based simulations that considered only neutral processes. Our results challenge the ubiquity of existing verbal models that explain the accumulation of genomic differences across the speciation continuum and instead support the idea that divergence both within and outside of genomic islands is important during the speciation process.


2022 ◽  
Author(s):  
Jean R David ◽  
Erina A Ferreira ◽  
Laure Jabaud ◽  
David Ogereau ◽  
Héloïse Bastide ◽  
...  

Adaptive introgression is ubiquitous in animals but experimental support for its role in driving speciation remains scarce. In the absence of conscious selection, admixed laboratory strains of Drosophila asymmetrically and progressively lose alleles from one parental species and reproductive isolation against the predominant parent ceases after 10 generations. Here, we selectively introgressed during one year light pigmentation genes of D. santomea into the genome of its dark sibling D. yakuba, and vice versa. We found that the pace of phenotypic change differed between the species and the sexes, and identified through genome sequencing common as well as distinct introgressed loci in each species. Mating assays showed that assortative mating between introgressed flies and both parental species persisted even after four years (~ 60 generations) from the end of the selection. Those results indicate that selective introgression of as low as 0.5% of the genome can beget morphologically-distinct and reproductively-isolated strains, two prerequisites for the delimitation of new species. Our findings hence represent a significant step towards understanding the genome-wide dynamics of speciation-through-introgression.


2021 ◽  
Vol 12 ◽  
Author(s):  
Mohamed Abdelaziz ◽  
A. Jesús Muñoz-Pajares ◽  
Modesto Berbel ◽  
Ana García-Muñoz ◽  
José M. Gómez ◽  
...  

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.


2019 ◽  
Author(s):  
I. van Riemsdijk ◽  
J.W. Arntzen ◽  
G. Bucciarelli ◽  
E. McCartney-Melstad ◽  
M. Rafajlović ◽  
...  

AbstractThe barrier effect is a restriction of gene flow between diverged populations by barrier genes. Restriction of gene flow and asymmetric introgression over multiple transects indicates species wide (genetic) adaptations, whereas transect-specific barrier loci may indicate local adaptation to gene flow. Asymmetric introgression can be caused by selection, hybrid zone movement, asymmetric reproductive isolation, or a combination of these. We study two widely separated transects (northwest and southeast France) for the 900 km long hybrid zone between Bufo bufo and B. spinosus toads, using ~1200 markers from restriction-site associated DNA (RAD) sequencing data. Genomic and geographic clines were used to identify outlier markers which show restricted or elevated introgression. Twenty-six barrier markers are shared between transects (the union of 56 and 123 barrier markers identified in each transect), which is more than would be expected by chance. However, the number of barrier markers is twice as high in the southeast transect. In the northwest transect a high amount of (asymmetric) introgression from B. spinosus into B. bufo is consistent with hybrid zone movement or asymmetric reproductive isolation. In the southeast transect, introgression is symmetric and consistent with a stable hybrid zone. Differences between transects may be related to genetic sub-structure within B. bufo. A longer period of secondary contact in southeast France appears to result in a relatively stronger barrier effect than in the northwest. The Bufo hybrid zone provides an excellent opportunity to separate a general barrier to gene flow from local reductions in gene flow.


2020 ◽  
Vol 375 (1806) ◽  
pp. 20190548 ◽  
Author(s):  
Yo Y. Yamasaki ◽  
Ryo Kakioka ◽  
Hiroshi Takahashi ◽  
Atsushi Toyoda ◽  
Atsushi J. Nagano ◽  
...  

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’.


2020 ◽  
Vol 7 (6) ◽  
pp. 191805
Author(s):  
Emrah Çoraman ◽  
Heliana Dundarova ◽  
Christian Dietz ◽  
Frieder Mayer

Secondary contacts can play a major role in the evolutionary histories of species. Various taxa diverge in allopatry and later on come into secondary contact during range expansions. When they meet, their interactions and the extent of gene flow depend on the level of their ecological differentiation and the strength of their reproductive isolation. In this study, we present the multilocus phylogeography of two cryptic whiskered bat species, Myotis mystacinus and M. davidii , with a particular focus on their putative sympatric zone. Our findings suggest that M. mystacinus and M. davidii evolved in allopatry and came into secondary contact during range expansions. Individuals in the area of secondary contact, in Anatolia and the Balkans, have discordant population assignments based on the mitochondrial and the nuclear datasets. These observed patterns suggest that the local M. mystacinus populations hybridized with expanding M. davidii populations, which resulted in mitochondrial introgression from the former. In the introgression area, M. mystacinus individuals with concordant nuclear and mitochondrial genotypes were identified in relatively few locations, suggesting that the indigenous populations might have been largely replaced by invading M. davidii . Changing environmental conditions coupled with ecological competition is the likely reason for this replacement. Our study presents one possible example of a historical population replacement that was captured in phylogeographic patterns.


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