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opencc-by-4.0Jul 2024View details →

Beyond gene flow: (non)-parallelism of secondary contact in a pair of highly differentiated sibling species

Replicated secondary contact zones can provide insights on the barriers to gene flow that are important during speciation and can reveal to which degree secondary contact may result in similar evolutionary outcomes. Here, we studied two secondary contact zones between highly differentiated Alpine butterflies of the genus Erebia using whole-genome re-sequencing data. We assessed the genomic relationships between populations and species and find hybridization to be rare, with no to little current or historical introgression in either contact zone. There are large similarities between the contact zones, consistent with an allopatric origin of interspecific differentiation, with no indications for ongoing reinforcing selection. Consistent with expected reduced effective population size, we further find that scaffolds related to the Z-chromosome show increased differentiation compared to the already high levels across the entire genome, which could also hint towards a contribution of the Z chromosome to species divergence in this system. Finally, we detected the presence of the endosymbiont Wolbachia, which can cause reproductive isolation between its hosts, in all E. cassioides, while it appears to be fully or largely absent in contact zone populations of E. tyndarus. We discuss how this rare pattern may have arisen and how it may have affected the dynamics of speciation upon secondary contact.

Fig. 11 in Introgression at the emerging secondary contact zone of magpie Pica pica subspecies (Aves: Corvidae): integrating data on nuclear and mitochondrial markers, vocalizations, and field observations

Fig. 11 Rates of chatter calls in different magpie populations and individuals. a Each mark represents average chattering rate for a single bird from five populations indicated by colours. Figures are numbers for the outliers: 1, 2—jankowskii from the mixed population of Argun'; 3, 4, 5—hybrid birds from the hybridogeneous population of Kerulen. b Each mark represents average chattering rate for a series of chatterings of one selected individual representing jankowskii, leucoptera, and hybrid birds, respectively. Green mark—pair #6 jankowskii from Vladivostok; gray—pair #43 leucoptera from Tsasuchei, Transbaikalia; blue—pair #24 hybrids from Kerulen, eastern Mongolia. X-axis—number of elements per second in a total series of chattering; Y-axis— number of elements per second in a series of 5 elements of chattering

Fig. 12 in Introgression at the emerging secondary contact zone of magpie Pica pica subspecies (Aves: Corvidae): integrating data on nuclear and mitochondrial markers, vocalizations, and field observations

Fig. 12 Violin plot diagram of the chatter call speed (elements per second) of Eurasian magpie populations across regions. X-axis presents a set of populations; Y-axis—elements per second. Box outlines the interquantile range (25%, 75%), whiskers represent range without outliers, central bar is the median, red dot is the mean, and figure shape is the probability density. The brackets on the top denote statistically significant pairwise differences (GamesHowell test, p<0.05)

Fig. 9 in Introgression at the emerging secondary contact zone of magpie Pica pica subspecies (Aves: Corvidae): integrating data on nuclear and mitochondrial markers, vocalizations, and field observations

Fig. 9 Population genetic structure based on unlinked SNP markers. Scatter plots of principal component analysis (PCA) show individual variation in components one and two (a) and three and four (b). The amount of variance explained by each PC is shown in parentheses. I—leucoptera,

Fig. 7 in Introgression at the emerging secondary contact zone of magpie Pica pica subspecies (Aves: Corvidae): integrating data on nuclear and mitochondrial markers, vocalizations, and field observations

Fig. 7 Bayesian skyline plots (BSPs) for effective female population sizes for haplogroups, subspecies, and populations of Pica pica. a Comparison of 6 haplogroups, depicted in the network Fig. 4. b Comparison of 6 subspecies. c Comparison of 4 populations of P. p. jankowskii. d Comparison of 3 populations of P. p. leucoptera.

Fig. 6 in Introgression at the emerging secondary contact zone of magpie Pica pica subspecies (Aves: Corvidae): integrating data on nuclear and mitochondrial markers, vocalizations, and field observations

Fig. 6 Mismatch distribution of nucleotide differences in populations representing different haplogroups as at Figs. 4 and 5. X-axis— number of nucleotide differences; Y-axis—proportion (frequency). Solid lines—expected distributions (under expectation of population growth); dashed lines—observed distributions. a Haplogroup 1:

Fig. 5 in Introgression at the emerging secondary contact zone of magpie Pica pica subspecies (Aves: Corvidae): integrating data on nuclear and mitochondrial markers, vocalizations, and field observations

Fig. 5 Time-calibrated Bayesian tree based on mitochondrial control region sequences of Pica pica. Numbers at the branches indicate Bayesian posterior probability values (left) and bootstrap values of the ML analysis (right, in percent). Triangle widths are proportional to specimen numbers. Blue bars next to nodes indicate 95% credibility intervals for their age estimates. The figures in bold and the time scale below are in million years (Ma) before present

Fig. 4 in Introgression at the emerging secondary contact zone of magpie Pica pica subspecies (Aves: Corvidae): integrating data on nuclear and mitochondrial markers, vocalizations, and field observations

Fig. 4 Phylogenetic medianjoining network based on 256 mitochondrial control region sequences. Sizes of circles correspond to the number of birds sharing this haplotype; branch lengths are proportional to the number of substitutions and those over 2 are shown at the branches. Haplogroups 1–6 are indicated by numbers

Fig. 2 in Introgression at the emerging secondary contact zone of magpie Pica pica subspecies (Aves: Corvidae): integrating data on nuclear and mitochondrial markers, vocalizations, and field observations

Fig. 2 Map of sampling localities for mitochondrial DNA analysis in the zone of contact between Pica pica leucoptera and Pica pica jankowskii. Distribution of haplotypes is indicated by colours: Pica

opencc-zeroJan 2020View details →

Assessing changes in genomic divergence following a century of human mediated secondary contact among wild and captive-bred ducks

Along with manipulating habitat, the direct release of domesticated individuals into the wild is a practice used world-wide to augment wildlife populations. We test between possible outcomes of human-mediated secondary contact using genomic techniques at both historical and contemporary time scales for two iconic duck species. First, we sequence several thousand ddRAD-seq loci for contemporary mallards (Anas platyrhynchos) throughout North America, and two domestic mallard-types (i.e., known game-farm mallards and feral Khaki Campbell's). We show that North American mallards may well be becoming a hybrid swarm due to interbreeding with domesticated game-farm mallards released for hunting. Next, to attain a historical perspective, we applied a bait-capture array targeting thousands of loci in century-old (1842-1915) and contemporary (2009-2010) mallard and American black duck (A. rubripes) specimens. We conclude that American black ducks and mallards have always been closely related, with a divergence time of ~600,000 years before present, and likely evolved through prolonged isolation followed by limited bouts of gene flow (i.e., secondary contact). They continue to maintain genetic separation, a finding that overturns decades of prior research and speculation suggesting the genetic extinction of the American black duck due to contemporary interbreeding with mallards. Thus, despite having high rates of hybridization, actual gene flow is limited between mallards and American black ducks. Conversely, our historical and contemporary data confirm that the intensive stocking of game-farm mallards during the last ~100 years has fundamentally changed the genetic integrity of North America's wild mallard population, especially in the east. It thus becomes of great interest to ask whether the iconic North American mallard is declining in the wild due to introgression of maladaptive traits from domesticated forms. Moreover, we hypothesize that differential gene flow from domestic game-farm mallards into the wild mallard population may explain the overall temporal increase in differentiation between wild black ducks and mallards, as well as the uncoupling of genetic diversity and effective population size estimates across time in our results. Finally, our findings highlight how genomic methods can recover complex population histories by capturing DNA preserved in traditional museum specimens.

opencc-zeroMar 2024View details →

Data from: Inference of selective force on house mice genomes during secondary contact in East Asia

The house mouse (Mus musculus), commensal to humans, has spread globally via human activities, leading to secondary contact between genetically divergent subspecies. This pattern of genetic admixture can provide insights into the selective forces at play in this well-studied model organism. Our analysis of 163 house mouse genomes, mainly from East Asia, revealed substantial admixture between the subspecies castaneus and musculus, particularly in Japan and southern China. We revealed, despite the admixture, that all Y chromosomes in the East Asian samples belonged to the musculus-type haplogroup, potentially explained by genomic conflict under sex ratio distortion due to varying copy numbers of ampliconic genes on sex chromosomes. We also investigated the influence of natural selection on the post-hybridization of the subspecies castaneus and musculus in Japan. Even though the genetic background of most Japanese samples closely resembles the subspecies musculus, certain genomic regions overrepresented the castaneus-like genetic components, particularly in immune-related genes. Furthermore, a large genomic block containing a vomeronasal/olfactory receptor gene cluster predominantly harbored castaneus-type haplotypes in the Japanese samples, highlighting the possible role of olfaction-based recognition in shaping hybrid genomes.

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Genomic data, part 1, of "Secondary contact rather than co-existence – Erebia butterflies in the Alps"

Secondary contact zones are ideal systems to study the processes that govern the evolution of reproductive barriers, especially at advanced stages of the speciation process. An increase in reproductive isolation resulting from selection against maladaptive hybrids is thought to contribute to reproductive barrier buildup in secondary contact zones. While such processes have been invoked for many systems, it remains unclear to which extent they influence contact zone dynamics in nature. Here, we study a very narrow contact zone between the butterfly species Erebia cassioides and E. tyndarus in the Swiss Alps. We quantified phenotypic traits related to wing shape and reproduction as well as ecology in order to compare the degree of intra- and interspecific differentiation. Even though only very few first-generation hybrids occur, we find no strong indications for current reinforcing selection, suggesting that if reinforcement occurred in our system, it likely operated in the past. Additionally, we show that both species differ less in their ecological niche at the contact zone than elsewhere, which could explain why co-existence between these butterflies may currently not be possible.

opencc-by-4.0Aug 2022View details →

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Genomic data, part 2, of "Secondary contact rather than co-existence – Erebia butterflies in the Alps"

Secondary contact zones are ideal systems to study the processes that govern the evolution of reproductive barriers, especially at advanced stages of the speciation process. An increase in reproductive isolation resulting from selection against maladaptive hybrids is thought to contribute to reproductive barrier buildup in secondary contact zones. While such processes have been invoked for many systems, it remains unclear to which extent they influence contact zone dynamics in nature. Here, we study a very narrow contact zone between the butterfly species Erebia cassioides and E. tyndarus in the Swiss Alps. We quantified phenotypic traits related to wing shape and reproduction as well as ecology in order to compare the degree of intra- and interspecific differentiation. Even though only very few first-generation hybrids occur, we find no strong indications for current reinforcing selection, suggesting that if reinforcement occurred in our system, it likely operated in the past. Additionally, we show that both species differ less in their ecological niche at the contact zone than elsewhere, which could explain why co-existence between these butterflies may currently not be possible.

opencc-by-4.0Aug 2022View details →

opencc-zeroDec 2020View details →

Parental population range expansion before secondary contact promotes heterosis

Population genomic analysis of hybrid zones is instrumental to our understanding of the evolution of reproductive isolation. Many temperate hybrid zones are formed by the secondary contact between two parental populations that have undergone post-glacial range expansion. Here we show that explicitly accounting for historical parental isolation followed by range expansion prior to secondary contact is fundamental for explaining genetic and fitness patterns in these hybrid zones. Specifically, ancestral population expansion can result in allele surfing where neutral or slightly deleterious mutations drift to high frequency at the expansion front. If these surfed deleterious alleles are recessive, they can contribute to substantial heterosis in hybrids produced at secondary contact, counteracting negative effects of Bateson-Dobzhansky-Muller incompatibilities (BDMIs) hence weakening reproductive isolation. When BDMIs are linked to such recessive deleterious alleles the fitness benefit of introgression at these loci can facilitate introgression at the BDMIs. The extent to which this occurs depends on the strength of selection against the linked deleterious alleles and the distribution of recombination across the chromosome. Finally, surfing of neutral loci can alter the expected pattern of population ancestry, thus accounting for historical population expansion is necessary to develop accurate null genomic models of secondary-contact hybrid zones.

opencc-zeroOct 2022View details →

Is there hybridisation between diploid and tetraploid Euphrasia in a secondary contact zone?

• Premise of the study: Hybridisation between species with contrasting ploidy is usually considered rare in nature due to strong ploidy related postzygotic reproductive isolating barriers. However, genomic sequencing has revealed previously overlooked examples of natural cross-ploidy hybridisation, suggesting this phenomenon may be more common than once thought. Here, we investigate potential cross-ploidy hybridisation in British eyebrights (Euphrasia, Orobanchaceae), a group where thirteen putative cross-ploidy hybrid combinations have been reported based on morphology. • Methods: We analysed a contact zone between diploid E. rostkoviana and tetraploid E. arctica in Wales. We sequenced part of the internal transcribed spacer of nuclear ribosomal DNA (ITS1) and used Genotyping by Sequencing (GBS) to look for evidence of cross-ploidy hybridisation and introgression. • Key results: All variant sites in the ITS1 region were fixed between diploids and tetraploids, indicating a strong barrier to hybridisation. Clustering analyses of 356 SNPs generated using GBS clearly separated samples by ploidy and revealed strong genetic structure (FST = 0.44). However, the FST distribution across all SNPs was bimodal, indicating potential differential selection on loci between diploids and tetraploids. Demographic inference with dadI suggested potential gene flow – with this limited to around one or fewer migrants per generation. • Conclusions: Our results suggest recent cross-ploidy hybridisation is rare or absent in a site of secondary contact in Euphrasia. While a strong ploidy barrier prevents hybridisation over ecological time-scales, such hybrids may form in stable populations over evolutionary time-scales and may allow for cross-ploidy introgression to take place.