Postglacial Colonization Research Articles

Widespread continental mtDNA lineages prevail in the bumblebee fauna of Iceland

Origins of the fauna in Iceland is controversial, although the majority of modern research supports the postglacial colonization of this island by terrestrial invertebrates rather than their long-term survival in glacial refugia. In this study, we use three bumblebee species as a model to test the hypothesis regarding possible cryptic refugia in Iceland and to evaluate a putative origin of recently introduced taxa. Bombus jonellus is thought to be a possible native Icelandic lineage, whereas B. lucorum and B. hortorum were evidently introduced in the second half of the 20th century. These phylogeographic analyses reveal that the Icelandic Bombus jonellus shares two COI lineages, one of which also occurs in populations on the British Isles and in mainland Europe, but a second lineage (BJ-02) has not been recorded anywhere. These results indicate that this species may have colonized Iceland two times and that the lineage BJ-02 may reflect a more ancient Late Pleistocene or Early Holocene founder event (e.g., from the British Isles). The Icelandic populations of both Bombus lucorum and B. hortorum share the COI lineages that were recorded as widespread throughout Eurasia, from the European countries across Russia to China and Japan. The findings presented here highlight that the bumblebee fauna of Iceland comprises mainly widespread ubiquitous lineages that arrived via natural or human-mediated dispersal events from the British Isles or the mainland.

Postglacial Colonization of the North European Seas by Pacific Fishes and Lamprey

A critical analysis of literature data on the distribution, morphology, and phylogeography of the Arctic lamprey (Lethenteron camtschaticum) and five species of marine and anadromous fish such as navaga (Eleginus navaga), pollock (Theragra chalcogramma), rainbow smelt (Osmerus mordax dentex), Pacific herring (Clupea pallasii), and pond smelt (Hypomesus olidus) has been performed. The results show that all these species have colonized Northern European seas, distributing along the Arctic coastline of Eurasia after the glacier retreat. The reasons that the dispersal of these species in the Atlantic Ocean may be impeded (preference for a cold environment, competition, and decrease of the evolutionary potential) are discussed.

Genomics of end-Pleistocene population replacement in a small mammal.

Current species distributions at high latitudes are the product of expansion from glacial refugia into previously uninhabitable areas at the end of the last glaciation. The traditional view of postglacial colonization is that southern populations expanded their ranges into unoccupied northern territories. Recent findings on mitochondrial DNA (mtDNA) of British small mammals have challenged this simple colonization scenario by demonstrating a more complex genetic turnover in Britain during the Pleistocene-Holocene transition where one mtDNA clade of each species was replaced by another mtDNA clade of the same species. Here, we provide evidence from one of those small mammals, the bank vole (Clethrionomys glareolus), that the replacement was genome-wide. Using more than 10 000 autosomal SNPs we found that similar to mtDNA, bank vole genomes in Britain form two (north and south) clusters which admix. Therefore, the genome of the original postglacial colonists (the northern cluster) was probably replaced by another wave of migration from a different continental European population (the southern cluster), and we gained support for this by modelling with approximate Bayesian computation. This finding emphasizes the importance of analysis of genome-wide diversity within species under changing climate in creating opportunities for sophisticated testing of population history scenarios.

Demography and mating system shape the genome-wide impact of purifying selection in Arabis alpina

Plant mating systems have profound effects on levels and structuring of genetic variation and can affect the impact of natural selection. Although theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population-genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles, whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, mating system and demography shape the impact of purifying selection on genomic variation in A. alpina These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.

Post-Glacial Colonization of the North European Seas by Pacific Fishes and Lamprey

Post-Glacial Colonization of the North European Seas by Pacific Fishes and Lamprey

Penguin colonization following the last glacial-interglacial transition in the Vestfold Hills, East Antarctica

The population history of the Adélie penguin (Pygoscelis adeliae) and its response to climatic and environmental changes have been widely studied in maritime Antarctica and several glacial refugia of Adélie penguins were dated back to the Last Glacial Maximum. However, the process of colony expansion during the subsequent glacial-interglacial transition was less well-documented. In this paper, we investigate an ornithogenic core from Vestfold Hills, East Antarctica, to improve knowledge of postglacial penguin colonization. Local deglaciation occurred around 15.6kyr BP, based on a coarse-grained detrital layer, a date that is earlier than most of those reported in other studies from the same region. Geochemical analysis of the core suggests penguins started colonizing the northern Vestfold Hills around 14.6kyr BP, the oldest geological record in East Antarctica on penguin occupation, and their population exhibited a broadly increasing trend thereafter. The population expanded at approximately 6740yr BP, in the mid-Holocene, which corresponds to a local climatic optimum. Although this inference is based on population changes of local sub-colonies, it corresponds well to reconstructions of regional climate change, and changes in the penguin population based on genetic studies. From a consideration of the results of previous studies of the occupation history of sea birds following deglaciation in the Arctic, as well as other parts of Antarctica, we propose that sea birds colonized the emerging ice-free areas shortly after local glacier retreat. Over geological time-scales, the availability of breeding habitat is a key factor controlling the population size and activity range of Antarctic Adélie penguins.

Notes on the postglacial spread of abundant European tree taxa

The reaction of vegetation to past climate change provides important insights for vegetation responses to future climate change. A key problem for projections into the future is obtaining estimates of the rates at which plants are able to spread as their environment changes. To address this uncertainty, we review the palaeoecological and phylogeographic literature to estimate the range of observed rates of spread for the major European trees and discuss aspects of their postglacial spread. The review is illustrated with isochrone maps depicting the time when particular thresholds in pollen proportion were reached in pollen diagrams available from the European Pollen Database. We find that rates of at least 1,000 m year−1 were realised by early colonisers including Corylus and Ulmus, while trees spreading later into established woodlands, e.g. Quercus and Tilia, achieved rates of around 500 m year−1. Phylogeographic investigations are available for most of the abundant European trees, often indicating that populations in the central and southern parts of the three south European peninsulas were not the origins for the postglacial colonization of central and northern Europe. In some cases, the results of these studies clearly show the direction of postglacial spread, while generally providing new information to help in interpreting pollen data. Phylogeographic results for Alnus suggest that the high apparent rates of postglacial spread are due to an initial spread at low population density and a later expansion. This decoupling between spread and population expansion is also seen for late expanding trees such as Picea, Fagus and Carpinus. Here, population expansion was probably not delayed by dispersal, but by a limiting climate as assumed by von Post. While the late Holocene expansion of Picea and Fagus in Sweden was important as a dating tool in the development of pollen analysis by von Post 100 years ago, we remain unable to determine which particular driver caused the late expansion of these two trees.

Evolution and postglacial colonization of Seewis hantavirus with Sorex araneus in Finland

Hantaviruses have co-existed with their hosts for millions of years. Seewis virus (SWSV), a soricomorph-borne hantavirus, is widespread in Eurasia, ranging from Central Siberia to Western Europe. To gain insight into the phylogeography and evolutionary history of SWSV in Finland, lung tissue samples of 225 common shrews (Sorex araneus) trapped from different parts of Finland were screened for the presence of SWSV RNA. Forty-two of the samples were positive. Partial small (S), medium (M) and large (L) segments of the virus were sequenced, and analyzed together with all SWSV sequences available in Genbank. The phylogenetic analysis of the partial S-segment sequences suggested that all Finnish SWSV strains shared their most recent common ancestor with the Eastern European strains, while the L-segment suggested multiple introductions. The difference between the L- and S-segment phylogenies implied that reassortment events play a role in the evolution of SWSV. Of the Finnish strains, variants from Eastern Finland occupied the root position in the phylogeny, and had the highest genetic diversity, supporting the hypothesis that SWSV reached Finland first form the east. During the spread in Finland, the virus has formed three separate lineages, identified here by correlation analysis of genetic versus geographic distance combined with median-joining network analysis. These results support the hypothesis that Finnish SWSV recolonized Finland with its host, the common shrew, from east after the last ice age 12,000–8000years ago, and then subsequently spread along emerging land bridges towards west or north with the migration and population expansion of its host.

Determination of genetic variations in the genus Dryomys Thomas, 1906 (Rodentia: Gliridae) distributed in Turkey using NADH dehydrogenase 1 (ND1) gene

Genetic diversity and phylogeny of Dryomys nitedula and Dryomys laniger from Turkey was described in the present study by using mitochondrial DNA NADH dehydrogenase 1 gene (ND1). Genetic variation in ND1 gene was determined by two model-based phylogenetic analyses and a network analysis revealed 27 haplotypes of D. nitedula constructing four main lineages (Thrace, Anatolia, North-eastern Anatolia and Şavşat) that have non-overlapping geographic distributions and no shared haplotypes, but on the other hand, three haplotypes were detected in four samples of D. laniger from Turkey. It was determined that nucleotide diversity was low but haplotype diversity was high in D. laniger, whereas, D. nitedula has both high level of haplotype and nucleotide diversity. Characterization of Thrace lineage of D. nitedula with low nucleotide diversity and determination of the total nucleotide diversity of Anatolian lineages (Anatolia + North-eastern Anatolia+Şavşat) to be approximately four times higher than that of Thrace lineage indicated that Anatolia may have served as a refuge for D. nitedula. Divergence times and high level of nucleotide differences between D. nitedula lineages showed that diversification of the lineages may have occurred before and during ice ages in Turkey, thought to be a refuge for post-glacial colonization and biodiversity resource of Europe. Additionally, estimated divergence times and calculated genetic distances yielded compatible results with the previous paleontological and genomic data for the diversification time of two species in the genus.

Molecular phylogeny and biogeography of the West‐Palaearctic Velia (Heteroptera: Gerromorpha: Veliidae)

AbstractWe investigated the systematics and biogeography of the West‐Palaearctic water cricket genus Velia Latreille based on a phylogenetic analysis of five molecular markers obtained from 79% of all known taxa of the subgenera Velia (s.s.) and Velia (Plesiovelia) Tamanini. The results revealed a sister‐group relationship between Velia (Plesiovelia) and the monotypic subgenus Velia (s.s.), and showed that the former is divided into three major clades. All taxa of Velia (Plesiovelia) were recovered as monophyletic, except for V. (P.) serbica Tamanini, which was paraphyletic with respect to V. (P.) mancinii mancinii Tamanini. Our results also indicate the existence of several unrecognized species. Molecular dating based on fossil data and COI rates indicates that the split between Velia (s.s.) and Velia (Plesiovelia) occurred between 40 and 22 Ma. An ancestral area reconstruction suggests that the latter originated in southeastern Europe, from where it radiated to the west and east, along the Neogene archipelagos of Europe and Asia Minor. Northwestern Africa served as the second most important diversification centre of the subgenus. The low genetic variability in the widespread V. (P.) caprai caprai Tamanini and V. (P.) saulii Tamanini implies a rapid postglacial colonization of Europe, whereas high diversity within the lineages of V. (P.) serbica indicates survival of Pleistocene glaciations in microrefugia throughout southeastern Europe. These results serve as a useful framework for future studies ranging from the systematics of the group to historical biogeography, ecology and biodiversity conservation.

Post-glacial colonization of Western Europe brown bears from a cryptic Atlantic refugium out of the Iberian Peninsula

The European brown bear (Ursus arctos) shows a particular phylogeography that has been used to illustrate the model for contraction-expansion dynamics related to glacial refugia in Southern European peninsulas. Recent studies, however, have nuanced the once generally accepted paradigm, indicating the existence of cryptic refugia for some species further north. In this paper we collected available data on chronology and mitochondrial haplotypes from Western European brown bears, adding new sequences from present day individuals from the Cantabrian (North Iberia) area, in order to reconstruct the dynamics of the species in the region. Both genetics and chronology show that the Iberian Pleistocene lineages were not the direct ancestors of the Holocene ones, the latter entering the Peninsula belatedly (around 10,000 years BP) with respect to other areas such as the British Isles. We therefore propose the existence of a cryptic refugium in continental Atlantic Europe, from where the bears would expand as the ice receded. The delay in the recolonization of the Iberian Peninsula could be due to the orographic characteristics of the Pyrenean-Cantabrian region and to the abundant presence of humans in the natural entrance to the Peninsula.

Drift, selection, or migration? Processes affecting genetic differentiation and variation along a latitudinal gradient in an amphibian

BackgroundPast events like fluctuations in population size and post-glacial colonization processes may influence the relative importance of genetic drift, migration and selection when determining the present day patterns of genetic variation. We disentangle how drift, selection and migration shape neutral and adaptive genetic variation in 12 moor frog populations along a 1700 km latitudinal gradient. We studied genetic differentiation and variation at a MHC exon II locus and a set of 18 microsatellites.ResultsUsing outlier analyses, we identified the MHC II exon 2 (corresponding to the β-2 domain) locus and one microsatellite locus (RCO8640) to be subject to diversifying selection, while five microsatellite loci showed signals of stabilizing selection among populations. STRUCTURE and DAPC analyses on the neutral microsatellites assigned populations to a northern and a southern cluster, reflecting two different post-glacial colonization routes found in previous studies. Genetic variation overall was lower in the northern cluster. The signature of selection on MHC exon II was weaker in the northern cluster, possibly as a consequence of smaller and more fragmented populations.ConclusionOur results show that historical demographic processes combined with selection and drift have led to a complex pattern of differentiation along the gradient where some loci are more divergent among populations than predicted from drift expectations due to diversifying selection, while other loci are more uniform among populations due to stabilizing selection. Importantly, both overall and MHC genetic variation are lower at northern latitudes. Due to lower evolutionary potential, the low genetic variation in northern populations may increase the risk of extinction when confronted with emerging pathogens and climate change.

Colonization dynamics of a clonal pioneer plant on a glacier foreland inferred from spatially explicit and size-structured matrix models

The regional distribution of a plant species is a result of the dynamics of extinctions and colonizations in suitable habitats, especially in strongly fragmented landscapes. Here, we studied the role of spatial dynamics of the long-lived, clonal pioneer plant Geum reptans occurring on glacier forelands in the European Alps. We used demographic data from several years and sites in the Swiss Alps in combination with dispersal data to parametrize a matrix model for G. reptans to simulate extinctions, colonizations and spatial spread of established populations on glacial forelands. We used different scenarios with varying germination rates, wind and animal dispersal capabilities, and modes of spatial spread (seed-only vs clonal spread), resulting in population growth rates (λ) ranging from 1.04 to 1.20. Our results suggest that due to the low germination rate (~1%) and the very limited wind dispersal distances (99.8% of seeds are dispersed < 5 m), G. reptans has a low probability of establishing new populations and a very low spatial spread by seed dispersal alone. In contrast to the low rate of establishment, the persistence of established populations is high and even populations of only a few individuals have an extinction probability of less than 25% within 100 years. This high persistency is partly due to clonal reproduction via aboveground stolons. Clonal reproduction increases the population size and contributes considerably to the spatial spread of established populations. Our simulation results together with the known pattern of molecular diversity of G. reptans indicate that the occurrence of populations of this species in the Alps is unlikely to be a result of recent colonizations by long-distance dispersal, but rather a result of post-glacial colonizations by large migrating populations that were fragmented when glaciers retreated. Additionally, our simulations suggest that the currently observed high rates of glacial retreat might be too fast for pioneer plants, such as G. reptans, to keep up with the retreating ice and therefore might threaten existing populations.

Genetic variation patterns of American chestnut populations at EST-SSRs

The objective of this study is to analyze patterns of genetic variation at genic expressed sequence tag – simple sequence repeats (EST-SSRs) and at chloroplast DNA markers in populations of American chestnut (Castanea dentata Borkh.) to assist in conservation and breeding efforts. Allelic diversity at EST-SSRs decreased significantly from southwest to northeast along the Appalachian range, suggesting repeated founder events during postglacial migration. Comparatively high allelic diversity in Ontario, northwest of the Appalachian range, suggested more recent long-distance dispersal. Clinal variation of allele frequencies along the Appalachian axis was also in accordance with postglacial colonization from one refugium southwest of the Appalachian range. We observed clustering of the northwestern population from Ontario with southwestern populations and sharing of a rare chloroplast haplotype among western populations across the whole latitudinal range. This pattern is consistent with a divergence of postglacial migration routes and higher levels of more recent potentially human-mediated gene exchange between populations west of the Appalachian range. Population pairs east and west of the Appalachian axis showed pronounced allele frequency differences over a small geographic range. These patterns of genetic variation should be considered when sampling reproductive material for conservation and breeding.

Genome-Wide Analysis of Colonization History and Concomitant Selection in Arabidopsis lyrata.

The high climatic variability in the past hundred thousand years has affected the demographic and adaptive processes in many species, especially in boreal and temperate regions undergoing glacial cycles. This has also influenced the patterns of genome-wide nucleotide variation, but the details of these effects are largely unknown. Here we study the patterns of genome-wide variation to infer colonization history and patterns of selection of the perennial herb species Arabidopsis lyrata, in locally adapted populations from different parts of its distribution range (Germany, UK, Norway, Sweden, and USA) representing different environmental conditions. Using site frequency spectra based demographic modeling, we found strong reduction in the effective population size of the species in general within the past 100,000 years, with more pronounced effects in the colonizing populations. We further found that the northwestern European A. lyrata populations (UK and Scandinavian) are more closely related to each other than with the Central European populations, and coalescent based population split modeling suggests that western European and Scandinavian populations became isolated relatively recently after the glacial retreat. We also highlighted loci showing evidence for local selection associated with the Scandinavian colonization. The results presented here give new insights into postglacial Scandinavian colonization history and its genome-wide effects.

The critical role of local refugia in postglacial colonization of Chinese pine: joint inferences from DNA analyses, pollen records, and species distribution modeling

The importance of long‐distance migration from low to high latitudes relative to local spread from northern refugia after the Last Glacial Maximum (LGM) remains a focus of debate for many temperate tree species. We assessed the dynamics of Chinese pine Pinus tabulaeformis, a widespread species endemic to northern China, since the LGM by integrating cytoplasmic DNA data, mapped pollen records and ecological niche modeling. Genetic variation among 544 individuals from 50 populations spanning the entire natural species range revealed eight genetic clusters with distinct geographic distribution, indicating glacial lineages likely originating from multiple local microrefugia. Palynological evidence suggested that the northernmost part of the natural distribution originated from local postglacial spread. Niche modeling indicated high probability of the species being present in the area of the Loess Plateau and coastal areas north of the Yangtze River during the LGM. The three lines of evidence jointly suggest that the species persisted through the last glaciation in the mountains surrounding the Loess Plateau of northern China and that the current distribution of the species originated primarily from the spread of local refugial populations, instead of long‐distance migration. These results cast doubt on the notion that Chinese pine migrated from areas south of the Yangtze River and underscore the importance of northern refugia.

Mitochondrial and nuclear intraspecific variation in the rusty blenny (Parablennius sanguinolentus, Blenniidae)

The genetic structure of Parablennius sanguinolentus from the northeastern Atlantic and Mediterranean was assessed using sequences from the mitochondrial control region (CR) and the first intron of the nuclear S7 ribosomal protein gene (S7). Our data show high genetic diversity for the central Mediterranean populations, contrasting with very low diversity in the Atlantic populations and in the westernmost Mediterranean population of Cabo de Gata. Both CR mismatch analysis and neutrality tests provide evidence of demographic and spatial expansion for the Atlantic and central Mediterranean populations. The significant correlation between genetic and geographic distances supported isolation-by-distance for the S7, but not for the CR, suggesting a complex scenario for the history of the rusty blenny in the Mediterranean Sea. The pattern of genetic structure displayed by P. sanguinolentus could be explained as the result of a post-glacial colonization of the Atlantic coast of Europe from the Mediterranean Sea.

Unique postglacial evolution of the hornbeam (Carpinus betulus L.) in the Carpathians and the Balkan Peninsula revealed by chloroplast DNA

The Balkan Peninsula is one of the largest and most important European glacial refugia. However, the evolutionary history and phylogeographic pattern of temperate tree species that survived in the Balkans glacial refugia and their contribution to the genetic structure of the current population in the Carpathian Mountains remains poorly understood.Using polymerase chain reaction - restriction fragment length polymorphism (PCR-RFLP), and extensive population sampling, we explored the phylogeographic pattern of Carpinus betulus in both the Balkan Peninsula and the Carpathian region. We aimed to determine the locations of potential glacial refugia, in order to delineate post-glacial colonization routes, and also to test if northern cryptic refugia had persisted during the Last Glacial Maximum (LGM).Our results provide strong support for the existence of multiple refugia similar to the ‘refugia-within-refugia’ scenario, which would suggest that Carpinus betulus has experienced a complex evolutionary history.In agreement with pollen data, our findings corroborate with previous hypotheses suggesting that hornbeam has a distinct postglacial evolution in the southeast of Europe (Carpathians and Balkan Peninsula) compared with that in Western Europe.Three postglacial re-colonization routes, from three distinct effective glacial refugia: (1) the Dinaric Alps; (2) the Pirin and Rhodope Mountains and (3) the Strandzha Mountains, were detected within the Balkan Peninsula. The pattern of cpDNA haplotypes distribution across the Ukrainian Carpathians revealed a “suture zone”, which is a consequence of contact due to postglacial re-colonization between hornbeam populations originating from all three effective glacial refugia.The peculiar haplotype geographical structure found in C. betulus and the identified multiple glacial refugia in the Balkans may have direct consequences in the management and conservation of hornbeam forest genetic resources.

Postglacial dispersal patterns and mitochondrial genetic structure of the Pyrenean desman (Galemys pyrenaicus) in the northwestern region of the Iberian Peninsula.

The genetic structure of small semiaquatic animals may be influenced by dispersal across both rivers and land. The relative importance of these two modes of dispersal may vary across different species and with ecological conditions and evolutionary periods. The Pyrenean desman (Galemys pyrenaicus) is an endemic mammal of the Iberian Peninsula with a strong phylogeographic structure and semiaquatic habits, thus making it an ideal model to study the effects of river and overland dispersal on its genetic structure. Thanks to different types of noninvasive samples, we obtained an extensive sampling of the Pyrenean desman from the northwestern region of the Iberian Peninsula and sequenced two mitochondrial DNA fragments. We then analyzed, using an isolation‐by‐distance approach, the correlation between phylogenetic distances and geographical distances measured along both river networks and land to infer the relative importance of river and overland dispersal. We found that the correlations in the whole area and in a large basin were consistent with an effect of overland dispersal, which may be due to the postglacial colonization of new territories using terrestrial corridors and, possibly, a more extensive fluvial network that may have been present during the Holocene. However, in a small basin, likely to be less influenced by the impact of ancient postglacial dispersal, the correlations suggested significant overall effects of both overland and river dispersal, as expected for a semiaquatic mammal. Therefore, different scales and geographical regions reflect different aspects of the evolutionary history and ecology of this semiaquatic species using this isolation‐by‐distance method. The results we obtained may have crucial implications for the conservation of the Pyrenean desman because they reinforce the importance of interbasin dispersal for this species in the studied area and the need to protect the whole riverine ecosystem, including rivers, upland streams and terrestrial corridors between basins.

Asymmetry matters: A genomic assessment of directional biases in gene flow between hybridizing spruces.

Assessing directional bias in interspecific gene flow might be important in determining the evolutionary trajectory of closely related species pairs. Using a set of 300 single nucleotide polymorphisms (SNPs) having variable propensity to cross species boundary, we evaluated the genomic extent and direction of interspecific gene flow in a progenitor‐derivative spruce species pair (black spruce and red spruce). A higher rate of gene flow was found from black spruce toward red spruce purebreds than vice versa. This asymmetry could reflect the historical gene flow between the two taxa at the time of species inception and during postglacial colonization. A clear asymmetry in introgression was depicted by a greater gene flow between red spruce and hybrids than between black spruce and hybrids. While backcrossing toward red spruce was invariably high across the genome, the actual species boundary is between hybrids and black spruce where gene flow is impeded at those genomic regions impermeable to introgression. Associations between hybrid index and climatic variables (total annual precipitation and mean annual temperature) were tested, as these might indicate a role for exogenous selection in maintaining the species boundary. While an apparent association was found between the hybrid index and precipitation, it collapsed when considered in light of the directional bias in interspecific gene flow. Hence, considering asymmetrical patterns of introgression allowed us to falsify an apparent role for exogenous selection. Although this was not formerly tested here, we suggest that this pattern could result from asymmetrical endogenous selection, a contention that deserves further investigations.