Variable patterns of introgression in two sculpin hybrid zones suggest that genomic isolation differs among populations

Theory predicts that reproductive isolation may be due to intrinsic genetic incompatibilities or extrinsic ecological factors. Therefore, an understanding of the genetic basis of isolation may require analyses of evolutionary processes in situ to include environmental factors. Here we study genetic isolation between populations of sculpins ( Cottus ) at 168 microsatellites. Genomic clines were fit using 480 individuals sampled across independent natural hybrid zones that have formed between one invading species and two separate populations of a resident species. Our analysis tests for deviations from neutral patterns of introgression at individual loci based on expectations given genome-wide admixture. Roughly 51% of the loci analysed displayed significant deviations. An overall deficit of interspecific heterozygotes in 26% and 21% of the loci suggests that widespread underdominance drives genomic isolation. At the same time, selection promotes introgression of almost 30% of the markers, which implies that hybridization may increase the fitness of admixed individuals. Cases of overdominance or epistatic interactions were relatively rare. Despite the similarity of the two hybrid zones in their overall genomic composition, patterns observed at individual loci show little correlation between zones and many fit different genotypic models of fitness. At this point, it remains difficult to determine whether these results are due to differences in external selection pressures or cryptic genetic differentiation of distinct parental populations. In the future, data from mapped genetic markers and on variation of ecological factors will provide additional insights into the contribution of these factors to variation in the evolutionary consequences of hybridization.     

Demographic history shapes genomic ancestry in hybrid zones

Demographic factors such as migration rate and population size can impede or facilitate speciation. In hybrid zones, reproductive boundaries between species are tested and demography mediates the opportunity for admixture between lineages that are partially isolated. Genomic ancestry is a powerful tool for revealing the history of admixed populations, but models and methods based on local ancestry are rarely applied to structured hybrid zones. To understand the effects of demography on ancestry in hybrids zones, we performed individual‐based simulations under a stepping‐stone model, treating migration rate, deme size, and hybrid zone age as parameters. We find that the number of ancestry junctions (the transition points between genomic regions with different ancestries) and heterogenicity (the genomic proportion heterozygous for ancestry) are often closely connected to demographic history. Reducing deme size reduces junction number and heterogenicity. Elevating migration rate increases heterogenicity, but migration affects junction number in more complex ways. We highlight the junction frequency spectrum as a novel and informative summary of ancestry that responds to demographic history. A substantial proportion of junctions are expected to fix when migration is limited or deme size is small, changing the shape of the spectrum. Our findings suggest that genomic patterns of ancestry could be used to infer demographic history in hybrid zones.     

Genomic variation across two barn swallow hybrid zones reveals traits associated with divergence in sympatry and allopatry

Hybrid zones are geographic regions where isolating barriers between divergent populations are challenged by admixture. Identifying factors that facilitate or inhibit hybridization in sympatry can illuminate the processes that maintain those reproductive barriers. We analysed patterns of hybridization and phenotypic variation across two newly discovered hybrid zones between three subspecies of barn swallow (Hirundo rustica). These subspecies differ in ventral coloration and wing length, traits that are targets of sexual and natural selection, respectively, and are associated with genome‐wide differentiation in allopatry. We tested the hypothesis that the degree of divergence in these traits is associated with the extent of hybridization in secondary contact. We applied measures of population structure based on >23,000 SNPs to confirm that named subspecies correspond to distinct genomic clusters, and assessed coincidence between geographic clines for ancestry and phenotype. Although gene flow was ongoing across both hybrid zones and pairwise F_ST between subspecies was extremely low, we found striking differences in the extent of hybridization. In the more phenotypically differentiated subspecies pair, clines for ancestry, wing length and ventral coloration were steep and coincident, suggestive of strong isolation and, potentially, selection associated with phenotype. In the less phenotypically differentiated pair, gene flow and phenotypic variation occurred over a wide geographic span, indicative of weaker isolation. Traits associated with genome‐wide differentiation in allopatry may thus also contribute to isolation in sympatry. We discuss potentially important additional roles for evolutionary history and ecology in shaping variation in the extent hybridization between closely related pairs of subspecies.     

Mammalian hybrid zones: a review

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Hybridization and introgression in two ecologically dissimilar Fundulus hybrid zones

Hybridization and introgression appear more common in rapidly evolving groups, suggesting an important role in the evolutionary process. Detailed studies of how extrinsic or intrinsic forces regulate hybridization and introgression have the potential for broadening our understanding of mechanisms generating diversity. Species in the Fundulus notatus species complex have broad overlapping ranges and occur in replicated hybrid zones along predictable stream gradients. Typical hybrid zone structure has Fundulus olivaceus in headwaters, F. notatus downstream, and hybrid zones near confluences or abrupt shifts in habitat. Rarely, the typical upstream‐downstream orientation is reversed raising questions as to how hybrid zones are formed and maintained. We used next‐generation sequencing data to study hybridization and introgression in hybrid zones in neighboring drainages that differ in orientation (typical and reversed). We predicted extrinsic forces linked to stream gradients would result in noticeable differences between the two. Contrary to predictions, the data indicate the hybrid zones are remarkably similar. We used individual‐based simulations to explore the potential role of intrinsic and extrinsic forces in generating and maintaining typical and reversed hybrid zones. Simulation results were consistent with reversed hybrid zones being formed from stochastic processes combined with strong intrinsic forces and weak extrinsic forces.     

Estimating the location and shape of hybrid zones

We propose a new model to make use of georeferenced genetic data for inferring the location and shape of a hybrid zone. The model output includes the posterior distribution of a parameter that quantifies the width of the hybrid zone. The model proposed is implemented in the GUI and command-line versions of the Geneland program versions ≥ 3.3.0. Information about the program can be found on http://www2.imm.dtu.dk/gigu/Geneland/.     

Altitudinal gradients,plant hybrid zones and evolutionary novelty

Altitudinal gradients are characterized by steep changes of the physical and biotic environment that present challenges to plant adaptation throughout large parts of the world. Hybrid zones may form where related species inhabit different neighbouring altitudes and can facilitate interspecific gene flow and potentially the breakdown of species barriers. Studies of such hybrid zones can reveal much about the genetic basis of adaptation to environmental differences stemming from changes in altitude and the maintenance of species divergence in the face of gene flow. Furthermore, owing to recombination and transgressive effects, such hybrid zones can be sources of evolutionary novelty. We document plant hybrid zones associated with altitudinal gradients and emphasize similarities and differences in their structure. We then focus on recent studies of a hybrid zone between two Senecio species that occur at high and low altitude on Mount Etna, Sicily, showing how adaptation to local environments and intrinsic selection against hybrids act to maintain it. Finally, we consider the potential of altitudinal hybrid zones for generating evolutionary novelty through adaptive introgression and hybrid speciation. Examples of homoploid hybrid species of Senecio and Pinus that originated from altitudinal hybrid zones are discussed.     

Variation in Drosophila melanogaster central metabolic genes appears driven by natural selection both within and between populations

In this report, we examine the hypothesis that the drivers of latitudinal selection observed in the eastern US Drosophila melanogaster populations are reiterated within seasons in a temperate orchard population in Pennsylvania, USA. Specifically, we ask whether alleles that are apparently favoured in northern populations are also favoured early in the spring, and decrease in frequency from the spring to autumn with the population expansion. We use SNP data collected for 46 metabolic genes and 128 SNPs representing the central metabolic pathway and examine for the aggregate SNP allele frequencies whether the association of allele change with latitude and that with increasing days of spring–autumn season are reversed. Testing by random permutation, we observe a highly significant negative correlation between these associations that is consistent with this expectation. This correlation is stronger when we confine our analysis to only those alleles that show significant latitudinal changes. This pattern is not caused by association with chromosomal inversions. When data are resampled using SNPs for amino acid change the relationship is not significant but is supported when SNPs associated with cis-expression are only considered. Our results suggest that climate factors driving latitudinal molecular variation in a metabolic pathway are related to those operating on a seasonal level within populations.     

A comparison of five hybrid zones of the weta Hemideina thoracica (Orthoptera: Anostostomatidae): degree of cytogenetic differentiation fails to predict zone width

Abstract Tension zones are maintained by the interaction between selection against hybrids and dispersal of individuals. Investigating multiple hybrid zones within a single species provides the opportunity to examine differences in zone structure on a background of differences in extrinsic factors (e.g., age of the zone, ecology) or intrinsic factors (e.g., chromosomes). The New Zealand tree weta Hemideina thoracica comprises at least eight distinct chromosomal races with diploid numbers ranging from 2n = 11 (XO) to 2n = 23 (XO). Five independent hybrid zones were located that involve races differing from one another by a variety of chromosomal rearrangements. The predicted negative correlation between extent of karyotypic differentiation (measured in terms of both percent of genome and number of rearrangements) and zone width was not found. Conversely, the widest zones were those characterized by two chromosome rearrangements involving up to 35% of the genome. The narrowest zone occurred where the two races differ by a single chromosome rearrangement involving approximately 2% of the genome. The five estimates of chromosomal cline width ranged from 0.5 km to 47 km. A comparative investigation of cline width for both chromosomal and mitochondrial markers revealed a complex pattern of zone characteristics. Three of the five zones in this study showed cline concordance for the nuclear and cytoplasmic markers, and at two of the zones the clines were also coincident. Zones with the widest chromosomal clines had the widest mitochondrial DNA clines. It appears that, even within a single species, the extent of karyotypic differentiation between pairs of races is not a good predictor of the level of disadvantage suffered by hybrids.     

Genetic mapping in hybrid zones

Recent advances in genetic mapping methodologies make it feasible to localize quantitative trait loci (QTL) that contribute to adaptation and speciation. However, it has not been possible to employ these methods in many wild species because of difficulties associated with creating and propagating recombinant populations of sufficient size for QTL mapping. Natural hybrid zones contain recombinant individuals resulting from many generations of hybridization and thus offer a potential solution to these problems. For studies of speciation, hybrid zones offer the possibility of mapping QTL simultaneously with assessments of their effects on assortative mating, hybrid fitness, and interspecific gene flow. Here, we explore the problems and prospects associated with genetic map building and QTL analyses in natural hybrid zones by analyzing correlations among markers of known genomic location in four hybrid zones between the wild sunflower species Helianthus annuus and Helianthus petiolaris. Results indicate that mapping in hybrid zones presents many challenges. These include overlap in the strength of marker correlations between linked and unlinked markers, unevenness in marker frequencies along linkages, and heterogeneity in the relationship between marker distances and correlations. All make it difficult to accurately group and order markers or to estimate the distances between them. These problems can be ameliorated by sampling strategies that maximize the difference in linkage disequilibria between linked and unlinked markers and that minimize differences in frequencies among markers or QTL. In addition, studies that employ a previously determined molecular marker map for gene localization have a greater likelihood of success than those that rely on the hybrid zone data for both map construction and QTL analyses.     

The transient properties of balancing selection in large finite populations

The transient properties of balancing selection in large, but finite, populations are described by means of an asymptotic analysis. Heterotic selection is shown to retard the rate of loss of genetic variation while random environment selection is shown to retard the rate of loss of variation when the initial variant is a rare mutant. Otherwise random environment selection can speed up the loss of variation for certain parametric cases. The asymptotic analysis leads to a particularly simple conceptualization of the selection process which allows the computation of asymptotic forms of the dominant eigenvalue of the process.     

Genetic diversity and natural selection in wild fruit flies revealed by whole-genome resequencing

We characterized 26 wild fruit flies comparative population genomics from six different altitude and latitude locations by whole genome resequencing. Genetic diversity was relatively higher in Ganzi and Chongqing populations. We also found 13 genes showing selection signature between different altitude flies and variants related to hypoxia and temperature stimulus, were preferentially selected during the flies evolution. One of the most striking selective sweeps found in all high altitude flies occurred in the region harboring Hsp70Aa and Hsp70Ab on chromosome 3R. Interestingly, these two genes are involved in GO terms including response to hypoxia, unfolded protein, temperature stimulus, heat, oxygen levels. Mutation in HPH gene, a candidate gene in the hypoxia inducible factor pathway, might contributes to hypoxic high-altitude adaptation. Intriguingly, some of the selected genes, primarily utilized in humans, were involved in the response to hypoxia, which could imply a conserved molecular mechanisms underlying high-altitude adaptation between insects and humans.     

Counterselection on sex chromosomes in the Mus musculus European hybrid zone

The extent to which alleles can disperse across a hybrid zone depends on the selection they are subjected to in the hybrid genetic background or, for those that are selectively neutral, on their ability to escape from the unfavourable environment by recombination. Three markers spanning a 45 cM segment in the center of the X chromosome were used to investigate the degree to which selection against X chromosome linked genes helps to maintain the barrier to gene flow in the hybrid zone between Mus musculus domesticus and M. m. musculus in Denmark. The introgression of all the sex chromosome specific markers was more limited than that of the autosomal enzymes (Idh1, Amy, Gpd1, Pgm1, Es1, Es2, Mpi, Np1, Es10, Sod1) and the mitochondrial DNA. The cline for DXPas2, which is in the center of the X chromosome, is extremely steep and shows that certain genes located in this region are strongly selected against in the hybrid background. The clines of the other two X-linked markers, Hprt and DXPas1, and of the Y chromosome are not as abrupt and all three have similar asymmetric introgression patterns. Although the musculus variants appear to behave in much the same way as those of the autosomal genes, the domesticus variants do not introgress. The results show that X-linked and to a lesser extent Y-linked genes are more strongly selected against in the hybrid genome than the mitochondrial genome or the different autosomal loci. This suggests that co-adapted gene systems involving the sex chromosomes may play an important role in the hybrid breakdown between the two subspecies.     

Molecular and morphological analysis of secondary contact zones of Cottus gobio in Fennoscandia: geographical discordance of character transitions

Northern Europe was postglacially colonized from different directions by distinct phylogeographical lineages of the bullhead Cottus gobio L. (Pisces: Scorpaeniformes). These lineages have then come into contact in coastal habitats of the currently brackish Baltic Sea and in the freshwaters north of it. We studied the patterns of intergradation in the contact zones in four morphometric and six molecular characters. In the north, intergradation between the western (W) and eastern (E) bullhead lineages is found both among rivers (west‐to‐east) and along individual rivers (south‐to‐north). The locations of the transition zones probably relate to the timing of the initial contact, subsequent Baltic shoreline displacement (i.e. emergence of the lower river reaches), and dispersal barriers caused by variations of coastal salinity. The transitions (clines) in different characters are, however, not geographically coincident. Mitochondrial DNA clines are generally found upstream and to the east of the other transitions, and GPI‐1 allozyme clines are mostly shifted downstream in the rivers, and west of the other transitions on the broader scale of the Baltic Sea. The location of the mtDNA clines may best reflect the initial contact between lineages, and the displacement of the other clines could result from dispersal being overall asymmetric (predominantly downstream) and sex‐biased (stronger in males). Alternatively, the non‐coincidence might reflect selection against deleterious cytonuclear character combinations. No clear evidence of reproductive incompatibility between the lineages was seen in local population structures; no remaining genetic correlations were observed locally among traits. In another transition area, a coastal transect in southern Finland, clinal patterns similar to those in the northern contact zone were recorded, but the population compositions could not be explained by simple in situ mixing of any of the putatively pure, invading refugial lineages. Probably, the bullhead stocks that initially came into contact in this southern study area already represented mixtures of the invading lineages. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 81 , 535–552.     

Environmental factors, microgeographic patterns of endemism and hybrid zones in Monobella grassei (Insecta: Collembola: Neanuridae)

A complex pattern of narrow parapatric distributions with hybrid zones is described among subspecies of the Collembola species Monobella grassei in the eastern Pyrenees. Though hybrid zones are usually narrow, they vary from simple contact zones without recorded hybrids to relatively wide hybrid swarms, suggesting that large differences exist locally in the level of genetic divergence between subspecies. The course and structure of contact zones are analysed on morphological grounds, in relation to environmental (rainfall, vegetation, substrate) and topographical (altitude, hydrography) parameters. The results show that, unlike most cases documented so far, the courses of the contact zones in M. grassei are not connected to major ecological boundaries nor to ecological ecotones, on either the regional or the habitat scale. It is suggested that this is due to the great ecological similarity between the different parapatric subspecies of M. grassei , and their broad ecological requirements. There is no conclusive evidence that the distribution observed is linked to recent palaeoclimatic events such as glaciation. Endogenous selection could therefore be prevalent in this model to explain parapatry and the hybrid zone pattern.     

Geographical distribution and phenotypic differentiation in populations of Dactylis glomerata L. in Japan

Although the perennial grass Dactylis glomerata L. has established dominant populations in Japan since its introduction in the 1870s, there have been marked reductions in its abundance in southern and northeastern regions. In order to examine the effects of climatic factors on distribution and differentiation of the naturalized populations of D. glomerata, abundance of 26 populations over a distance of 1500 km along a latitudinal gradient was recorded at each site, and life-history traits of each population were measured in a common garden. It was found that the reduction in abundance was related to the mean summer temperature in southern regions and to the lowest temperature before snow cover in northeastern regions. Recent climatic records in Japan show an increase in the mean summer temperature but no apparent changes in the lowest temperature before snow cover. These data suggest that, assuming the recent trend in climatic changes continues, the population abundance will decrease in southern regions and will change little in the northeastern regions. Germination speed, leaf width and reproductive allocations showed clinal variation over a geographical range, and the southern populations had more rapid germination, narrower leaves and lower reproductive allocation than did the northern populations. On the other hand, seed size and germination date showed margin-center differentiation. Marginal populations in both distributional borders had smaller seeds and lower germination rates than did the central populations. This revised version was published online in June 2006 with corrections to the Cover Date.     

Three-trophic-level interactions in cattail hybrid zones

Plant-herbivore and herbivore-parasitoid wasp interactions were examined in three hybrid zones of the cattails Typha latifolia and T. angustifolia in south-eastern Michigan over a 2-year period. Patterns of resource use by two lepidopteran species of seed-eating herbivores were studied and herbivore densities sustained by the hybrid cattail T. x glauca and its parental species were determined. Densities of the commoner seed-eating lepidopteran, Lymnaecia phragmitella, were found to be highest in seed heads of both parental species and lowest in hybrid seed heads in zones of hybridization, thus supporting the hybrid resistance hypothesis of Fritz et al. (1994). Densities of the second herbivore, Dicymolomia julianalis, on the hybrid were lower than on the parental T. latifolia, but did not differ from the mean of the combined herbivore densities of the two parental species. D. julianalis in cattails appears to fit the additive hypothesis (Fritz et al. 1994). Parasitism of L. phragmitella by four species of parasitoid wasp, Itoplectis conquisitor (Ichneumonidae), Scambus hispae (Ichneumonidae), Macrocentrus delicatus (Braconidae), and Temelucha gracilipes (Ichneumonidae), was studied to determine if rates of parasitization by these natural enemics on the different cattails were similar to the patterns of plant exploitation exhibited by their hosts. Parasitism rates of L. phragmitella were significantly higher in larvae reared on hybrid cattails. This study reveals two different patterns of hybrid utilization by two very similar herbivores. Opposite patterns of plant utilization were found for the parasitoids compared with their host (L. phragmitella) in cattail hybrid zones.     

High gene flow despite opposite chirality in hybrid zones between enantiomorphic door snails

We studied differentiation and geneflow patterns between enantiomorphic door‐snail species in two hybrid zones in the Bucegi Mountains (Romania) to investigate the effects of intrinsic barriers (complications in copulation) and extrinsic selection by environmental factors. A mitochondrial gene tree confirmed the historical separation of the examined populations into the dextral Alopia livida and the sinistral Alopia straminicollis in accordance with the morphological classification, but also indicated gene flow between the species. By contrast, a network based on amplified fragment length polymorphisms (AFLP) markers revealed local groups of populations as units independent of their species affiliation. Admixture analyses based on AFLP data showed that the genomes of most individuals in the hybrid zones are composed of parts of the genomes of both parental taxa. The introgression patterns of a notable fraction of the examined markers deviated from neutral introgression. However, the patterns of most non‐neutral markers were not concordant between the two hybrid zones. There was also no concordance between non‐neutral markers in the two genomic clines and markers that were correlated with environmental variables or markers that were correlated with the proportion of dextral individuals in the populations. Neither extrinsic selection by environmental factors nor intrinsic barriers resulting from positive frequency‐dependent selection of the prevailing coiling direction were sufficient to maintain the distinctness of A. straminicollis and A. livida. Despite being historically separated units, we conclude that these taxa now merge where they come into contact.     

Migratory divides coincide with reproductive barriers across replicated avian hybrid zones above the Tibetan Plateau

Migratory divides are proposed to be catalysts for speciation across a diversity of taxa. However, it is difficult to test the relative contributions of migratory behaviour vs. other divergent traits to reproductive isolation. Comparing hybrid zones with and without migratory divides offers a rare opportunity to directly examine the contribution of divergent migratory behaviour to reproductive barriers. We show that across replicate sampling transects of two pairs of barn swallow (Hirundo rustica) subspecies, strong reproductive isolation coincided with a migratory divide spanning 20 degrees of latitude. A third subspecies pair exhibited no evidence for a migratory divide and hybridised extensively. Within migratory divides, overwintering habitats were associated with assortative mating, implicating a central contribution of divergent migratory behaviour to reproductive barriers. The remarkable geographic coincidence between migratory divides and genetic breaks supports a long‐standing hypothesis that the Tibetan Plateau is a substantial barrier contributing to the diversity of Siberian avifauna.