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.     

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.     

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.     

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.     

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.     

Local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones

Few marine hybrid zones have been studied extensively, the major exception being the hybrid zone between the mussels Mytilus edulis and Mytilus galloprovincialis in southwestern Europe. Here, we focus on two less studied hybrid zones that also involve Mytilus spp.; Mytilus edulis and Mytilus trossulus are sympatric and hybridize on both western and eastern coasts of the Atlantic Ocean. We review the dynamics of hybridization in these two hybrid zones and evaluate the role of local adaptation for maintaining species boundaries. In Scandinavia, hybridization and gene introgression is so extensive that no individuals with pure M. trossulus genotypes have been found. However, M. trossulus alleles are maintained at high frequencies in the extremely low salinity Baltic Sea for some allozyme genes. A synthesis of reciprocal transplantation experiments between different salinity regimes shows that unlinked Gpi and Pgm alleles change frequency following transplantation, such that post-transplantation allelic composition resembles native populations found in the same salinity. These experiments provide strong evidence for salinity adaptation at Gpi and Pgm (or genes linked to them). In the Canadian Maritimes, pure M. edulis and M. trossulus individuals are abundant, and limited data suggest that M. edulis predominates in low salinity and sheltered conditions, whereas M. trossulus are more abundant on the wave-exposed open coasts. We suggest that these conflicting patterns of species segregation are, in part, caused by local adaptation of Scandinavian M. trossulus to the extremely low salinity Baltic Sea environment.     

Sewall Wright’s adaptive landscapes: 1932 vs. 1988

Sewall Wright introduced the metaphor of evolution on “adaptive landscapes” in a pair of papers published in 1931 and 1932. The metaphor has been one of the most influential in modern evolutionary biology, although recent theoretical advancements show that it is deeply flawed and may have actually created research questions that are not, in fact, fecund. In this paper I examine in detail what Wright actually said in the 1932 paper, as well as what he thought of the matter at the very end of his career, in 1988. While the metaphor is flawed, some of the problems which Wright was attempting to address are still with us today, and are in the process of being reformulated as part of a forthcoming Extended Evolutionary Synthesis.

Phenotype and animal domestication: A study of dental variation between domestic,wild, captive,hybrid and insular Sus scrofa

Background

Identifying the phenotypic responses to domestication remains a long-standing and important question for researchers studying its early history. The great diversity in domestic animals and plants that exists today bears testament to the profound changes that domestication has induced in their ancestral wild forms over the last millennia. Domestication is a complex evolutionary process in which wild organisms are moved to new anthropogenic environments. Although modern genetics are significantly improving our understanding of domestication and breed formation, little is still known about the associated morphological changes linked to the process itself. In order to explore phenotypic variation induced by different levels of human control, we analysed the diversity of dental size, shape and allometry in modern free-living and captive wild, wild x domestic hybrid, domestic and insular Sus scrofa populations.

Results

We show that domestication has created completely new dental phenotypes not found in wild boar (although the amount of variation amongst domestic pigs does not exceed that found in the wild). Wild boar tooth shape also appears to be biogeographically structured, likely the result of post-glacial recolonisation history. Furthermore, distinct dental phenotypes were also observed among domestic breeds, probably the result of differing types and intensity of past and present husbandry practices. Captivity also appears to impact tooth shape. Wild x domestic hybrids possess second molars that are strictly intermediate in shape between wild boar and domestic pigs (third molars, however, showing greater shape similarity with wild boar) while their size is more similar to domestic pigs. The dental phenotypes of insular Sus scrofa populations found on Corsica and Sardinia today (originally introduced by Neolithic settlers to the islands) can be explained either by feralization of the original introduced domestic swine or that the founding population maintained a wild boar phenotype through time.

Conclusions

Domestication has driven significant phenotypic diversification in Sus scrofa. Captivity (environmental control), hybridization (genome admixture), and introduction to islands all correspond to differing levels of human control and may be considered different stages of the domestication process. The relatively well-known genetic evolutionary history of pigs shows a similar complexity at the phenotypic level.

Electronic supplementary material

The online version of this article (doi:10.1186/s12862-014-0269-x) contains supplementary material, which is available to authorized users.     

Admixture mapping of quantitative traits in Populus hybrid zones: power and limitations

Uncovering the genetic architecture of species differences is of central importance forunderstanding the origin and maintenance of biological diversity. Admixture mapping can beused to identify the number and effect sizes of genes that contribute to the divergence ofecologically important traits, even in taxa that are not amenable to laboratory crossesbecause of their long generation time or other limitations. Here, we apply admixturemapping to naturally occurring hybrids between two ecologically divergent Populusspecies. We map quantitative trait loci for eight leaf morphological traits using 77mapped microsatellite markers from all 19 chromosomes of Populus. We applymultivariate linear regression analysis allowing the modeling of additive and non-additivegene action and identify several candidate genomic regions associated with leaf morphologyusing an information-theoretic approach. We perform simulation studies to assess the powerand limitations of admixture mapping of quantitative traits in natural hybrid populationsfor a variety of genetic architectures and modes of gene action. Our results indicate that(1) admixture mapping has considerable power to identify the genetic architecture ofspecies differences if sample sizes and marker densities are sufficiently high, (2)modeling of non-additive gene action can help to elucidate the discrepancy betweengenotype and phenotype sometimes seen in interspecific hybrids, and (3) the geneticarchitecture of leaf morphological traits in the studied Populus species involvescomplementary and overdominant gene action, providing the basis for rapid adaptation ofthese ecologically important forest trees.     

The evolutionary history of Drosophila buzzatti. XXVI. Macrogeographic patterns of inversion polymorphism in New World populations

Inversion polymorphisms in the second and fourth chromosomes of the cactophilic Drosophila buzzatti in the native distribution range of the species are described. Over 5,000 flies from 26 localities were scored revealing interesting geographic structuring of arrangement frequencies. Multiple regression and partial correlation approaches showed that the frequencies of second and fourth chromosome arrangements vary clinically along latitudinal and altitudinal gradients and to a lesser extent with longitude. Although many non selective explanations can account for this pattern, its resemblance to the clinal pattern described in recently established Australian populations of Drosophila buzzatii, strongly suggests a selective explanation. Additionally, the correlated variation observed between the frequencies of arrangements 2St on the second chromosome and 4St on the fourth suggests a pattern of interchromosomal association, which, when considering the vast area surveyed, might be explained as the result of epistatic interactions. The analysis of population structure revealed a significant regional pattern, concordant with previously described phytogeographic regions. F-statistics showed that the patterns of variation were different not only between the second and fourth chromosomes, but also between second chromosome arrangements, suggesting that selective differentiation might have contributed to population structure. Since D. buzzatii breeds and feeds on the decaying tissues of diverse cactus species present in different phytogeographic regions, it is difficult to distinguish the underlying causes of the geographic patterns observed. However, inversion heterozygosity is not correlated with the diversity of potential cactus hosts. The evidence presented suggests that differential selection may be the main cause for the population structure. It is also possible to conclude that the inversion polymorphism of D. buzzatti is flexible rather than rigid.     

Clustering of contact zones, hybrid zones, and phylogeographic breaks in North America

A recent test for the existence of suture zones in North America, based on hybrid zones studied since 1970, found support for only two of the 13 suture zones identified by Remington in 1968 (Swenson and Howard 2004). One limitation of that recent study was the relatively small number of hybrid zones available for mapping. In this study, we search for evidence of clustering of contact zones between closely related taxa using data not only from hybrid zones but from species range maps of trees, birds, and mammals and from the position of phylogeographic breaks within species. Digital geographic range maps and a geographic information system approach allowed for accurate and rapid mapping of distributional data. Areas of contact between closely related species and phylogeographic breaks within species clustered into areas characterized by common physiographic features or predicted by previously hypothesized glacial refugia. The results underscore the general importance of geographic barriers to dispersal (mountain chains) and climate change (periods of cooling alternating with periods of warming, which lead to the contraction and expansion of species ranges) in species evolution.     

Detecting clinal and balanced selection using spatial autocorrelation analysis under kin-structured migration

Recently spatial autocorrelation has been employed to infer microevolutionary processes from patterns of genetic variation. In theory, different processes should show characteristic signature correlograms; e. g., clinal selection should produce correlograms decreasing from positive to negative autocorrelation, whereas uniform balanced selection should lead to no spatial autocorrelation. The ability of a statistical method such as spatial autocorrelation analysis to distinguish between these selective regimes or even to detect departures from neutrality is dependent on the strength of the evolutionary force and the population structure. Weak selection or migration will not be apparent against the expected background of stochastic noise. Moreover, the population structure may generate sufficient stochastic variation such that even strong evolutionary forces may fail to be detected. This study uses computer simulation to examine the effects of kin-structured migration and three different selective regimes on the shape of spatial correlograms to assess the ability of this technique to detect different microevolutionary processes. Genetic variation among 8 loci is simulated in a linear set of 25 artificial populations. Kin-structured stepping-stone migration among adjacent populations is modeled; directional, balanced, and clinal selection, as well as neutral loci are considered. These experiments show that strong selection produces correlograms of the predicted shape. However, with an anthropologically reasonable population structure, considerable stochastic variation among correlograms for different alleles may still exist. This suggests the need for caution in inferring genetic process from spatial patterns. © 1994 Wiley-Liss, Inc.