REINFORCING SELECTION IS EFFECTIVE UNDER A RELATIVELY BROAD SET OF CONDITIONS IN A MOSAIC HYBRID ZONE

Many hybrid zones have a mosaic structure, yet we know of no theoretical work that examines the impact of mosaicism on the outcome of evolution. We developed a computer simulation model designed to test whether the outcome of reinforcing selection differs in a mosaic and a clinal hybrid zone. Our model was a one-dimensional stepping-stone model. The mosaic and clinal hybrid zones that we modeled were, respectively, a mosaic maintained by differential fitness of the interacting taxa in patchy habitats and a tension zone. We modeled changes in gene frequency at two biallelic loci, A and B. Hybrids at the A locus were selected against. An allele at the B locus caused assortative mating at the A locus, which promoted reinforcement; there was a selective cost to this allele. In a mosaic hybrid zone, spatial variation in the fitness of A-locus homozygotes in different patches caused gene and genotype frequencies at the A and B loci to differ greatly from those in a tension zone. Compared to a tension zone, a mosaic hybrid zone had a broader region in which hybrids could be formed and, thus, a broader region in which the assortative-mating allele provided a net selective advantage (via decreased production of the less fit A-locus hybrids). This caused the assortative-mating allele to be favored under a broader set of conditions in a mosaic hybrid zone than in a tension zone. In mosaic and tension hybrid zones, both low and high levels of migration could prevent the establishment of the allele that promoted reinforcement, but the allele could establish under a wider range of migration rates in a mosaic than in a tension zone. In a tension zone, both low and high levels of selection against A-locus hybrids could prevent the establishment of the assortative-mating allele. In a mosaic hybrid zone, the assortative-mating allele established under lower levels of selection against hybrids than in a tension zone, and high levels of selection did not impede the establishment of this allele. Overall, our work illustrates how the structure of a hybrid zone can alter the outcome of an important evolutionary process, in this case, reinforcement.     

NATURAL SELECTION ON QUANTITATIVE TRAITS IN THE BOMBINA HYBRID ZONE

Observations on the means, variances, and covariances of quantitative traits across hybrid zones can give information similar to that from Mendelian markers. In addition, they can identify particular traits through which the cline is maintained. We describe a survey of six traits across the hybrid zone between Bombina bombina and Bombina variegata (Amphibia: Discoglossidae) near Pe??enica in Croatia. We obtained laboratory measuments of the belly pattern, skin thickness, mating call, skeletal form, egg size, and the developmental time of tadpoles. Although offspring from hybrid populations showed no evidence of reduced viability, a third of the F₁ families failed completely, irrespective of the direction of the cross. All traits differed significantly between the taxa. Clines in belly pattern, skin thickness, mating call, and skeletal form were closely concordant with clines in four diagnostic enzyme loci. However, the cline in developmental time was displaced towards bombina, and the cline in egg size was displaced towards variegata. This discordance could be because the traits are not inherited additively or because they are subject to different selection pressures. We favor the latter explanation in the case of developmental time. We show that moderate selection acting directly on a trait suffices to shift its position; rather stronger selection is needed to change its width appreciably. Within hybrid populations, there are significant associations among quantitative traits, and between traits and enzymes. Phenotypic variances also increase in hybrid populations. These observations can be explained by linkage disequilibria among the underlying loci. However, the average magnitude of the covariance between traits is about half that expected from the linkage disequilibria between enzyme loci. The discrepancy is not readily explained by nonadditive gene action. This puzzle is now unresolved and calls for further investigation.     

THE EFFICACY OF DIVERGENCE HITCHHIKING IN GENERATING GENOMIC ISLANDS DURING ECOLOGICAL SPECIATION

Genes under divergent selection flow less readily between populations than other loci. This observation has led to verbal “divergence hitchhiking” models of speciation in which decreased interpopulation gene flow surrounding loci under divergent selection can generate large regions of differentiation within the genome (genomic islands). The efficacy of this model in promoting speciation depends on the size of the region affected by divergence hitchhiking. Empirical evidence is mixed, with examples of both large and small genomic islands. To address these empirical discrepancies and to formalize the theory, we present mathematical models of divergence hitchhiking, which examine neutral differentiation around selected sites. For a single locus under selection, regions of differentiation do not extend far along a chromosome away from a selected site unless both effective population sizes and migration rates are low. When multiple loci are considered, regions of differentiation can be larger. However, with many loci under selection, genome‐wide divergence occurs and genomic islands are erased. The results show that divergence hitchhiking can generate large regions of differentiation, but that the conditions under which this occurs are limited. Thus, speciation may often require multifarious selection acting on many, isolated and physically unlinked genes. How hitchhiking promotes further adaptive divergence warrants consideration.     

DIVERGENCE IS FOCUSED ON FEW GENOMIC REGIONS EARLY IN SPECIATION: INCIPIENT SPECIATION OF SUNFLOWER ECOTYPES

Early in speciation, as populations undergo the transition from local adaptation to incipient species, is when a number of transient, but potentially important, processes appear to be most easily detected. These include signatures of selective sweeps that can point to asymmetry in selection between habitats, divergence hitchhiking, and associations of adaptive genes with environments. In a genomic comparison of ecotypes of the prairie sunflower, Helianthus petiolaris, occurring at Great Sand Dunes National Park and Preserve (Colorado), we found that selective sweeps were mainly restricted to the dune ecotype and that there was variation across the genome in whether proximity to the nondune population constrained or promoted divergence. The major regions of divergence were few and large between ecotypes, in contrast with an interspecific comparison between H. petiolaris and a sympatric congener, Helianthus annuus. In general, the large regions of divergence observed in the ecotypic comparison swamped locus‐specific associations with environmental variables. In both comparisons, regions of high divergence occurred in portions of the genetic map with high marker density, probably reflecting regions of low recombination. The difference in genomic distributions of highly divergent regions between ecotypic and interspecific comparisons highlights the value of studies spanning the spectrum of speciation in related taxa.     

WEAK CROSSABILITY BARRIER BUT STRONG JUVENILE SELECTION SUPPORTS ECOLOGICAL SPECIATION OF THE HYBRID PINE PINUS DENSATA ON THE TIBETAN PLATEAU

Determining how a new hybrid lineage can achieve reproductive isolation is a key to understanding the process and mechanisms of homoploid hybrid speciation. Here, we evaluated the degree and nature of reproductive isolation between the ecologically successful hybrid species Pinus densata and its parental species P. tabuliformis and P. yunnanensis. We performed interspecific crosses among the three species to assess their crossability. We then conducted reciprocal transplantation experiments to evaluate their fitness differentiation, and to examine how natural populations representing different directions of introgression differ in adaptation. The crossing experiments revealed weak genetic barriers among the species. The transplantation trials showed manifest evidence of local adaptation as the three species all performed best in their native habitats. Pinus densata populations from the western edge of its distribution have evolved a strong local adaptation to the specific habitat in that range; populations representing different directions of introgressants with the two parental species all showed fitness disadvantages in this P. densata habitat. These observations illustrate that premating isolation through selection against immigrants from other habitat types or postzygotic isolation through selection against backcrosses between the three species is strong. Thus, ecological selection in combination with endogenous components and geographic isolation has likely played a significant role in the speciation of P. densata.     

SPATIAL VARIATION IN SELECTIVE REGIMES: SEXUAL SELECTION IN THE WATER STRIDER,GERRIS ODONTOGASTER

Studies of phenotypic selection in natural populations are often concerned with simply detecting selection. In adopting a more mechanistic approach, this study compares the sexual selection regimes in natural populations of the water strider Gerris odontogaster with a priori predictions of selection, based on a number of previous field and laboratory studies of the behavioral mechanisms of selection. In this species, a general reluctance of females to mate allows for intersexual selection for ability to subdue reluctant females in males. Female reluctance to mate has been shown to decrease with increasing population density, suggesting that sexual selection should be weaker in high density populations. Three different populations with large differences in population density were studied. A number of traits including parasite load, body mass, body size and male abdominal process length were found to experience significant sexual selection. The investigated populations differed considerably with regard to the total strength of selection on the measured traits and the form of selection on single traits. In general, males in the population with the highest density experienced the weakest selection for grasping ability. This pattern is ascribed to density-related alterations of female mating behavior. Selection for male grasping ability, as reflected by selection on male abdominal process length, is reduced in high-density populations where reluctant females are more easily subdued. Further, the studied populations differed significantly in mean phenotype and phenotypic variance for male abdominal process length. It is suggested that interpopulational differences in selective regimes may generate local adaptations with respect to male abdominal process length, and that gene flow may contribute to the maintenance of the high genetic variation in this trait. It is further suggested that more empirical effort should be made in quantifying and understanding spatial and temporal variation in selection in natural populations, since this may provide information on the prevalence of local adaptations in metric traits and on the mechanisms of selection.     

MAINTENANCE OF ECOLOGICALLY SIGNIFICANT GENETIC VARIATION IN THE TIGER SWALLOWTAIL BUTTERFLY THROUGH DIFFERENTIAL SELECTION AND GENE FLOW

Differential selection in a heterogeneous environment is thought to promote the maintenance of ecologically significant genetic variation. Variation is maintained when selection is counterbalanced by the homogenizing effects of gene flow and random mating. In this study, we examine the relative importance of differential selection and gene flow in maintaining genetic variation in Papilio glaucus. Differential selection on traits contributing to successful use of host plants (oviposition preference and larval performance) was assessed by comparing the responses of southern Ohio, north central Georgia, and southern Florida populations of P. glaucus to three hosts: Liriodendron tulipifera, Magnolia virginiana, and Prunus serotina. Gene flow among populations was estimated using allozyme frequencies from nine polymorphic loci. Significant genetic differentiation was observed among populations for both oviposition preference and larval performance. This differentiation was interpreted to be the result of selection acting on Florida P. glaucus for enhanced use of Magnolia, the prevalent host in Florida. In contrast, no evidence of population differentiation was revealed by allozyme frequencies. F_ST-values were very small and Nm, an estimate of the relative strengths of gene flow and genetic drift, was large, indicating that genetic exchange among P. glaucus populations is relatively unrestricted. The contrasting patterns of spatial differentiation for host-use traits and lack of differentiation for electrophoretically detectable variation implies that differential selection among populations will be counterbalanced by gene flow, thereby maintaining genetic variation for host-use traits.     

GENE FLOW AND SELECTION ON PHENOTYPIC PLASTICITY IN AN ISLAND SYSTEM OF RANA TEMPORARIA

Gene flow is often considered to be one of the main factors that constrains local adaptation in a heterogeneous environment. However, gene flow may also lead to the evolution of phenotypic plasticity. We investigated the effect of gene flow on local adaptation and phenotypic plasticity in development time in island populations of the common frog Rana temporaria which breed in pools that differ in drying regimes. This was done by investigating associations between traits (measured in a common garden experiment) and selective factors (pool drying regimes and gene flow from other populations inhabiting different environments) by regression analyses and by comparing pairwise F_ST values (obtained from microsatellite analyses) with pairwise Q_ST values. We found that the degree of phenotypic plasticity was positively correlated with gene flow from other populations inhabiting different environments (among‐island environmental heterogeneity), as well as with local environmental heterogeneity within each population. Furthermore, local adaptation, manifested in the correlation between development time and the degree of pool drying on the islands, appears to have been caused by divergent selection pressures. The local adaptation in development time and phenotypic plasticity is quite remarkable, because the populations are young (less than 300 generations) and substantial gene flow is present among islands.     

MIGRATION ENHANCES ADAPTATION IN BACTERIOPHAGE POPULATIONS EVOLVING IN ECOLOGICAL SINKS

Migration between populations can be a major evolutionary force. However, some disagreement exists as to precisely how migration affects population adaptation. Some theories emphasize the inhibitory effects of gene flow between locally adapted populations, whereas others propose that migration can enhance adaptation. Migration has also been theorized to rescue sink populations from extinction. In our experiments, we serially passaged bacteriophage Φ6 host range mutants under sink conditions on a novel host while manipulating the source and number of migrants into these experimental populations. Migrants from two sources were used: mutant Φ6 phage able to infect a novel host (treatment) and wild‐type Φ6 phage unable to infect a novel host (control). We used quadratic regressions to determine the relationship between the number of migrants per passage and the absolute fitnesses of experimental populations following 30 passages. Our results showed that migration from a control population had no effect on absolute fitnesses of our serially passaged populations following 30 passages. By contrast, the relationship between migrants per passage and absolute fitnesses for populations receiving migrants able to infect the novel host was best described by an upwardly concave curve. These results suggest that intermediate levels of migration can have favorable impacts on evolutionary adaptation.     

Strong divergent selection at multiple loci in two closely related species of ragworts adapted to high and low elevations on Mount Etna

Recently diverged species present particularly informative systems for studying speciation and maintenance of genetic divergence in the face of gene flow. We investigated speciation in two closely related Senecio species, S. aethnensis and S. chrysanthemifolius, which grow at high and low elevations, respectively, on Mount Etna, Sicily and form a hybrid zone at intermediate elevations. We used a newly generated genome‐wide single nucleotide polymorphism (SNP) dataset from 192 individuals collected over 18 localities along an elevational gradient to reconstruct the likely history of speciation, identify highly differentiated SNPs, and estimate the strength of divergent selection. We found that speciation in this system involved heterogeneous and bidirectional gene flow along the genome, and species experienced marked population size changes in the past. Furthermore, we identified highly‐differentiated SNPs between the species, some of which are located in genes potentially involved in ecological differences between species (such as photosynthesis and UV response). We analysed the shape of these SNPs’ allele frequency clines along the elevational gradient. These clines show significantly variable coincidence and concordance, indicative of the presence of multifarious selective forces. Selection against hybrids is estimated to be very strong (0.16–0.78) and one of the highest reported in literature. The combination of strong cumulative selection across the genome and previously identified intrinsic incompatibilities probably work together to maintain the genetic and phenotypic differentiation between these species – pointing to the importance of considering both intrinsic and extrinsic factors when studying divergence and speciation.     

The geography of divergence with gene flow facilitates multitrait adaptation and the evolution of pollinator isolation in Mimulus aurantiacus

Ecological adaptation is the driving force during divergence with gene flow and generates reproductive isolation early in speciation. Although gene flow opposes divergence, local adaptation can be facilitated by factors that prevent the breakup of favorable allelic combinations. We investigated how selection, genetic architecture, and geography have contributed to the maintenance of floral trait divergence and pollinator isolation between parapatric ecotypes of Mimulus aurantiacus. Combining greenhouse, field, and genomic studies, we show that sharp clines in floral traits are maintained by spatially varying selection. Although adaptation breaks down where the ecotypes co‐occur, leading to the formation of a hybrid zone, the largely non‐overlapping distributions of the ecotypes shield them from immigrant genes, facilitating divergence across most of the range. In contrast to the sharp genetic discontinuities observed across most hybrid zones, we observed a gradual cline in genome‐wide divergence and a pattern of isolation by distance across the landscape. Thus, contrary to a long period of allopatry followed by recent re‐contact, our data suggest that floral trait divergence in M. aurantiacus may have evolved with locally restricted, but ongoing gene flow. Therefore, our study reveals how the geographic distribution of an organism can contribute to the evolution of premating isolation in the early stages of divergence with gene flow.     

LOCAL ADAPTATION AND AGENTS OF SELECTION IN A MOBILE INSECT

The deme-formation hypothesis states that selection can produce adaptive genetic variation within and among phytophagous insect populations. We conducted three field experiments and tested this prediction by transferring eggs and measuring performance of a mobile leafmining insect, Stilbosis quadricustatella. In Experiment 1, we compared the rate of mine initiation of leafminers transferred to natal and novel sites. In Experiment 2, we compared mine-initiation rate of leafminers transferred to natal and novel host-plant species. In Experiment 3, we compared the mine-initiation rate, mine-completion rate, and sources of mortality of miners transferred to neighboring natal and novel Quercus geminata trees. In the first, second, and third experiments, leafminer larvae initiated significantly more mines at the natal site, on the natal plant species, and on the natal Q. geminata tree, evidence for adaptive differentiation. Furthermore, plant-mediated mortality was significantly lower among miners transferred to natal Q. geminata trees. This result supports a key assumption of the deme-formation hypothesis: insects adapt to the defensive phenotypes of individual trees. However, natural-enemy mortality was significantly higher among miners transferred to natal trees, essentially reversing the plant effect. Therefore, rates of successful mine completion were similar on natal (19%) and novel (17%) trees. This experiment suggests that host plants and natural enemies may represent opposing forces of selection. Leafminers adapted to individual trees may realize a selective advantage only when natural-enemy densities are low.     

NO EFFECT OF ENVIRONMENTAL HETEROGENEITY ON THE MAINTENANCE OF GENETIC VARIATION IN WING SHAPE IN DROSOPHILA MELANOGASTER

Theory suggests that heterogeneous environments should maintain more genetic variation within populations than homogeneous environments, yet experimental evidence for this effect in quantitative traits has been inconsistent. To examine the effect of heterogeneity on quantitative genetic variation, we maintained replicate populations of Drosophila melanogaster under treatments with constant temperatures, temporally variable temperature, or spatially variable temperature with either panmictic or limited migration. Despite observing differences in fitness and divergence in several wing traits between the environments, we did not find any differences in the additive genetic variance for any wing traits among any of the treatments. Although we found an effect of gene flow constraining adaptive divergence between cages in the limited migration treatment, it did not tend to increase within‐population genetic variance relative to any of the other treatments. The lack of any clear and repeatable patterns of response to heterogeneous versus homogeneous environments across several empirical studies suggests that a single general mechanism for the maintenance of standing genetic variation is unlikely; rather, the relative importance of putative mechanisms likely varies considerably from one trait and ecological context to another.     

THE INTENSITY OF SELECTION ACTING ON THE COUCH POTATO GENE—SPATIAL–TEMPORAL VARIATION IN A DIAPAUSE CLINE

Cosmopolitan populations of Drosophila melanogaster have co‐opted a form of reproductive diapause to overwinter in northern populations. Polymorphism in the couch potato gene has been implicated in genetic variation for this diapause trait. Using a collection of 20 populations from Florida to Canada and 11 collections from 3 years in a Pennsylvania orchard, we estimated the allele frequencies for 15 single nucleotide polymorphisms (SNPs) in the couch potato gene. These include the specific polymorphism associated with diapause inducability. We find that the SNP polymorphism, 48034(A/T), is correlated with latitude and its frequencies are predicted by the incidence of diapause trait. We find that the clinal patterns for cpo SNPs sampled in 1997 are similar to the same SNPs sampled in 2009–2010. SNPs that show apparent associations with cpo expression are also clinal with the low‐expression allele increasing in frequency, as would be predicted from functional knockout studies of cpo. Finally, we see a significant pattern where the frequency of the diapause‐causing allele drops in frequency during the summer season, consistent with the drop in the incidence of the diapause trait. The selection required to drive this response is large, roughly 24% to 59% per generation depending on the degree of dominance.     

毛乌素沙地柠条群体分子生态学 初步研究：RAPD证据

毛乌素沙地柠条群体是一个杂种带。为了进一步阐明分子变异和基因流与生境或生态过渡带的联系,应用ＲＡＰＤ标记开展了柠条群体的分子生态学研究。根据ＲＡＰＤ数据利用Ｓｈａｎｎｏｎ信息指数估计了６个柠条群体的遗传多样性,发现大部分的分子变异存在于柠条群体之内（８２．４％）,只有少部分的分子变异存在于群体之间（１７．６％）。又利用Ｎｅｉ指数统计了ＲＡＰＤ数据,也证实了大部分的遗传变异存在于群体之内。柠条锦鸡儿群体与中间锦鸡儿群体的遗传分化系数和遗传距离都很小。以上结果都肯定了柠条群体间和种间的基因流动。无论是从多态位点比率还是群体的遗传多样性来看,硬梁和硬梁覆沙群体是最小的,滩地覆沙群体则具有较高的水平。某些ＲＡＰＤ扩增片段的频率在柠条群体间有规律的变化也许具有着特殊的生态学意义,更可能是中性突变的随机固定。根据以上研究可以得出下列结论：①通过比较Ｓｈａｎｎｏｎ指数和Ｎｅｉ指数的统计结果,可以认为,对于异交植物来讲,Ｓｈａｎｎｏｎ指数在统计ＲＡＰＤ数据方面有用。②毛乌素沙地柠条群体之间存在着强大的基因流,物种的杂交性与生态过渡性一致     

毛乌素沙地柠条群体分子生态学初步研究:RAPD证据

毛乌素沙地柠条群体是一个杂种带,为了进一步阐明分子变异和基因流与生境或生态过渡带的联系,应用ＲＡＰＤ标记开展了柠条群体的分子生态学研究。根据ＲＡＰＤ数据利用Ｓｈａｎｎｏｎ信息指数估计了６个柠条群体的遗传多样性,发现大部分的分子变异存在于柠条群体之内（８２．４％）,只有少部分的分子变异存在于群体之间（１７．６％）,又利用ｅｉ指数统计了ＲＡＰＤ数据,也证实了大部分的遗传变异存在于群体之间,柠条锦鸡儿群     

THE EFFECTS OF THE RELATIVE GEOGRAPHIC SCALES OF GENE FLOW AND SELECTION ON MORPH FREQUENCIES IN THE WALKING-STICK TIMEMA CRISTINAE

Gene frequencies in large populations are determined by a balance between selection and gene flow between neighborhoods of different selection regimes. This balance is affected by the area of the patches of a given selection regime relative to the gene-flow distance. If patches are small relative to gene-flow distance, similarity in the total area occupied by different patch types is a crucial condition for the stability of polymorphisms. However, if patches are larger than the gene-flow distance, then the relative area of different patch types is less important because of reduced gene flow resulting from isolation by distance. Two morphs (striped and unstriped) of the walking-stick Timema cristinae were each strongly associated with patches of distinct species of food plants on which they are most cryptic. The frequency of a morph was high on the plant on which it is most cryptic when either: (1) the area occupied by the food plant (patch) was very large; (2) the patch was completely isolated from other patches; or (3) the patch was larger than adjacent patches. Results (1) and (2) are consistent with isolation-by-distance models, and result (3) is consistent with Levene's multiple-niche polymorphism model.     

AN EMPIRICAL TEST OF PREDICTIONS OF TWO COMPETING MODELS FOR THE MAINTENANCE AND FATE OF HYBRID ZONES: BOTH MODELS ARE SUPPORTED IN A HARD-CLAM HYBRID ZONE

Two models developed to discern the mode of selection in hybrid zones differ in some predictions. The tension-zone model predicts that selection acts against hybrids and independently of the environment (endogenous selection) and that selection is invariant throughout the hybrid zone. The ecological selection-gradient, or ecotone, model maintains that fitness of different genotypes varies in response to environmental variation (exogenous selection) and thus, that in a region of the zone, fitness of hybrids is at least equal to that of the parental species. Therefore, to assess the predominant mode of selection operating in a hybrid zone, it is fundamental to evaluate whether selection is acting specifically against hybrid individuals, that is, whether hybridity alone is the basis for deficiencies of hybrids, and to evaluate whether the relative fitness of hybrids versus that of pure species varies across the zone. In a hardclam (genus Mercenaria) hybrid zone located in a polyhaline lagoon in east-central Florida, we used age-specific and location-specific analyses to determine that a hybrid deficit occurrs, that the deficit seems to be due to selection against hybrids, and that selection varies across the zone. Various measures of deviation from Hardy-Weinberg equilibrium, linkage disequilibrium analyses, and shifts in allele frequencies at semidiagnostic loci support the idea that selection is strongest in the northern region of the lagoon, the zone of sympatry and hybridization. Southward, into the range of M. mercenaria (the numerically predominant species), the percentage of hybrids remains relatively high and selection against hybrids decreases. For some genetic linkage groups, selection for M. mercenaria alleles seems to be occurring, but selection seems to be acting principally against alleles characteristic of M. mercenaria and, to a lesser degree, for alleles characteristic of M. campechiensis (the rarer species). These findings and others from previous analyses we have done on this hybrid zone demonstrate that selection in the zone is complex, and that characteristics of both the tension-zone and ecotone models are present. Supporting the tension-zone model, selection against hybrids per se clearly occurs, but specific genotypes seem to be at a selective disadvantage, whereas others have a selective advantage, and selection operates differentially on the two parental species within the zone. Supporting the ecotone model, the strength of overall selection varies throughout the zone, and environmentally mediated selection in which each species and hybrids have an advantage in specific habitats occurs, but some selection against hybrids is invariant throughout the zone. Thus, the structure and genetic architecture of this hybrid zone appear to be products of a complicated interaction between both types of selective forces cited in the two competing models.