Quantifying the roles of ecology and geography in spatial genetic divergence

Investigating the properties of ecological landscapes that influence gene flow among populations can provide key insights into the earliest stages of biological divergence. Both ecological and geographical factors can reduce gene flow, which can lead to population divergence, but we know little of the relative strengths of these phenomena in nature. Here, we use a novel application of structural equation modelling to quantify the contributions of ecological and geographical isolation to spatial genetic divergence in 17 species of Anolis lizards. Our comparative analysis shows that although both processes contributed significantly, geographical isolation explained substantially more genetic divergence than ecological isolation (36.3 vs. 17.9% of variance respectively), suggesting that despite the proposed ubiquity of ecological divergence, non‐ecological factors play the dominant role in the evolution of spatial genetic divergence.     

Shallow genetic divergence and species delineations in the endemic Labeobarbus species flock of Lake Tana,Ethiopia

To assess whether the species distinctions of Lake Tana's Labeobarbus spp. are supported by genetic information, microsatellite markers were used. A total of 376 Labeobarbus spp., belonging to 24 populations of 11 species from three regions of the lake (north, south and east), were sampled. Eight microsatellite markers were analysed. In general, differences between conspecific populations were smaller than differences between populations of different species. For six species, conspecific populations from different regions in the lake were consistently more similar than populations of other species from the same region. For four species this was not the case, while for one species two populations were similar, but different from the third population. River‐spawning species appeared to be more distinct than presumed lake spawners. On the species level, there was a significant correlation between genetic and morphological differentiation, especially in morphological aspects associated with ecological functioning. This suggests that genetic differentiation arose together with adaptive radiation, although the overall genetic differentiation among the Lake Tana Labeobarbus spp. is small.     

Population divergence in plant species reflects latitudinal biodiversity gradients

The trend for increasing biodiversity from the poles to the tropics is one of the best-known patterns in nature. This latitudinal biodiversity gradient has primarily been documented so far with extant species as the measure of biodiversity. Here, we evaluate the global pattern in biodiversity across latitudes based on the magnitude of genetic population divergence within plant species, using a robust spatial design to compare published allozyme datasets. Like the pattern of plant species richness across latitudes, we expected the divergence among populations of current plant species would have a similar pattern and direction. We found that lower latitudinal populations showed greater genetic differentiation within species after controlling for geographical distance. Our analyses are consistent with previous population-level studies in animals, suggesting a high possibility of tropical peaks in speciation rates associated with observed levels of species richness.     

Along the speciation continuum: Quantifying intrinsic and extrinsic isolating barriers across five million years of evolutionary divergence in California jewelflowers

Understanding the relative roles of intrinsic and extrinsic reproductive barriers, and their interplay within the geographic context of diverging taxa, remains an outstanding challenge in the study of speciation. We conducted a comparative analysis of reproductive isolation in California Jewelflowers (Streptanthus, s.l., Brassicaceae) by quantifying potential barriers to gene flow at multiple life history stages in 39 species pairs spanning five million years of evolutionary divergence. We quantified nine potential pre‐ and postzygotic barriers and explored patterns of reproductive isolation in relation to genetic distance. Intrinsic postzygotic isolation was initially weak, increased at intermediate genetic distances, and reached a threshold characterized by complete genetic incompatibility. Climatic niche differences were strong at shallow genetic distances, and species pairs with overlapping ranges showed slight but appreciable phenological isolation, highlighting the potential for ecological barriers to contribute to speciation. Geographic analyses suggest that speciation is not regionally allopatric in the California Jewelflowers, as recently diverged taxa occur in relatively close proximity and display substantial range overlap. Young pairs are characterized by incomplete intrinsic postzygotic isolation, suggesting that extrinsic barriers or fine‐scale spatial segregation are more important early in the divergence process than genetic incompatibilities.     

Recombination and the divergence of hybridizing species

The interplay between hybridization and recombination can have a dramatic effect on the likelihood of speciation or persistence of incompletely isolated species. Many models have suggested recombination can oppose speciation, and several recent empirical investigations suggest that reductions in recombination between various components of reproductive isolation and/or adaptation can allow species to persist in the presence of gene flow. In this article, we discuss these ideas in relation to speciation models, phylogenetic analyses, and species concepts. In particular, we revisit genetic architectures and population mechanisms that create genetic correlations and facilitate divergence in the face of gene flow. Linkage among genes contributing to adaptation or reproductive isolation due to chromosomal rearrangements as well as pleiotropy or proximity of loci can greatly increase the odds of species divergence or persistence. Finally, we recommend recombination to be a focus of inquiry when studying the origins of biological diversity.     

Different processes shape the patterns of divergence in the nuclear and chloroplast genomes of a relict tree species in East Asia

Isolation by spatial distance (IBD), environment (IBE), and historical climatic instability (IBI) are three common processes assessed in phylogeographic and/or landscape genetic studies. However, the relative contributions of these three processes with respect to spatial genetic patterns have seldom been compared. Moreover, whether the relative contribution differs in different regions or when assessed using different genetic markers has rarely been reported. Lindera obtusiloba has been found to have two sister genetic clades of chloroplast (cpDNA) and nuclear microsatellite (nSSR), both of which show discontinuous distribution in northern and southern East Asia. In this study, we used the Mantel test and multiple matrix regression with randomization (MMRR) to determine the relative contributions of IBD, IBE, and IBI with respect to L. obtusiloba populations. Independent Mantel tests and MMRR calculations were conducted for two genetic data sets (cpDNA and nSSR) and for different regions (the overall species range, and northern and southern subregions of the range). We found a significant IBI pattern in nSSR divergence for all assessed regions, whereas no clear IBI pattern was detected with respect to cpDNA. In contrast, significant (or marginal) divergent IBD patterns were detected for cpDNA in all regions, whereas although a significant IBE was apparent with respect to the overall range, the effect was not detected in the two subregions. The differences identified in nSSR and cpDNA population divergence may be related to differences in the heredity and ploidy of the markers. Compared with the southern region, the northern region showed less significant correlation patterns, which may be related to the shorter population history and restricted population range. The findings of this study serve to illustrate that comparing between markers or regions can contribute to gaining a better understanding the population histories of different genomes or within different regions of a species' range.     

Studies of the species barrier between Drosophila subobscura and D. madeirensis IV. A genetic dissection of the X chromosome for speciation genes

The genetics of four traits contributing to the isolation mechanism between the two closely related species of Drosophila belonging to the obscura group, D. subobscura and D. madeirensis, have been investigated, especially regarding the influence exerted by the X chromosome. This chromosome has been roughly dissected genetically by the use of four markers. It was found that factors affecting viability of backcross males are spread from the centromeric end of the chromosome up the region marked by Bx. Three sections were responsible for male sterility/fertility. The abnormal head shape of the backcross males was affected by factor(s) on the madeirensis and the subobscura sex chromosome located at the region of MAD1 inversion. Finally, an abnormal trait in these males (presence of extra sex combs) was found to be controlled by four sections, two on the madeirensis X chromosome and two on the subobscura one.     

Mate recognition systems in a species flock of Mexican pupfish

The pupfishes of Lake Chichancanab (Mexico) provide a unique opportunity to study the evolution of premating reproductive barriers. This group of endemic species is of recent origin and the lineages differ in morphological traits indicating trophic specialization, but show very little genetic change. We studied the function of visual and chemical cues in the mate recognition system of three morphospecies, Cyprinodon beltrani, C. labiosus and C. maya. Only in C. maya, which is genetically the most distinct member of the group, do females show the ability to identify males of their own type, both visually and chemically. C. labiosus females discriminated between their own and C. beltrani males based on chemical but not visual cues. C. beltrani, which is morphologically the least differentiated member of the group, showed no interspecific mate recognition. Females responded more strongly to the visual and chemical cues of their own males than to their own females, but they did not discriminate between their own males and those of the other two morphospecies based upon either type of cue. These results suggest that different levels of behavioural isolation have been established: most isolated is C. maya, and the least is C. beltrani. C. labiosus has an intermediate position. The results also suggest that species recognition cues based on different sensory modalities do not necessarily evolve together, and may evolve at different rates.     

Mating preferences in a species flock of Mexican pupfishes (Cyprinodon, Teleostei)

Female mating preferences were examined in three members of an evolutionarily young Cyprinodon lineage from Laguna Chichancanab, Yucatan, Mexico. In separate experiments, females of C. beltrani and C. labiosus , and C. beltrani and C. maya were simultaneously presented with conspecific and heterospecific males and given the opportunity to spawn with either or both. These three species showed different degrees of conspecific mate recognition: complete for C. maya , intermediate for C. labiosus , and indiscriminate for C. beltrani. We conclude that only C. maya is reproductively isolated and that C. beltrani and C. labiosus still hybridize in nature. Whereas between C. beltrani and C. maya mate choice is symmetric, it is asymmetric between C. beltrani and C labiosus. The results of the mating trials are consistent with mitochondrial DNA data which indicate that C. maya is genetically the most distinct species in the flock. They are also supported by experiments on visually and chemically mediated mate preferences.     

Hierarchical components of genetic variation at a species boundary: population structure in two sympatric varieties of Lupinus microcarpus (Leguminosae)

Lupinus microcarpus is a self-compatible annual plant that forms a species complex of morphologically variable but indeterminate varieties. In order to examine the hypothesis that varieties of L. microcarpus comprise genetically differentiated and reproductively isolated species, populations of L. microcarpus var. horizontalis and var. densiflorus were sampled from an area of sympatry in central California and genotyped using six microsatellite loci. Bayesian clustering divided the total sample into two groups corresponding to the named varieties with extremely low levels of inferred coancestry. Similarly, maximum likelihood and distance methods for genetic assignment placed individuals in two nonoverlapping groups. Evidence for isolation by distance (IBD) within each variety was found at shorter distance classes, but varieties remained differentiated in sympatry. Furthermore, coalescent estimates of divergence time indicate separation within the past 950-5050 generations, with minimal gene flow after divergence. A four-level hierarchical analysis of molecular variance (amova) found significant levels of genetic differentiation among varieties (theta(P) = 0.292), populations within varieties (theta(S) = 0.449), subpopulations within populations (theta(SS) = 0.623), and individuals within subpopulations (f = 0.421); but the greatest degree of differentiation was at the subpopulation level. Although it is sometimes assumed that the magnitude of genetic differences (e.g. F(ST)) should be greater between species than among populations or subpopulations of the same species, shared ancestral polymorphism may lead to relatively low levels of differentiation at the species level, even as the stochastic effects of genetic drift generate higher levels of differentiation at lower hierarchical levels. These results suggest that L. microcarpus var. horizontalis and var. densiflorus are recently diverged yet reproductively isolated species, with high levels of inbreeding resulting from the combined effects of limited gene flow, demographic bottlenecks, and partial selfing in finite, geographically structured populations.     

Phenotypic divergence but not genetic distance predicts assortative mating among species of a cichlid fish radiation

The hypothesis of ecological divergence giving rise to premating isolation in the face of gene flow is controversial. However, this may be an important mechanism to explain the rapid multiplication of species during adaptive radiation following the colonization of a new environment when geographical barriers to gene flow are largely absent but underutilized niche space is abundant. Using cichlid fish, we tested the prediction of ecological speciation that the strength of premating isolation among species is predicted by phenotypic rather than genetic distance. We conducted mate choice experiments between three closely related, sympatric species of a recent radiation in Lake Mweru (Zambia/DRC) that differ in habitat use and phenotype, and a distantly related population from Lake Bangweulu that resembles one of the species in Lake Mweru. We found significant assortative mating among all closely related, sympatric species that differed phenotypically, but none between the distantly related allopatric populations of more similar phenotype. Phenotypic distance between species was a good predictor of the strength of premating isolation, suggesting that assortative mating can evolve rapidly in association with ecological divergence during adaptive radiation. Our data also reveals that distantly related allopatric populations that have not diverged phenotypically, may hybridize when coming into secondary contact, e.g. upon river capture because of diversion of drainage systems.     

Intraspecific variation in reproductive barriers between two closely related Arabidopsis sister species

Reproductive isolation (RI) is a critical component of speciation and varies strongly in timing and strength among different sister taxa, depending on, for example the geography of speciation and divergence time. However, these factors may also produce variation in timing and strength among populations within species. Here we tested for variation in the expression of RI among replicate population pairs between the sister taxa Arabidopsis lyrata subsp. lyrata and A. arenicola. While the former is predominantly outcrossing, the latter is predominantly selfing. We focused on intrinsic prezygotic and postzygotic RI as both species occur largely in allopatry. We assessed RI by performing within-population crosses and interspecific between-population crosses, and by raising offspring. RI was generally high between all interspecific population pairs, but it varied in timing and strength depending on population history. Prezygotic isolation was strongest between the closest-related population pair, while early postzygotic isolation was high for all other population pairs. Furthermore, the timing and strength of RI depended strongly on cross direction. Our study provides empirical support that reproductive barriers between species are highly variable among population pairs and asymmetric within population pairs, and this variation seems to follow patterns typically described across species pairs.     

History,geography and host use shape genomewide patterns of genetic variation in the redheaded pine sawfly (Neodiprion lecontei)

Divergent host use has long been suspected to drive population differentiation and speciation in plant‐feeding insects. Evaluating the contribution of divergent host use to genetic differentiation can be difficult, however, as dispersal limitation and population structure may also influence patterns of genetic variation. In this study, we use double‐digest restriction‐associated DNA (ddRAD) sequencing to test the hypothesis that divergent host use contributes to genetic differentiation among populations of the redheaded pine sawfly (Neodiprion lecontei), a widespread pest that uses multiple Pinus hosts throughout its range in eastern North America. Because this species has a broad range and specializes on host plants known to have migrated extensively during the Pleistocene, we first assess overall genetic structure using model‐based and model‐free clustering methods and identify three geographically distinct genetic clusters. Next, using a composite‐likelihood approach based on the site frequency spectrum and a novel strategy for maximizing the utility of linked RAD markers, we infer the population topology and date divergence to the Pleistocene. Based on existing knowledge of Pinus refugia, estimated demographic parameters and patterns of diversity among sawfly populations, we propose a Pleistocene divergence scenario for N. lecontei. Finally, using Mantel and partial Mantel tests, we identify a significant relationship between genetic distance and geography in all clusters, and between genetic distance and host use in two of three clusters. Overall, our results indicate that Pleistocene isolation, dispersal limitation and ecological divergence all contribute to genomewide differentiation in this species and support the hypothesis that host use is a common driver of population divergence in host‐specialized insects.     

Reproductive isolation in natural populations of Drosophila melanogaster from Brazzaville (Congo)

The aim of this work is to analyze the homogamy previously detected between two natural populations of Drosophila melanogaster from Brazzaville. It is shown that mating isolation was still maintained under laboratory conditions 10 years after the populations samples were trapped. Isolation seemed to be due mainly to pre-mating isolation and we checked for any suggestion of post-mating mortality of hybrids. Pre-mating isolation was not symmetrical, and significant ² values were found in 3/4 possible 3-way mating choice experiments. The only exception involved a male from the countryside and two females (one from each population) for which no significant mating preference was detected. Mortality of hybrids was intermediate between those of the parental strains showing a clear maternal effect and the existence of partial dominance. Major differences in the cuticular hydrocarbons were also found and they could account for the isolation. These findings in populations from African breweries indicate that they are closely related to European ones, suggesting that this phenomenon is not a case of sympatric speciation, but probably attributable to the reintroduction of an allopatric population.     

Genetic divergence in the Chorthippus parallelus species group (Orthoptera: Acrididae)

Specimens of Chorthippus parallelus parallelus, C. p. erythropus, C. montanus, C. curtipennis and C. dorsatus were examined electrophoretically. This analysis indicates that C. curtipennis is very closely related to C. p. parallelus and C.p. erythropus (Nei's I = 0.97) while C. montanus is more distantly related ( I = 0.88). The values are consistent with divergence of C. p. erythropus from C. p. parallelus since its separation by the Pyrenean ice sheet during the Pleistocene and of C. curtipennis since invasion of North America by C. parallelus at the same time. A much earlier divergence of C. montanus is implied.     

Genetic association of physically unlinked islands of genomic divergence in incipient species of Anopheles gambiae

Previous efforts to uncover the genetic underpinnings of ongoing ecological speciation of the M and S forms of the African malaria vector Anopheles gambiae revealed two centromere‐proximal islands of genetic divergence on X and chromosome 2. Under the assumption of considerable ongoing gene flow between M and S, these persistently divergent genomic islands were widely considered to be ‘speciation islands’. In the course of microarray‐based divergence mapping, we discovered a third centromere‐associated island of divergence on chromosome 3, which was validated by targeted re‐sequencing. To test for genetic association between the divergence islands on all three chromosomes, SNP‐based assays were applied in four natural populations of M and S spanning West, Central and East Africa. Genotyping of 517 female M and S mosquitoes revealed nearly complete linkage disequilibrium between the centromeres of the three independently assorting chromosomes. These results suggest that despite the potential for inter‐form gene flow through hybridization, actual (realized) gene flow between M and S may be substantially less than commonly assumed and may not explain most shared variation. Moreover, the possibility of very low gene flow calls into question whether diverged pericentromeric regions—characterized by reduced levels of variation and recombination—are in fact instrumental rather than merely incidental to the speciation process.     

Disassociation between weak sexual isolation and genetic divergence in a hermaphroditic land snail and implications about chirality

Examination of the association between reproductive isolation and genetic divergence in a variety of organisms is essential for elucidating the mechanisms causing speciation. However, such studies are lacking for hermaphrodites. We measured premating (sexual) isolation in species pairs of the hermaphroditic land snail Albinaria and we compared it with their genetic divergence. We did not find substantial sexual isolation barriers between the species studied. The absence of strong sexual isolation between species implies its minor effect in the evolution of this genus, because distributional, population and life-history characteristics of Albinaria make mate-choice possibly redundant. Furthermore, we found disassociation between genetic divergence and sexual isolation, suggesting that they do not form necessarily a cause-effect duet. However, Albinaria voithii, the only dextral Albinaria species, shows strong sexual isolation against the other sinistral species. We discuss whether change in coiling either has triggered instantaneous speciation, or is an example of character displacement.     

Allozymic variation and divergence in three species of Antirrhinum L. (Scrophulariaceae-Antirrhineae)

An allozymic study of three wild species of Antirrhinum L. A. lopesiamum Rothm., A. mollissimum Roihni. and A. microphyllum Rothm. is described. All are members of subsection Kickiella Rothm., and are narrow-range endemics of the Iberian Peninsula. The variability of the different loci, as well as the number and mobility of the alleles, differ among the three species, a demonstration of the usefulness of allozymes for the systematics of the genus. The finding of alleles unique to each species indicates high divergence among species suggesting ancient diversification, and supports the hypothesis of a geographical model of speciation. All three species show high levels of within-species variability, mainly partitioned within populations, while between populations genetic differentiation is low. Correlations between population size, sample size and genetic variability, and the usefulness of allozymic data for conservation purposes, are discussed.     

Variation in reproductive isolation across a species range

Reproductive isolation is often variable within species, a phenomenon that while largely ignored by speciation studies, can be leveraged to gain insight into the potential mechanisms driving the evolution of genetic incompatibilities. We used experimental greenhouse crosses to characterize patterns of reproductive isolation among three divergent genetic lineages of Campanulastrum americanum that occur in close geographic proximity in the Appalachian Mountains. Substantial, asymmetrical reproductive isolation for survival due to cytonuclear incompatibility was found among the lineages (up to 94% reduction). Moderate reductions in pollen viability, as well as cytoplasmic male sterility, were also found between some Mountain populations. We then compared these results to previously established patterns of reproductive isolation between these Mountain lineages and a fourth, widespread Western lineage to fully characterize reproductive isolation across the complete geographic and genetic range of C. americanum. Reproductive isolation for survival and pollen viability was consistent across studies, indicating the evolution of the underlying genetic incompatibilities is primarily determined by intrinsic factors. In contrast, reproductive isolation for germination was only found when crossing Mountain populations with the Western lineage, suggesting the underlying genetic incompatibility is likely influenced by environmental or demographic differences between the two lineages. Cytoplasmic male sterility was also limited in occurrence, being restricted to a handful of Mountain populations in a narrow geographic range. These findings illustrate the complexity of speciation by demonstrating multiple, independent genetic incompatibilities that lead to a mosaic of genetic divergence and reproductive isolation across a species range.