Enhanced and asymmetric signatures of hybridization at climatic margins: Evidence from closely related dioecious fig species.

Hybridization plays a significant role in biological evolution. However, it is not clear whether ecological contingency differentially influences likelihood of hybridization, particularly at ecological margins where parental species may exhibit reduced fitnesses. Moreover, it is unknown whether future ecosystem change will increase the prevalence of hybridization. Ficus heterostyla and F. squamosa are closely related species co-distributed from southern Thailand to southwest China where hybridization, yielding viable seeds, has been documented. As a robust test of ecological factors driving hybridization, we investigated spatial hybridization signatures based on nuclear microsatellites from extensive population sampling across a widespread contact range. Both species showed high population differentiation and strong patterns of isolation by distance. Admixture estimates exposed asymmetric interspecific gene flow. Signatures of hybridization increase significantly towards higher latitude zones, peaking at the northern climatic margins. Geographic variation in reproductive phenology combined with ecologically challenging marginal habitats may promote this phenomenon. Our work is a first systematic evaluation of such patterns in a comprehensive, latitudinally-based clinal context, and indicates that tendency to hybridize appears strongly influenced by environmental conditions. Moreover, that future climate change scenarios will likely alter and possibly augment cases of hybridization at ecosystem scales.

Asymmetric character displacement in mixed oak stands.

Ecological character displacement (ECD) refers to a pattern of increased divergence at sites where species ranges overlap caused by competition for resources. Although ECD is believed to be common, there are few in-depth studies that clearly establish its existence, especially in plants. Thus, we have compared leaf traits in allopatric and sympatric populations of two East Asian deciduous oaks: Quercus dentata and Quercus aliena. In contrast to previous studies, we define sympatry and allopatry at a local scale, thereby comparing populations that can or cannot directly interact. Using genetic markers, we found greater genetic divergence between the two oak species growing in mixed stands and inferred that long-term gene flow has predominantly occurred asymmetrically from the cold-tolerant species (Q. dentata) to the warm-demanding later colonizing species (Q. aliena). Analysis of leaf traits revealed greater divergence in mixed than in pure oak stands. This was mostly due to the later colonizing species being characterized by more resource-conservative traits in the presence of the other species. Controlling for relevant environmental differences did not alter these conclusions. These results suggest that asymmetric trait divergence can take place where species coexist, possibly due to the imbalance in demographic history of species resulting in asymmetric inter-specific selection pressures.

Demographic consequences of dispersal-related trait shift in two recently diverged taxa of montane grasshoppers.

Although the pervasiveness of intraspecific wing-size polymorphism and transitions to flightlessness have long captivated biologists, the demographic outcomes of shifts in dispersal ability are not yet well understood and have been seldom studied at early stages of diversification. Here, we use genomic data to infer the consequences of dispersal-related trait variation in the taxonomically controversial short-winged (Chorthippus corsicus corsicus) and long-winged (Chorthippus corsicus pascuorum) Corsican grasshoppers. Our analyses revealed lack of contemporary hybridization between sympatric long- and short-winged forms and phylogenomic reconstructions supported their taxonomic distinctiveness, rejecting the hypothesis of intraspecific wing polymorphism. Statistical evaluation of alternative models of speciation strongly supported a scenario of Pleistocene divergence (<1.5 Ma) with ancestral gene flow. According to neutral expectations from differences in dispersal capacity, historical effective migration rates from the long- to the short-winged taxon were threefold higher than in the opposite direction. Although populations of the two taxa present a marked genetic structure and have experienced parallel demographic histories, our coalescent-based analyses suggest that reduced dispersal has fueled diversification in the short-winged C. c. corsicus. Collectively, our study illustrates how dispersal reduction can speed up geographical diversification and increase the opportunity for allopatric speciation in topographically complex landscapes.

Evolutionary history of a desert perennial Arnebia szechenyi (Boraginaceae): Intraspecific divergence, regional expansion and asymmetric gene flow.

The complex interactions of historical, geological and climatic events on plant evolution have been an important research focus for many years. However, the role of desert formation and expansion in shaping the genetic structures and demographic histories of plants occurring in arid areas has not been well explored. In the present study, we investigated the phylogeography of Arnebia szechenyi, a desert herb showing a near-circular distribution surrounding the Tengger Desert in Northwest China. We measured genetic diversity of populations using three maternally inherited chloroplast DNA (cpDNA) fragments and seven bi-paternally inherited nuclear DNA (nDNA) loci that were sequenced from individuals collected from 16 natural populations across its range and modelled current and historical potential habitats of the species. Our data indicated a considerably high level of genetic variation within A. szechenyi and noteworthy asymmetry in historical migration from the east to the west. Moreover, two nuclear genetic groups of populations were revealed, corresponding to the two geographic regions separated by the Tengger Desert. However, analysis of cpDNA data did not show significant geographic structure. The most plausible explanation for the discrepancy between our findings based on cpDNA and nDNA data is that A. szechenyi populations experienced long periods of geographic isolation followed by range expansion, which would have promoted generalized recombination of the nuclear genome. Our findings further highlight the important role that the Tengger Desert, together with the Helan Mountains, has played in the evolution of desert plants and the preservation of biodiversity in arid Northwest China.

Asymmetric, but opposing reductions in immigrant viability and fecundity promote reproductive isolation among host-associated populations of an insect herbivore.

Immigrant inviability can contribute to reproductive isolation (RI) during ecological speciation by reducing the survival of immigrants in non-native environments. However, studies that assess the fitness consequence of immigrants moving from native to non-native environments typically fail to explore the potential role of concomitant reductions in immigrant fecundity despite recent evidence suggesting its prominent role during local adaptation. Here, we evaluate the directionality and magnitude of both immigrant viability and fecundity to RI in a host-specific gall-forming wasp, Belonocnema treatae. Using reciprocal transplant experiments replicated across sites, we measure immigrant viability and fecundity by comparing differences in the incidence of gall formation (viability) and predicted the number of eggs per female (fecundity) between residents and immigrants in each of two host-plant environments. Reduced immigrant viability was found in one host environment while reduced immigrant fecundity was found in the other. Such habitat-dependent barriers resulted in asymmetric RI between populations. By surveying recent literature on local adaptation, we find that asymmetry in immigrant viability and fecundity are widespread across disparate taxa, which highlights the need to combine estimates of both common and overlooked barriers in cases of potential bi-directional gene flow to create a more comprehensive view of the evolution of RI.

When are populations not connected like a circuit? Identifying biases in gene flow from coalescent times.

Connectivity and movement patterns of populations are influenced by past and present environmental and biotic factors, which are reflected in genetic relatedness among populations. Methods that estimate the "commute time" between populations based on electrical resistance (i.e., isolation-by-resistance [IBR]) have been widely applied to either infer movement patterns directly from environmental factors or detect possible barriers to gene flow given empirical genetic relatedness. Yet, the commute time is only equivalent to the coalescence time between populations under symmetric migration with isotropic landscapes. Asymmetric gene flow is relatively common when populations are expanding, retreating, or with source-sink dynamics. In a From the Cover paper in this issue of Molecular Ecology Resources, Lundgren and Ralph (Molecular Ecology Resources, 19, 2019) describe a Bayesian method to infer bidirectional gene flow rates and population sizes without the assumption of symmetry. The method shows great accuracy in connectivity estimations under symmetric, as well as asymmetric gene flow scenarios where resistance methods fail. However, computational complexity limits the method to a few populations, preventing its application to finescale environmental maps. Also, as a discrete-deme static model, the inferred differences in gene flow rates are sensitive to population discretization and cannot be directly used to differentiate among processes (e.g., past expansion vs. current barrier). Here, we discuss scenarios where the new method can best be utilized and provide potential directions to identify the underlying processes causing deviations in gene flow patterns.

Co-occurrence of related asexual, but not sexual, lineages suggests that reproductive interference limits coexistence.

We used randomizations to analyse patterns of co-occurrence of sexual and apomictic (asexual) members of the North American Crepis agamic complex (Asteraceae). We expect strong asymmetry in reproductive interactions in Crepis: apomicts produce clonal seeds with no need for pollination and are not subject to reproductive interference from co-occurring relatives. However, because they still produce some viable pollen, apomicts can reduce reproductive success of nearby sexual relatives, potentially leading to eventual local exclusion of sexuals. Consistent with this, randomizations reveal that sexuals are over-represented in isolated sites, while apomicts freely co-occur. Incorporation of taxonomic and phylogenetic evidence indicates that this pattern is not driven by local origins of asexuals. Our evidence that patterns of local co-occurrence are structured by reproductive interference suggests an underappreciated role for these interactions in community assembly, and highlights the need for explicit tests of the relative contributions of ecological and reproductive interactions in generating patterns of limiting similarity.

Incongruent range dynamics between co-occurring Asian temperate tree species facilitated by life history traits.

Postglacial expansion to former range limits varies substantially among species of temperate deciduous forests in eastern Asia. Isolation hypotheses (with or without gene flow) have been proposed to explain this variance, but they ignore detailed population dynamics spanning geological time and neglect the role of life history traits. Using population genetics to uncover these dynamics across their Asian range, we infer processes that formed the disjunct distributions of Ginkgo biloba and the co-occurring Cercidiphyllum japonicum (published data). Phylogenetic, coalescent, and comparative data suggest that Ginkgo population structure is regional, dichotomous (to west-east refugia), and formed ˜51 kya, resulting from random genetic drift during the last glaciation. This split is far younger than the north-south population structure of Cercidiphyllum (~1.89 Mya). Significant (recent) unidirectional gene flow has not homogenized the two Ginkgo refugia, despite 2Nm > 1. Prior to this split, gene flow was potentially higher, resulting in conflicting support for a priori hypotheses that view isolation as an explanation for the variation in postglacial range limits. Isolation hypotheses (with or without gene flow) are thus not necessarily mutually exclusive due to temporal variation of gene flow and genetic drift. In comparison with Cercidiphyllum, the restricted range of Ginkgo has been facilitated by uncompetitive life history traits associated with seed ecology, highlighting the importance of both demography and lifetime reproductive success when interpreting range shifts.

Introduced Scotch broom (Cytisus scoparius) invades the genome of native populations in vulnerable heathland habitats.

Cytisus scoparius is a global invasive species that affects local flora and fauna at the intercontinental level. Its natural distribution spans across Europe, but seeds have also been moved among countries, mixing plants of native and non-native genetic origins. Hybridization between the introduced and native gene pool is likely to threaten both the native gene pool and the local flora. In this study, we address the potential threat of invasive C. scoparius to local gene pools in vulnerable heathlands. We used nuclear single nucleotide polymorphic (SNP) and simple sequence repeat (SSR) markers together with plastid SSR and indel markers to investigate the level and direction of gene flow between invasive and native heathland C. scoparius. Analyses of population structures confirmed the presence of two gene pools: one native and the other invasive. The nuclear genome of the native types was highly introgressed with the invasive genome, and we observed advanced-generation hybrids, suggesting that hybridization has been occurring for several generations. There is asymmetrical gene flow from the invasive to the native gene pool, which can be attributed to higher fecundity in the invasive individuals, measured by the number of flowers and seed pods. Strong spatial genetic structure in plastid markers and weaker structure in nuclear markers suggest that seeds spread over relatively short distances and that gene flow over longer distances is mainly facilitated by pollen dispersal. We further show that the growth habits of heathland plants become more vigorous with increased introgression from the invaders. Implications of the findings are discussed in relation to future management of invading C. scoparius.

Evolutionary processes driving spatial patterns of intraspecific genetic diversity in river ecosystems.

Describing, understanding and predicting the spatial distribution of genetic diversity is a central issue in biological sciences. In river landscapes, it is generally predicted that neutral genetic diversity should increase downstream, but there have been few attempts to test and validate this assumption across taxonomic groups. Moreover, it is still unclear what are the evolutionary processes that may generate this apparent spatial pattern of diversity. Here, we quantitatively synthesized published results from diverse taxa living in river ecosystems, and we performed a meta-analysis to show that a downstream increase in intraspecific genetic diversity (DIGD) actually constitutes a general spatial pattern of biodiversity that is repeatable across taxa. We further demonstrated that DIGD was stronger for strictly waterborne dispersing than for overland dispersing species. However, for a restricted data set focusing on fishes, there was no evidence that DIGD was related to particular species traits. We then searched for general processes underlying DIGD by simulating genetic data in dendritic-like river systems. Simulations revealed that the three processes we considered (downstream-biased dispersal, increase in habitat availability downstream and upstream-directed colonization) might generate DIGD. Using random forest models, we identified from simulations a set of highly informative summary statistics allowing discriminating among the processes causing DIGD. Finally, combining these discriminant statistics and approximate Bayesian computations on a set of twelve empirical case studies, we hypothesized that DIGD were most likely due to the interaction of two of these three processes and that contrary to expectation, they were not solely caused by downstream-biased dispersal.

Ecological differentiation, lack of hybrids involving diploids, and asymmetric gene flow between polyploids in narrow contact zones of Senecio carniolicus (syn. Jacobaea carniolica, Asteraceae).

Areas of immediate contact of different cytotypes offer a unique opportunity to study evolutionary dynamics within heteroploid species and to assess isolation mechanisms governing coexistence of cytotypes of different ploidy. The degree of reproductive isolation of cytotypes, that is, the frequency of heteroploid crosses and subsequent formation of viable and (partly) fertile hybrids, plays a crucial role for the long-term integrity of lineages in contact zones. Here, we assessed fine-scale distribution, spatial clustering, and ecological niches as well as patterns of gene flow in parental and hybrid cytotypes in zones of immediate contact of di-, tetra-, and hexaploid Senecio carniolicus (Asteraceae) in the Eastern Alps. Cytotypes were spatially separated also at the investigated microscale; the strongest spatial separation was observed for the fully interfertile tetra- and hexaploids. The three main cytotypes showed highly significant niche differences, which were, however, weaker than across their entire distribution ranges in the Eastern Alps. Individuals with intermediate ploidy levels were found neither in the diploid/tetraploid nor in the diploid/hexaploid contact zones indicating strong reproductive barriers. In contrast, pentaploid individuals were frequent in the tetraploid/hexaploid contact zone, albeit limited to a narrow strip in the immediate contact zone of their parental cytotypes. AFLP fingerprinting data revealed introgressive gene flow mediated by pentaploid hybrids from tetra- to hexaploid individuals, but not vice versa. The ecological niche of pentaploids differed significantly from that of tetraploids but not from hexaploids.

Inference of domestication history and differentiation between early- and late-flowering varieties in pearl millet.

Pearl millet (Pennisetum glaucum) is a staple crop in Sahelian Africa. Farmers usually grow varieties with different cycle lengths and complementary functions in Sahelian agrosystems. Both the level of genetic differentiation of these varieties and the domestication history of pearl millet have been poorly studied. We investigated the neutral genetic diversity and population genetic structure of early- and late-flowering domesticated and wild pearl millet populations using 18 microsatellite loci and 8 nucleotide sequences. Strikingly, early- and late-flowering domesticated varieties were not differentiated over their whole distribution area, despite a clear difference in their isolation-by-distance pattern. Conversely, our data brought evidence for two well-differentiated genetic pools in wild pearl millet, allowing us to test scenarios with different numbers and origins of domestication using approximate Bayesian computation (ABC). The ABC analysis showed the likely existence of asymmetric migration between wild and domesticated populations. The model choice procedure indicated that a single domestication from the eastern wild populations was the more likely scenario to explain the polymorphism patterns observed in cultivated pearl millet.

Spatial and temporal genetic structure of a river-resident Atlantic salmon (Salmo salar) after millennia of isolation.

The river-resident Salmo salar ("småblank") has been isolated from other Atlantic salmon populations for 9,500 years in upper River Namsen, Norway. This is the only European Atlantic salmon population accomplishing its entire life cycle in a river. Hydropower development during the last six decades has introduced movement barriers and changed more than 50% of the river habitat to lentic conditions. Based on microsatellites and SNPs, genetic variation within småblank was only about 50% of that in the anadromous Atlantic salmon within the same river. The genetic differentiation (F ST) between småblank and the anadromous population was 0.24. This is similar to the differentiation between anadromous Atlantic salmon in Europe and North America. Microsatellite analyses identified three genetic subpopulations within småblank, each with an effective population size Ne of a few hundred individuals. There was no evidence of reduced heterozygosity and allelic richness in contemporary samples (2005-2008) compared with historical samples (1955-56 and 1978-79). However, there was a reduction in genetic differentiation between sampling localities over time. SNP data supported the differentiation of småblank into subpopulations and revealed downstream asymmetric gene flow between subpopulations. In spite of this, genetic variation was not higher in the lower than in the upper areas. The meta-population structure of småblank probably maintains genetic variation better than one panmictic population would do, as long as gene flow among subpopulations is maintained. Småblank is a unique endemic island population of Atlantic salmon. It is in a precarious situation due to a variety of anthropogenic impacts on its restricted habitat area. Thus, maintaining population size and avoiding further habitat fragmentation are important.