Differential introgression reveals candidate genes for selection across a spruce (Picea sitchensis × P. glauca) hybrid zone

Differential patterns of introgression between species across ecological gradients provide a fine-scale depiction of extrinsic and intrinsic factors that contribute to the maintenance of species barriers and adaptation across heterogeneous environments. Introgression was examined for 721 individuals collected from the ecological transition zone spanning maritime to continental climates within the Picea sitchensis–Picea glauca contact zone using a panel of 268 candidate gene single nucleotide polymorphisms. Geographic clines showed a strong spatial relationship between allele frequencies and both distance from the ocean along major rivers and mean annual precipitation, indicating a strong role for environmental selection. Interspecific patterns of differentiation using outlier tests revealed three candidate genes that may be targets of long-term divergent selection between the parental species, although contemporary genomic clines within the hybrid zone suggested neutral patterns of introgression for these genes. This study provides a fine-scale analysis of locus-specific introgression, identifying a suite of candidate loci that may be targets of extrinsic or intrinsic selection, with broad application in understanding local adaptation to climate

Polymorphism of postmating reproductive isolation within plant species

Speciation can be viewed as the evolution of reproductive isolation between formerly interbreeding populations. Recent years have seen great advances in our understanding of the genetic mechanisms underlying postmating reproductive isolation during plant speciation. Nevertheless, little is known about the early stages of species divergence and the evolution of reproductive isolation at the within species level. Direct or indirect evidence indicates that intrinsic postzygotic mechanisms are prevalent and often polymorphic among allopatric conspecific populations of plants. We review studies that report direct or indirect evidence for polymorphism of genic (i.e., gene-based) postmating reproductive isolation within species' ranges. Specifically, we focus on three genic mechanisms often held responsible for reproductive isolation between species: Bateson-Dobzhansky-Muller (BDM) incompatibilities and two widespread types of genomic conflict, transmission ratio distortion and cytonuclear interactions. We further highlight the close similarity between reported cases of outbreeding depression among conspecific populations, especially those that correspond to the intrinsic co-adaptation model, and the origin of genetic incompatibilities. This association holds great promise to help improve our understanding of the processes involved in the initial stage of speciation, and it highlights the close (and often overlooked) relationship between evolutionary and conservation biology

Unexpected ancestry of Populus seedlings from a hybrid zone implies a large role for postzygotic selection in the maintenance of species

In the context of potential interspecific gene flow, the integrity of species will be maintained by reproductive barriers that reduce genetic exchange, including traits associated with prezygotic isolation or poor performance of hybrids. Hybrid zones can be used to study the importance of different reproductive barriers, particularly when both parental species and hybrids occur in close spatial proximity. We investigated the importance of barriers to gene flow that act early versus late in the life cycle of European Populus by quantifying the prevalence of homospecific and hybrid matings within a mosaic hybrid zone. We obtained genotypic data for 11,976 loci from progeny and their maternal parents and constructed a Bayesian model to estimate individual admixture proportions and hybrid classes for sampled trees, and for the unsampled pollen parent. Matings that included one or two hybrid parents were common, resulting in admixture proportions of progeny that spanned the whole range of potential ancestries between the two parental species. This result contrasts strongly with the distribution of admixture proportions in adult trees, where intermediate hybrids and each of the parental species are separated into three discrete ancestry clusters. The existence of the full range of hybrids in seedlings is consistent with weak reproductive isolation early in the life cycle of Populus. Instead, a considerable amount of selection must take place between the seedling stage and maturity to remove many hybrid seedlings. Our results highlight that high hybridization rates and appreciable hybrid fitness do not necessarily conflict with the maintenance of species integrity

Mating system variation and assortative mating of sympatric bromeliads (Pitcairnia spp.) endemic to neotropical inselbergs

Premise of the study: The mating system is an important component of the complex set of reproductive isolation barriers causing plant speciation. However, empirical evidence showing that the mating system may promote reproductive isolation in co-occurring species is limited. The mechanisms by which the mating system can act as a reproductive isolation barrier are also largely unknown. Methods: Here we studied progeny arrays genotyped with microsatellites and patterns of stigma–anther separation (herkogamy) to understand the role of mating system shifts in promoting reproductive isolation between two hybridizing taxa with porous genomes, Pitcairnia albiflos and P. staminea (Bromeliaceae). Key results: In P. staminea, we detected increased selfing and reduced herkogamy in one sympatric relative to two allopatric populations, consistent with mating system shifts in sympatry acting to maintain the species integrity of P. staminea when in contact with P. albiflos. Conclusions: Mating system variation is a result of several factors acting simultaneously in these populations. We report mating system shifts as one possible reproductive barrier between these species, acting in addition to numerous other prezygotic (i.e., flower phenology and pollination syndromes) and postzygotic barriers (Bateson–Dobzhansky–Muller genetic incompatibilities)

Limited pollen flow and high selfing rates toward geographic range limit in an Atlantic forest bromeliad

Bromeliaceae is a Neotropical family that evolved ecological key innovations in association with extensive adaptive radiation. Its species present a variety of different mating system strategies varying within and among species, within genera and subfamilies. Also, species with a wide geographical range can display large variation in mating system, reproductive success and genetic diversity. Here we combined data from hand pollinations and genetic analysis to assess outcomes of contemporary gene flow and mating system variation at the range edge of Vriesea gigantea. Results from pollen germination rates showed that this species is cryptically self-incompatible. Hand-pollination experiments and genetic analysis of progeny arrays revealed that V. gigantea has a mixed mating system, with high selfing rates (s = 0.612), and high inbreeding coefficient (F = 0.372). Inbreeding in V. gigantea at southern edge of its distribution range was caused by high levels of selfing rather than by mating among relatives. Moreover, strong pollen pool genetic structure was observed (Φ’FT = 0.671), with an increase from north to south. The parameters observed help us to understand historical and ecological conditions under which V. gigantea has experienced moderate to high levels of selfing in the face of reduced pollen flow from central to peripheral populations due to recent southward range expansion

Pollen-pistil interactions and self-incompatibility in the Asteraceae: new insights from studies of Senecio squalidus (Oxford ragwort)

Background Pollen-pistil interactions are an essential prelude to fertilization in angiosperms and determine compatibility/incompatibility. Pollen-pistil interactions have been studied at a molecular and cellular level in relatively few families. Self-incompatibility (SI) is the best understood pollen-pistil interaction at a molecular level where three different molecular mechanisms have been identified in just five families. Here we review studies of pollen-pistil interactions and SI in the Asteraceae, an important family that has been relatively understudied in these areas of reproductive biology. Scope We begin by describing the historical literature which first identified sporophytic SI (SSI) in species of Asteraceae, the SI system later identified and characterized at a molecular level in the Brassicaceae. Early structural and cytological studies in these two families suggested that pollen-pistil interactions and SSI were similar, if not the same. Recent cellular and molecular studies in Senecio squalidus (Oxford ragwort) have challenged this belief by revealing that despite sharing the same genetic system of SSI, the Brassicaceae and Asteraceae molecular mechanisms are different. Key cellular differences have also been highlighted in pollen-stigma interactions, which may arise as a consequence of the Asteraceae possessing a ‘semi-dry' stigma, rather than the ‘dry' stigma typical of the Brassicaceae. The review concludes with a summary of recent transcriptomic analyses aimed at identifying proteins regulating pollen-pistil interactions and SI in S. squalidus, and by implication the Asteraceae. The Senecio pistil transcriptome contains many novel pistil-specific genes, but also pistil-specific genes previously shown to play a role in pollen-pistil interactions in other species. Conclusions Studies in S. squalidus have shown that stigma structure and the molecular mechanism of SSI in the Asteraceae and Brassicaceae are different. The availability of a pool of pistil-specific genes for S. squalidus offers an opportunity to elucidate the molecular mechanisms of pollen-pistil interactions and SI in the Asteracea

Genetic relationships and variation in reproductive strategies in four closely related bromeliads adapted to neotropical ‘inselbergs': Alcantarea glaziouana, A. regina, A. geniculata and A. imperialis (Bromeliaceae)

Background and Aims Bromeliads (Bromeliaceae) adapted to rock outcrops or ‘inselbergs' in neotropical rain forests have been identified as suitable plant models for studying population divergence and speciation during continental plant radiations. Little is known about genetic relationships and variation in reproductive strategies within and among inselberg-adapted species, yet knowledge of these parameters is important for understanding divergence processes and for conservation planning. Methods Nuclear microsatellites were used to assess the role of clonal reproduction, estimate genetic diversity and explore genetic relationships and variation in reproductive strategies for a total of 15 populations of four closely related Alcantarea inselberg species in south-eastern Brazil: A. glaziouana, A. regina, A. geniculata and A. imperialis. Key Results Clonal propagation is frequent in coastal populations of A. glaziouana and A. regina, but absent in the high-altitude species A. geniculata and A. imperialis. Considerable variation in clonal diversity, gene diversity (He), allelic richness, and Wright's inbreeding coefficient (FIS) exists within and between species of Alcantarea. A Bayesian analysis of coastal inselberg species indicated pronounced genetic structure. A neighbor-joining analysis grouped populations of each species together with moderate bootstrap support, except for the high altitude species A. imperialis. Conclusions The coastal inselberg species A. glaziouana and A. regina tend to propagate asexually via vegetative clonal growth, and both reproductive strategies and breeding systems vary greatly between populations and species of Alcantarea. The microsatellite data indicate a history of hybridization and reticulation involving the high-altitude species A. geniculata and A. imperialis in areas of co-occurrence. The results highlight the need to understand similarities and differences in reproductive strategies both within and between related species for conservation planning and as a basis for understanding evolutionary processes in tropical radiation

Causes and consequences of large clonal assemblies in a poplar hybrid zone

Asexual reproduction is a common and fundamental mode of reproduction in plants. Although persistence in adverse conditions underlies most known cases of clonal dominance, proximal genetic drivers remain unclear, in particular for populations dominated by a few large clones. In this study, we studied a clonal population of the riparian tree Populus alba in the Douro river basin (northwestern Iberian Peninsula) where it hybridizes with Populus tremula, a species that grows in highly contrasted ecological conditions. We used 73 nuclear microsatellites to test whether genomic background (species ancestry) is a relevant cause of clonal success, and to assess the evolutionary consequences of clonal dominance by a few genets. Additional genotyping-by-sequencing data were produced to estimate the age of the largest clones. We found that a few ancient (over a few thousand years old) and widespread genets dominate the population, both in terms of clone size and number of sexual offspring produced. Interestingly, large clones possessed two genomic regions introgressed from P. tremula, which may have favoured their spread under stressful environmental conditions. At the population level, the spread of large genets was accompanied by an overall ancient (>0.1 Myr) but soft decline of effective population size. Despite this decrease, and the high clonality and dominance of sexual reproduction by large clones, the Douro hybrid zone still displays considerable genetic diversity and low inbreeding. This suggests that even in extreme cases as in the Douro, asexual and sexual dominance of a few large, geographically extended individuals does not threaten population survival

Genetic structure and introgression in riparian populations of Populus alba L.

White poplar (Populus alba) is a widespread species of the northern hemisphere. Introgressed populations or hybrid zones with the related species of the European aspen (Populus tremula) have been suggested as potential venues for the identification of functionally important variation for germplasm conservation, restoration efforts and tree breeding. Data on the genetic diversity and structure of introgressed P. alba are available only for sympatric populations from central Europe. Here, clonality, introgression and spatial genetic patterns were evaluated in three riparian populations of P. alba along the Ticino, Paglia-Tevere and Cesano river drainages in Italy. Samples of all three populations were typed for five nuclear microsatellite markers and 137 polymorphic amplified fragment length polymorphisms. Microsatellite-based inbreeding co-efficients (FIS) were significantly positive in all three populations. Genetic diversity was consistently highest in Ticino, the population with the highest level of introgression from P. tremula. Population differentiation (FST) was low between the Ticino valley in northern Italy and the Cesano valley in central Italy and between the central Italian populations of Cesano and Paglia-Tevere, consistent with a role of the Appenine mountain range as a barrier to gene flow between adjacent drainage areas. Introgression was not the primary determinant of within-population spatial genetic structure (SGS) in the studied populations