Components Of Reproductive Isolation Research Articles

Reproductive barriers and genetic differentiation between continental and island populations of Epidendrum fulgens (Orchidaceae)

Studies on insular organisms provide an important framework for investigating patterns of genetic differentiation and reproductive isolation. By focusing on populations of the same species, we have the opportunity to study the mechanisms operating during the earliest stages of speciation, as reproductive barriers can be examined among divergent lineages in a geographic context. We investigated the genetic differentiation and the evolution of early stages of intrinsic postmating reproductive isolation between continental and insular populations of Epidendrum fulgens, a neotropical orchid distributed in southeastern Brazil. Genetic diversity and structure were estimated for both nuclear and plastid markers by using genetic differentiation measures and model-based assignment test. Furthermore, two components of reproductive isolation were examined by analyzing fruit set and seed viability in interpopulation crosses. Strong plastid genetic structure (FST = 0.679) was found between insular and remaining populations, indicating that E. fulgens reduced gene flow via seed dispersal, although significant nuclear genetic structure was lower (DST = 0.179), likely due to the smaller effective population size of the plastid genome. Significant differences in seed viability between self- and cross-pollinated plants were found, indicating the occurrence of inbreeding depression in all populations. Seed viability was significantly lower in crosses between insular and remaining populations, suggesting a late postzygotic reproductive barrier due to low migration associated with genetic drift (i.e., bottleneck) and its consequences. Our results confirm the importance of islands as drivers for populational differentiation and suggest a central role for outbreeding depression during the early stages of lineage diversification.

Studies on Mating Preference and Productivity in Drosophila ananassae and D. pallidosa and Their Hybrids

During speciation different kinds of reproductive barriers originate to preclude gene flow between diverging populations. Reproductive isolation or barriers to gene flow can be categorized by the temporal nature of their effect: pre-zygotic barriers occur before fertilization and post-zygotic barriers occur after fertilization. In this study, we studied each components of reproductive isolation between D. ananassae and D. pallidosa, including both pre-zygotic and post-zygotic barriers. Because it might be possible that by dissecting these barriers one can get the answers of many unresolved questions related to the process of speciation of these two sibling species. We reported premating isolation because females of both D. ananassae and D. pallidosa were more discriminative for mating against the alien males rather than conspecific males, and this discrimination was much stronger in case of D. ananassae females for being the ancestral and cosmopolitan species. We also did not find any decrease in the production of progeny or viable offspring in comparison to conspecific males, indicating a lack of postmating prezygotic isolating barriers. Further, there is no complete lack of intrinsic post-zygotic isolation between these species or not complete presence of post-zygotic isolation, as both the hybrid sons were producing less number of progeny in comparison to all the crosses but it is near to significant but not significant and this is contrasting to the results of a previous study.

Impact of pre- and post-pollination barriers on pollen transfer and reproductive isolation among three sympatric Pedicularis (Orobanchaceae) species.

Pedicularis is the largest genus in the Orobanchaceae (>300) with many species co-occurring and co-blooming in subalpine to alpine meadows in the Himalayas. Although it is well known that different Pedicularis species place pollen on different parts of the same bumblebee's body, thus reducing interspecific pollen transfer, it is not known whether post-pollination components also contribute to reproductive isolation (RI). In this study, we quantified the individual strengths and absolute contributions of six pre- and post-pollination components of RI between three sympatric species in two pairs; Pedicularis gruina×Pedicularis tenuisecta (gru×ten) and Pedicularis comptoniifolia×Pedicularis tenuisecta (com×ten). All three Pedicularis species shared the same Bombus species. Individual foragers showed a high, but incomplete, floral constancy for each species. Therefore, pre-pollination barriers were potentially 'leaky' as Bombus species showed a low but consistent frequency of interspecific visitation. The RI strength of pre-pollination was lower in com×ten than in gru×ten. In contrast, post-pollination barriers completely blocked gene flow between both sets of species pairs. Two post-pollination recognition sites were identified. Late acting rejection of interspecific pollen tube growth occurred in com♀×ten♂, while seeds produced in bi-directional crosses of gru×ten failed to germinate. We propose that, although floral isolation based on pollen placement on pollinators in the genus Pedicularis is crucial to avoid interspecific pollen transfer, the importance of this mode of interspecific isolation may be exaggerated. Post-pollination barriers may play even larger roles for currently established populations of co-blooming and sympatric species in this huge genus in the Himalayas.

Female Choice Undermines the Emergence of Strong Sexual Isolation between Locally Adapted Populations of Atlantic Mollies (Poecilia mexicana).

Divergent selection between ecologically dissimilar habitats promotes local adaptation, which can lead to reproductive isolation (RI). Populations in the Poecilia mexicana species complex have independently adapted to toxic hydrogen sulfide and show varying degrees of RI. Here, we examined the variation in the mate choice component of prezygotic RI. Mate choice tests across drainages (with stimulus males from another drainage) suggest that specific features of the males coupled with a general female preference for yellow color patterns explain the observed variation. Analyses of male body coloration identified the intensity of yellow fin coloration as a strong candidate to explain this pattern, and common-garden rearing suggested heritable population differences. Male sexual ornamentation apparently evolved differently across sulfide-adapted populations, for example because of differences in natural counterselection via predation. The ubiquitous preference for yellow color ornaments in poeciliid females likely undermines the emergence of strong RI, as female discrimination in favor of own males becomes weaker when yellow fin coloration in the respective sulfide ecotype increases. Our study illustrates the complexity of the (partly non-parallel) pathways to divergence among replicated ecological gradients. We suggest that future work should identify the genomic loci involved in the pattern reported here, making use of the increasing genomic and transcriptomic datasets available for our study system.

Components of reproductive isolation between the closely related grasshopper species Chorthippus biguttulus and C. mollis

The formation and maintenance of species in nature is accomplished by the evolution of reproductive isolating mechanisms. To understand patterns of speciation and coexistence between species, it is crucial to obtain a complete synopsis of reproductive isolating barriers. We identified multiple reproductive isolation barriers between two closely related species, Chorthippus biguttulus and Chorthippus mollis, and quantified their respective contributions to isolation. To this end, we produced hybrids and backcrosses in the laboratory to examine reproductive isolation at multiple stages in the life history. The prezygotic barriers, based on chemical and acoustic cues, are currently the strongest impediments to gene flow between C. biguttulus and C. mollis. This indicates an important role for sexual selection in the maintenance of species isolation. However, extrinsic and intrinsic postzygotic isolation barriers also contributed to reproductive isolation. The virtual sterility of F1 hybrid males was based on both the dysfunctionality of their testes and intermediate behavioral mating traits (behavioral sterility). This study demonstrates that a cascade of reproductive isolating mechanisms reduces the gene flow between C. biguttulus and C. mollis. Our results further demonstrate that the courtship display in these species consists of multimodal signals and indicates a key role of chemical cues in reproductive isolation and speciation in grasshoppers. The identification of species isolating mechanisms is essential for understanding the processes that drive speciation. A profound understanding of reproductive isolating mechanisms and their fitness consequences in a system is required to predict a specific speciation scenario. Members of the grasshopper subfamily Gomphocerinae show an enormous diversity and complexity in courtship behavior, especially in acoustic displays. Here, we demonstrate that non-acoustic and postzygotic isolation mechanisms also strongly contribute to reproductive isolation between the closely related grasshopper species, C. biguttulus and C. mollis. In addition, our results suggest that ongoing gene flow between this species pair is unlikely and that sexual selection plays an important role in the maintenance of species isolation.

Genetic mapping of two components of reproductive isolation between two sibling species of moths, Ostrinia nubilalis and O. scapulalis

We report the quantitative trait loci (QTL) mapping of reproductive isolation traits between Ostrinia nubilalis (the European corn borer) and its sibling species O. scapulalis (the Adzuki bean borer), focusing on two traits: mating isolation (mi) and pheromone production (Pher). Four genetic maps were generated from two backcross families, with two maps (one chromosomal map and one linkage map) per backcross. We located 165-323 AFLP markers on these four maps, resulting in the identification of 27-31 linkage groups, depending on the map considered. No-choice mating experiments with the offspring of each backcross led to the detection of at least two QTLs for mi in different linkage groups. QTLs underlying Pher were located in a third linkage group. The Z heterochromosome was identified by a specific marker (Tpi) and did not carry any of these QTLs. Finally, we considered the global divergence between the two sibling species, distortions of segregation throughout the genome, and the location and effect of mi and Pher QTLs in light of the known candidate genes for reproductive isolation within the genus Ostrinia and, more broadly, in phytophagous insects.

COMPONENTS OF REPRODUCTIVE ISOLATION BETWEEN ORCHIS MASCULA AND ORCHIS PAUCIFLORA

Studies of the strength and nature of reproductive isolation (RI) between species can greatly contribute to our understanding of speciation. Although the role of RI in speciation is well recognized, there is a dearth of information on the contributions of different barriers between related plant species. Here, we estimated multiple components of RI between two Mediterranean orchid sister species (Orchis mascula and Orchis pauciflora), disentangling the strength and absolute contributions of seven different isolating mechanisms. Our survey includes one prepollination, two postpollination prezygotic (pollen-stigma incompatibility, conspecific pollen precedence), two intrinsic postzygotic (embryo mortality and hybrid sterility) and two extrinsic postzygotic (hybrid habitat differentiation and hybrid pollination) isolating mechanisms. We found strong RI between the investigated species, although none of the barriers were able to completely impede gene flow. Five isolating mechanisms contributed positively to the maintenance of species boundaries. Contrary to most surveys of isolating mechanisms, our data speak against a clear predominance of prepollination or of prezygotic barriers but confirm the emerging pattern of multiple barriers contributing to the maintenance of species integrity. These findings suggest an allopatric condition during early phases of species divergence. We discuss our data in the wider context of previous studies carried out in this orchid group by using a comparative approach.

Pulling together or pulling apart: hybridization in theory and practice

Pulling together or pulling apart: hybridization in theory and practice

Genomics of isolation in hybrids

Hybrid zones are common in nature and can offer critical insights into the dynamics and components of reproductive isolation. Hybrids between diverged lineages are particularly informative about the genetic architecture of reproductive isolation, because introgression in an admixed population is a direct measure of isolation. In this paper, we combine simulations and a new statistical model to determine the extent to which different genetic architectures of isolation leave different signatures on genome-level patterns of introgression. We found that reproductive isolation caused by one or several loci of large effect caused greater heterogeneity in patterns of introgression than architectures involving many loci with small fitness effects, particularly when isolating factors were closely linked. The same conditions that led to heterogeneous introgression often resulted in a reasonable correspondence between outlier loci and the genetic loci that contributed to isolation. However, demographic conditions affected both of these results, highlighting potential limitations to the study of the speciation genomics. Further progress in understanding the genomics of speciation will require large-scale empirical studies of introgression in hybrid zones and model-based analyses, as well as more comprehensive modelling of the expected levels of isolation with different demographies and genetic architectures of isolation.

A framework for comparing processes of speciation in the presence of gene flow

How common is speciation-with-gene-flow? How much does gene flow impact on speciation? To answer questions like these requires understanding of the common obstacles to evolving reproductive isolation in the face of gene flow and the factors that favour this crucial step. We provide a common framework for the ways in which gene flow opposes speciation and the potential conditions that may ease divergence. This framework is centred on the challenge shared by most scenarios of speciation-with-gene-flow, i.e. the need for coupling among different components of reproductive isolation. Using this structure, we review and compare the factors favouring speciation with the intention of providing a more integrated picture of speciation-with-gene-flow.

Relationship between genetic distances and postzygotic reproductive isolation in diploid Fragaria (Rosaceae)

Studies of reproductive isolation are important for understanding speciation and species delimitation. We studied seven components of reproductive isolation at different taxonomic and geographical levels and their relationship with genetic distance in diploid Fragaria. Isolation was only evident between different taxa at later stages (post F1 survivorship), and not at the earlier ones of fruit and seed set, F1 seed germination, and survivorship. Within Fragaria vesca, isolation at the later stages was positively correlated with genetic distance, although this was not found at interspecific levels. The lack of isolation between F. vesca and the other species at the early stages provide the chance for hybrid formation, although high levels of infertility expressed among the offspring can lead to potentially opposing evolutionary outcomes. Within F. vesca, there was evidence of unexpected isolation promoting evolutionary diversification and incipient speciation. Reproductive isolation values between sympatric and allopatric species pairs were similar and indicate a lack of reinforcement in Fragaria. This, combined with the lack of correlation between genetic distance and isolation at interspecific levels, shows that genetic distance is not always proportionally correlated with the degree of isolation in plants and suggests that evolutionary processes may be playing differently in plants compared to animals. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 510–526.

Defensin-Like ZmES4 Mediates Pollen Tube Burst in Maize via Opening of the Potassium Channel KZM1

Author SummarySperm cells of animals and lower plants are mobile and can swim to the oocyte or egg cell. In contrast, flowering plants generate immobile sperm encased in a pollen coat to protect them from drying out and are transported via the pollen tube cell towards the egg apparatus to achieve double fertilization. Upon arrival the pollen tube tip bursts to deliver two sperm cells, one fusing with the egg cell to generate the embryo and the other fusing with the central cell to generate the endosperm. Here, we report the mechanisms leading to pollen tube burst and sperm discharge in maize. We found that before fertilization the defensin-like protein ZmES1-4 is stored in the secretory zone of the egg apparatus cells and that pollen tubes cannot discharge sperm in ZmES1-4 knock-down plants. Application of chemically synthesized ZmES4 leads to pollen tube burst within seconds in maize, but not in other plant species, suggesting this mechanism may be species specific. Finally, we identified the pollen tube-expressed potassium channel KZM1 as a target of ZmES4, which opens after ZmES4 treatment and probably leads to K+ influx and sperm release after osmotic burst.

Components of reproductive isolation between North American pheromone strains of the European corn borer.

Of 12 potential reproductive isolating barriers between closely related Z- and E-pheromone strains of the European corn borer moth (Ostrinia nubilalis), seven significantly reduced gene flow but none were complete, suggesting that speciation in this lineage is a gradual process in which multiple barriers of intermediate strength accumulate. Estimation of the cumulative effect of all barriers resulted in nearly complete isolation (>99%), but geographic variation in seasonal isolation allowed as much as approximately 10% gene flow. With the strongest barriers arising from mate-selection behavior or ecologically relevant traits, sexual and natural selection are the most likely evolutionary processes driving population divergence. A recent multilocus genealogical study corroborates the roles of selection and gene flow (Dopman et al. 2005), because introgression is supported at all loci besides Tpi, a sex-linked gene. Tpi reveals strains as exclusive groups, possesses signatures of selection, and is tightly linked to a QTL that contributes to seasonal isolation. With more than 98% of total cumulative isolation consisting of prezygotic barriers, Z and E strains of ECB join a growing list of taxa in which species boundaries are primarily maintained by the prevention of hybridization, possibly because premating barriers evolve during early stages of population divergence.

THE EVOLUTION OF STRONG REPRODUCTIVE ISOLATION

Felsenstein distinguished two ways by which selection can directly strengthen isolation. First, a modifier that strengthens prezygotic isolation can be favored everywhere. This fits with the traditional view of reinforcement as an adaptation to reduce deleterious hybridization by strengthening assortative mating. Second, selection can favor association between different incompatibilities, despite recombination. We generalize this "two allele" model to follow associations among any number of incompatibilities, which may include both assortment and hybrid inviability. Our key argument is that this process, of coupling between incompatibilities, may be quite different from the usual view of reinforcement: strong isolation can evolve through the coupling of any kind of incompatibility, whether prezygotic or postzygotic. Single locus incompatibilities become coupled because associations between them increase the variance in compatibility, which in turn increases mean fitness if there is positive epistasis. Multiple incompatibilities, each maintained by epistasis, can become coupled in the same way. In contrast, a single-locus incompatibility can become coupled with loci that reduce the viability of haploid hybrids because this reduces harmful recombination. We obtain simple approximations for the limits of tight linkage, and strong assortment, and show how assortment alleles can invade through associations with other components of reproductive isolation.

Evolution of reproductive isolation in plants

Reproductive isolation is essential for the process of speciation and much has been learned in recent years about the ecology and underlying genetics of reproductive barriers. But plant species are typically isolated not by a single factor, but by a large number of different pre- and postzygotic barriers, and their potentially complex interactions. This phenomenon has often been ignored to date. Recent studies of the relative importance of different isolating barriers between plant species pairs concluded that prezygotic isolation is much stronger than postzygotic isolation. But studies of the patterns of reproductive isolation in plants did not find that prezygotic isolation evolves faster than postzygotic isolation, in contrast to most animals. This may be due to the multiple premating barriers that isolate most species pairs, some of which may be controlled by few genes of major effect and evolve rapidly, whereas others have a complex genetic architecture and evolve more slowly. Intrinsic postzygotic isolation in plants is correlated with genetic divergence, but some instrinsic postzygotic barriers evolve rapidly and are polymorphic within species. Extrinsic postzygotic barriers are rarely included in estimates of different components of reproductive isolation. Much remains to be learned about ecological and molecular interactions among isolating barriers. The role of reinforcement and reproductive character displacement in the evolution of premating barriers is an open topic that deserves further study. At the molecular level, chromosomal and genic isolation factors may be associated and act in concert to mediate reproductive isolation, but their interactions are only starting to be explored.

Sympatric, parapatric or allopatric: the most important way to classify speciation?

The most common classification of modes of speciation begins with the spatial context in which divergence occurs: sympatric, parapatric or allopatric. This classification is unsatisfactory because it divides a continuum into discrete categories, concentrating attention on the extremes, and it subordinates other dimensions on which speciation processes vary, such as the forces driving differentiation and the genetic basis of reproductive isolation. It also ignores the fact that speciation is a prolonged process that commonly has phases in different spatial contexts. We use the example of local adaptation and partial reproductive isolation in the intertidal gastropod Littorina saxatilis to illustrate the inadequacy of the spatial classification of speciation modes. Parallel divergence in shell form in response to similar environmental gradients in England, Spain and Sweden makes this an excellent model system. However, attempts to demonstrate 'incipient' and 'sympatric' speciation involve speculation about the future and the past. We suggest that it is more productive to study the current balance between local adaptation and gene flow, the interaction between components of reproductive isolation and the genetic basis of differentiation.

Components of reproductive isolation and their role in speciation between Jamesbrittenia racemosa and J. pedunculosa (Manuleae)

Components of reproductive isolation and their role in speciation between Jamesbrittenia racemosa and J. pedunculosa (Manuleae)

Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa.

To what degree is the divergent adaptation responsible for life's phenotypic variety also responsible for generating the millions of species that manifest this variation? Theory predicts that ecological divergence among populations should promote reproductive isolation, and recent empirical studies provide support for this hypothesis in a limited number of specific taxa. However, the essential question of whether ecology plays a truly general role in speciation has yet to be systematically evaluated. Here we address this integral issue using an approach that adds an ecological dimension to comparative studies investigating the relationship between reproductive isolation and divergence time. Specifically, we quantify ecological divergence for >500 species pairs from eight plant, invertebrate, and vertebrate taxa and statistically isolate its association with reproductive isolation. This approach demonstrates a highly consistent and significant positive association between ecological divergence and reproductive isolation across taxa. This relationship was also observed across different aspects of ecological divergence and components of reproductive isolation. These findings are highly consistent with the hypothesis that ecological adaptation plays a fundamental and taxonomically general role in promoting reproductive isolation and speciation.

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.