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The significance of prezygotic isolation for speciation has been recognized at least since the Modern Synthesis. However, fundamental questions remain. For example, how are genetic associations between traits that contribute to prezygotic isolation maintained? What is the source of genetic variation underlying the evolution of these traits? And how do prezygotic barriers affect patterns of gene flow? We address these questions by reviewing genetic features shared across plants and animals that influence prezygotic isolation. Emerging technologies increasingly enable the identification and functional characterization of the genes involved, allowing us to test established theoretical expectations. Embedding these genes in their developmental context will allow further predictions about what constrains the evolution of prezygotic isolation. Ongoing improvements in statistical and computational tools will reveal how pre- and postzygotic isolation may differ in how they influence gene flow across the genome. Finally, we highlight opportunities for progress by combining theory with appropriate data., (Copyright © 2024 Cold Spring Harbor Laboratory Press; all rights reserved.)

Understanding the relative importance of reproductive isolating mechanisms across the speciation continuum remains an outstanding challenge in evolutionary biology. Here, we examine a common isolating mechanism, reproductive phenology, between plant sister taxa at different stages of adaptive divergence to gain insight into its relative importance during speciation. We study 17 plant taxa that have independently adapted to inhospitable serpentine soils, and contrast each with a nonserpentine sister taxon to form pairs at either ecotypic or species-level divergence. We use greenhouse-based reciprocal transplants in field soils to quantify how often flowering time (FT) shifts accompany serpentine adaptation, when FT shifts evolve during speciation, and the genetic versus plastic basis of these shifts. We find that genetically based shifts in FT in serpentine-adapted taxa are pervasive regardless of the stage of divergence. Although plasticity increases FT shifts in five of the pairs, the degree of plasticity does not differ when comparing ecotypic versus species-level divergence. FT shifts generally led to significant, but incomplete, reproductive isolation that did not vary in strength by stage of divergence. Our work shows that adaptation to a novel habitat may predictably drive phenological isolation early in the speciation process.

Background and Aims: Under a widely accepted model of pollinator-driven speciation, geographic variation in pollinator assemblage drives floral divergence and automatically causes reproductive isolation. Yet it is unclear whether divergent floral adaptation initially confers strong reproductive isolation, or whether that comes at later stages of speciation and requires other forms of reproductive isolation. This study uses a pair of recently diverged, interfertile and parapatric species in the genus Clarkia to determine whether adaptation to hawkmoths, a novel pollinator functional group, would automatically confer floral isolation upon sympatric contact., Methods: First, genetically based differences in floral traits between C. breweri and C. concinna that would be maintained upon migration are quantified. Then scenarios of experimental sympatry are constructed in which arrays of flowers are exposed to the novel pollinator, the hawkmoth Hyles lineata, and pollinator preference and heterospecific pollen transfer are assessed. Source populations from across the ranges of each species are used to understand how geographic variation in floral traits within species may affect floral isolation., Key Results: Although H. lineata has never been observed visiting C. concinna in the wild, it regularly moves between species in experimental floral arrays. Hawkmoth preference and heterospecific pollen transfer vary both among moths and among geographic source locations of C. concinna. The strength of floral isolation in this system is related to variation in flower size, especially hypanthium tube width, and nectar reward among C. concinna forms., Conclusions: Although C. breweri has adopted a novel hawkmoth pollination system, both ethological and mechanical floral isolation by hawkmoths are incomplete and vary according to the specific phenotype of the C. concinna source population. The results suggest that strong floral isolation is not automatically conferred by a pollinator shift and may require additional evolution of deterrent floral traits and habitat isolation that reduces the immediate spatial co-occurrence of young species.

Speciation involves the evolution of traits and genetic differences that contribute to reproductive isolation and the cessation of gene flow, and studying closely related species and divergent populations gives insight into how these phenomena proceed. Here, we document patterns of gene flow within and between two members of a rapid Neotropical species radiation, Costus pulverulentus and Costus scaber (Costaceae). These species co-occur in the tropical rainforest and share pollinators, but are reproductively isolated by a series of prezygotic barriers, some of which show evidence of reinforcement at sympatric sites. Here, we genotype microsatellite markers in plants from eight sites that span the geographical range of both species, including four sympatric sites. We also genotype putative hybrids found at two sympatric sites. We find high levels of genetic isolation among populations within each species and low but detectable levels of introgression between species at sympatric sites. Putative hybrids identified by morphology are consistent with F1 or more advanced hybrids. Our results highlight the effectiveness of prezygotic isolating mechanisms at maintaining species boundaries in young radiations and provide empirical data on levels of gene flow consistent with reinforcement., (© 2013 John Wiley & Sons Ltd.)

Trade-offs are crucial for species divergence and reproductive isolation. Trade-offs between investment in growth versus defense against herbivores are implicated in tropical forest diversity. Empirically exploring the role of growth-defense trade-offs in closely related species' reproductive isolation can clarify the eco-evolutionary dynamics through which growth-defense trade-offs contribute to diversity. Costus villosissimus and C. allenii are recently diverged, interfertile, and partially sympatric neotropical understory plant species primarily isolated by divergent habitat adaptation. This divergent adaptation involves differences in growth rate, which may constrain investment in defense. Here, we investigate growth-defense trade-offs and how they relate to the divergent habitat adaptation that isolates these species. We characterize leaf toughness and chemistry, evaluate the feeding preferences of primary beetle herbivores in controlled trials and field-based experiments, and investigate natural herbivory patterns. We find clear trade-offs between growth and defense: slower-growing C. allenii has tougher leaves and higher defensive chemical concentrations than faster-growing C. villosissimus. Costus villosissimus has rapid growth-based drought avoidance, enabling growth in drier habitats with few specialist herbivores. Therefore, growth-defense trade-offs mediate synergistic biotic and abiotic selection, causing the divergent habitat adaptation that prevents most interspecific mating between C. villosissimus and C. allenii. Our findings advance understanding of ecological speciation by highlighting the interplay of biotic and abiotic selection that dictates the outcome of trade-offs.

Understanding the relative importance of reproductive isolating mechanisms across the speciation continuum remains an outstanding challenge in evolutionary biology. Here, we examine a common isolating mechanism, reproductive phenology, between plant sister taxa at different stages of adaptive divergence to gain insight into its relative importance during speciation. We study 17 plant taxa that have independently adapted to inhospitable serpentine soils, and contrast each with a nonserpentine sister taxon to form pairs at either ecotypic or species-level divergence. We use greenhouse-based reciprocal transplants in field soils to quantify how often flowering time (FT) shifts accompany serpentine adaptation, when FT shifts evolve during speciation, and the genetic versus plastic basis of these shifts. We find that genetically based shifts in FT in serpentine-adapted taxa are pervasive regardless of the stage of divergence. Although plasticity increases FT shifts in five of the pairs, the degree of plasticity does not differ when comparing ecotypic versus species-level divergence. FT shifts generally led to significant, but incomplete, reproductive isolation that did not vary in strength by stage of divergence. Our work shows that adaptation to a novel habitat may predictably drive phenological isolation early in the speciation process.

Reproductive isolation is critical to the diversification of species. Postpollination barriers may be important in limiting gene flow between closely related species, but they are relatively cryptic and their evolution is poorly understood. Here, we review the role of postpollination reproductive isolation in plants, including the various stages at which it operates and the hypotheses for how it may evolve. We then review empirical studies in the plant genus Costus, evaluating documented postpollination barriers in light of these hypotheses. We summarize isolation due to parental style length differences and present evidence supporting the hypothesis that the differences are in part a by-product of selection on floral morphology. Additionally, we show that reduced pollen adhesion, germination, and tube growth contribute to reproductive isolation between two closely related sympatric species of Costus. Geographic variation in the strength of these crossing barriers supports the hypothesis that they evolved under reinforcement, or direct natural selection to strengthen isolation.

Floral divergence can contribute to reproductive isolation among plant lineages, and thus provides an opportunity to study the genetics of speciation, including the number, effect size, mode of action and interactions of quantitative trait loci (QTL). Moreover, flowers represent suites of functionally interrelated traits, but it is unclear to what extent the phenotypic integration of the flower is underlain by a shared genetic architecture, which could facilitate or constrain correlated evolution of floral traits. Here, we examine the genetic architecture of floral morphological traits involved in an evolutionary switch from bill to forehead pollen placement between two species of hummingbird‐pollinated Neotropical understorey herbs that are reproductively isolated by these floral differences. For the majority of traits, we find multiple QTL of relatively small effect spread throughout the genome. We also find substantial colocalization and alignment of effects of QTL underlying different floral traits that function together to promote outcrossing and reduce heterospecific pollen transfer. Our results are consistent with adaptive pleiotropy or linkage of many co‐adapted genes, either of which could have facilitated a response to correlated selection and helped to stabilize divergent phenotypes in the face of low levels of hybridization. Moreover, our results indicate that floral mechanical isolation can be consistent with an infinitesimal model of adaptation. see also the Perspective by Carolyn A. Wessinger [ABSTRACT FROM AUTHOR]

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Premise: Ecogeographic isolation, or geographic isolation caused by ecological divergence, is thought to be of primary importance in speciation, yet is difficult to demonstrate and quantify. To determine whether distributions are limited by divergent adaptation or historical contingency, the gold standard is to reciprocally transplant species between their geographic ranges. Alternatively, ecogeographic isolation is inferred from species distribution models and niche divergence tests using widely available environmental and occurrence data. Methods: We tested for ecogeographic isolation between two sister species of California annual wildflowers, Clarkia concinna and C. breweri, with a hybrid approach. We used niche models to predict water availability as the major axis of ecological divergence and then tested that with a greenhouse experiment. Specifically, we manipulated water availability in field soils for two populations of each species and predicted higher fitness in conditions representing home habitats to those representing the environment of each's sister species. Results: Water availability and soil representing C. concinna generally increased both species' fitness. Thus, water and soil may indeed limit C. concinna from colonizing the range of C. breweri, but not vice versa. We suggest that the competitive environment and pollinator availability, which are not directly captured with either approach, may be key biotic factors correlated with climate that contribute to unexplained ecogeographic isolation for C. breweri. Conclusions: Ours is a valuable approach to assessing ecogeographic isolation, in that it balances feasibility with model validation, and our results have implications for species distribution modeling efforts geared toward predicting climate change responses. [ABSTRACT FROM AUTHOR]

Summary Hybridization is increasingly recognized as an important evolutionary process across the tree of life. In many clades, phylogenomic approaches have permitted unparalleled insight into the extent and frequency of hybridization. However, we continue to lack a deep understanding of the factors that limit and shape patterns of hybridization, especially in evolutionary radiations. In this study, we characterized patterns of introgression across Costus (Costaceae), a young evolutionary radiation of tropical understory plants that maintain widespread interfertility despite exhibiting strong prezygotic reproductive isolation. We analyzed a phylogenomic dataset of 756 genes from 54 Costus species using multiple complementary approaches – D‐statistics, gene‐tree‐based tests, and phylogenetic network analyses – to detect and characterize introgression events throughout the evolutionary history of the radiation. Our results identified a moderate number of introgression events, including a particularly ancient, well‐supported event spanning one of the deepest divergences in the clade. Most introgression events occurred between taxa or ancestral lineages that shared the same pollination syndrome (bee‐pollinated or hummingbird‐pollinated). These findings suggest that prezygotic barriers, including pollinator specialization, have been key to the balance between introgression and reproductive isolation in Costus. [ABSTRACT FROM AUTHOR]

Abstract: Ecological differentiation and genetic isolation are thought to be critical in facilitating coexistence between related species, but the relative importance of these phenomena and the interactions between them are not well understood. Here, we examine divergence in abiotic habitat affinity and the extent of hybridization and introgression between two rare species of Monardella (Lamiaceae) that are both restricted to the same serpentine soil exposure in California. Although broadly sympatric, they are found in microhabitats that differ consistently in soil chemistry, slope, rockiness and vegetation. We identify one active hybrid zone at a site with intermediate soil and above‐ground characteristics, and we document admixture patterns indicative of extensive and asymmetric introgression from one species into the other. We find that genetic distance among heterospecific populations is related to geographic distance, such that the extent of apparent introgression is partly explained by the spatial proximity to the hybrid zone. Our work shows that plant species can maintain morphological and ecological integrity in the face of weak genetic isolation, intermediate habitats can facilitate the establishment of hybrids, and that the degree of apparent introgression a population experiences is related to its geographic location rather than its local habitat characteristics. [ABSTRACT FROM AUTHOR]

Although animal pollination is often proposed as a major driver of floral divergence, questions remain about its importance in plant speciation. One issue is whether pollinator specialization, traditionally thought necessary for floral isolation, is prevalent enough to have played a major role in speciation. Furthermore, the ecological and geographic scenarios under which pollinator transitions occur are poorly understood, and the underlying genetic factors are just beginning to be uncovered for a few systems. Nevertheless, macroevolutionary studies consistently show that transitions to animal pollination are accompanied by an increase in diversification rate. Here we consider several models and diverse empirical data on how pollinators could influence speciation. We conclude that floral isolation is rarely, if ever, sufficient to cause speciation on its own, but that it acts synergistically with other isolating mechanisms. A more comprehensive approach is the key to an improved understanding of the role of pollinators in angiosperm speciation. [ABSTRACT FROM AUTHOR]

Costus flammulus is a new herbaceous species endemic to montane cloud forests of the volcanic cordilleras in northern Costa Rica. Costus flammulus has been mistaken for C. wilsonii, but phylogenetic evidence demonstrates that it is closely related to the widespread lowland species C. pulverulentus. Here, we use an integrated framework of species concepts to evaluate whether C. flammulus and C. pulverulentus are distinct species. First, we re-evaluate prior phylogenetic analyses to assess whether C. flammulus bifurcated from or budded off from within C. pulverulentus and whether C. flammulus is monophyletic. We then compare phenotypic traits to determine which diagnostic vegetative and inflorescence traits can be used to identify species in herbarium specimens and examine whether floral traits may confer floral isolation. We compare pollinator assemblages to examine whether pollinator specificity may contribute to reproductive isolation. Finally, we model species distributions and climatic niche overlap to assess ecogeographic isolation. We found that C. flammulus is a monophyletic species phenotypically, ecologically, and geographically distinct from C. pulverulentus and may have speciated as a peripheral isolate at the high elevation range edge of C. pulverulentus. Several lines of evidence, such as C. pulverulentus paraphyly, range size asymmetry, and C. flammulus' nested distribution and vegetative traits, suggest that C. flammulus budded off from a C. pulverulentus-like progenitor species, evolving to tolerate a colder and more seasonal montane environment. [ABSTRACT FROM AUTHOR]