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Until recently, our understanding of the genetics of speciation was limited to a narrow group of model species with a specific set of characteristics that made genetic analysis feasible. Rapidly advancing genomic technologies are eliminating many of the distinctions between laboratory and natural systems. In light of these genomic developments, we review the history of speciation genetics, advances that have been gleaned from model and non-model organisms, the current state of the field, and prospects for broadening the diversity of taxa included in future studies. Responses to a survey of speciation scientists across the world reveal the ongoing division between the types of questions that are addressed in model and non-model organisms. To bridge this gap, we suggest integrating genetic studies from model systems that can be reared in the laboratory or greenhouse with genomic studies in related non-models where extensive ecological knowledge exists., (Copyright © 2024 Cold Spring Harbor Laboratory Press; all rights reserved.)

High species richness and endemism in tropical mountains are recognized as major contributors to the latitudinal diversity gradient. The processes underlying mountain speciation, however, are largely untested. The prevalence of steep ecogeographic gradients and the geographic isolation of populations by topographic features are predicted to promote speciation in mountains. We evaluate these processes in a species-rich Neotropical genus of understory herbs that range from the lowlands to montane forests and have higher species richness in topographically complex regions. We ask whether climatic niche divergence, geographic isolation, and pollination shifts differ between mountain-influenced and lowland Amazonian sister pairs inferred from a 756-gene phylogeny. Neotropical Costus ancestors diverged in Central America during a period of mountain formation in the last 3 million years with later colonization of Amazonia. Although climatic divergence, geographic isolation, and pollination shifts are prevalent in general, these factors do not differ between mountain-influenced and Amazonian sister pairs. Despite higher climatic niche and species diversity in the mountains, speciation modes in Costus appear similar across regions. Thus, greater species richness in tropical mountains may reflect differences in colonization history, diversification rates, or the prevalence of rapidly evolving plant life forms, rather than differences in speciation mode., (© 2020 The Authors. Evolution © 2020 The Society for the Study of Evolution.)

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.)

The California Floristic Province exhibits one of the richest floras on the planet, with more than 5500 native plant species, approximately 40% of which are endemic. Despite its impressive diversity and the attention it has garnered from ecologists and evolutionary biologists, historical causes of species richness and endemism in California remain poorly understood. Using a phylogenetic analysis of 16 angiosperm clades, each containing California natives in addition to species found only outside California, we show that CA's current biodiversity primarily results from low extinction rates, as opposed to elevated speciation or immigration rates. Speciation rates in California were lowest among Arcto-Tertiary lineages (i.e., those colonizing California from the north, during the Tertiary), but extinction rates were universally low across California native plants of all historical, geographic origins. In contrast to long-accepted ideas, we find that California diversification rates were generally unaffected by the onset of the Mediterranean climate. However, the Mediterranean climate coincided with immigration of many desert species, validating one previous hypothesis regarding origins of CA's plant diversity. This study implicates topographic complexity and climatic buffering as key, long-standing features of CA's landscape favoring plant species persistence and diversification, and highlights California as an important refuge under changing climates., (© 2013 The Author(s). Evolution© 2013 The Society for the Study of Evolution.)

The importance of reinforcement, that is, natural selection that strengthens reproductive isolation between incipient species, remains controversial. We used two approaches to test for reinforcement in a species radiation of Neotropical gingers in the genus Costus. First, we conducted an intensive study of Costus pulverulentus and Costus scaber, two recently diverged species that co-occur and share hummingbird pollinators. The hummingbird pollinators transfer pollen between these Costus species, but hybrids are rarely found in nature. By performing pollinations between populations of C. pulverulentus and C. scaber from three sites across the species' geographic ranges, we find that pollen-pistil incompatibilities acting prior to fertilization have evolved only between locally sympatric populations, whereas geographically distant populations within the region of sympatry and allopatric populations remain fully interfertile. Second, we conducted a comparative study of isolating mechanisms across the genus. We find lower seed set due to pollen-pistil incompatibility between species pairs that co-occur and experience pollen transfer in nature compared to species pairs that are otherwise isolated, regardless of genetic distance. Taken together, these studies indicate that crossing barriers prevent potentially maladaptive hybridization and effectively reinforce the speciation process. Our results add to mounting evidence for reinforcement from animal studies and show that plant speciation may also involve complex mate recognition systems. Reinforcement may be particularly important in rapidly diverging lineages where ecological factors play a primary role in reproductive isolation, as may often be the case in tropical communities.

Empirical estimates of the relative importance of different barriers to gene flow between recently diverged species are important for understanding processes of speciation. I investigated the factors contributing to reproductive isolation between Costus pulverulentus and C. scaber (Costaceae), two closely related hummingbird-pollinated understory Neotropical herbs. I studied broad-scale geographic isolation, microhabitat isolation, flowering phenology, overlap in pollinator assemblages, floral constancy by pollinators, mechanical floral isolation, pollen-pistil interactions, seed set in interspecific crosses, and postzygotic isolation (hybrid seed germination, greenhouse survival to flowering, and pollen fertility). Aside from substantial geographic isolation, I found evidence for several factors contributing to reproductive isolation in the sympatric portion of their geographic ranges, but the identity and relative strength of these factors varied depending on the direction of potential gene flow. For C. pulverulentus as the maternal parent, mechanical floral isolation was the most important factor, acting as a complete block to interspecific pollen deposition. For C. scaber as the maternal parent, microhabitat isolation, pollinator assemblage, mechanical floral isolation, and postpollination pollen-pistil incompatibility were important. Overall, prezygotic barriers were found to be strong, resulting in 100% reproductive isolation for C. pulverulentus as the maternal parent and 99.0% reproductive isolation for C. scaber as the maternal parent. Some postzygotic isolation also was identified in the F1 generation, increasing total isolation for C. scaber to 99.4%. The results suggest that ecological factors, including habitat use and plant-pollinator interactions, contributed to speciation in this system and evolved before extensive intrinsic postzygotic isolation.

Budding speciation involves isolation of marginal populations at the periphery of a species range and is thought to be a prominent mode of speciation in organisms with low dispersal and/or strong local adaptation among populations. Budding speciation is typically evidenced by abutting, asymmetric ranges of ecologically divergent sister species and low genetic diversity in putative budded species. Yet these indirect patterns may be unreliable, instead caused by postspeciation processes such as range or demographic shifts. Nested phylogenetic relationships provide the most conclusive evidence of budding speciation. A putative case of budding speciation in the serpentine endemic Clarkia franciscana and two closely related widespread congeners was studied by Harlan Lewis, Peter Raven, Leslie Gottlieb, and others over a 20-year period, yet the origin of C. franciscana remains controversial. Here, we reinvestigate this system with phylogenomic analyses to determine whether C. franciscana is a recently derived budded species, phylogenetically nested within one of the other two putative progenitor species. In contrast to the hypothesized pattern of relatedness among the three Clarkia species, we find no evidence for recent budding speciation. Instead, the data suggest the three species diverged simultaneously. We urge caution in using contemporary range patterns to infer geographic modes of speciation.

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 aimsUnder 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.MethodsFirst, 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 resultsAlthough 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.ConclusionsAlthough 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.

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]