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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.

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.

Different populations of plant species can adapt to their local pollinators and diverge in floral traits accordingly. Floral traits are subject to pollinator-driven natural selection to enhance plant reproductive success. Studies on temperate plant systems have shown pollinator-driven selection results in floral trait variation along elevational gradients, but studies in tropical systems are lacking. We analyzed floral traits and pollinator assemblages in the Neotropical bee-pollinated taxon Costus guanaiensis var. tarmicus across four sites along a steep elevational gradient in Peru. We found variations in floral traits of size, color, and reward, and in the pollinator assemblage along the elevational gradient. We examined our results considering two hypotheses, (1) local adaptation to different bee assemblages, and (2) the early stages of an evolutionary shift to a new pollinator functional group (hummingbirds). We found some evidence consistent with the adaptation of C. guanaiensis var. tarmicus to the local bee fauna along the studied elevational gradient. Corolla width across sites was associated with bee thorax width of the local most frequent pollinator. However, we could not rule out the possibility of the beginning of a bee-to-hummingbird pollination shift in the highest-studied site. Our study is one of the few geographic-scale analyses of floral trait and pollinator assemblage variation in tropical plant species. Our results broaden our understanding of plant-pollinator interactions beyond temperate systems by showing substantial intraspecific divergence in both floral traits and pollinator assemblages across geographic space in a tropical plant species.

The spiral gingers (Costus L.) are a pantropical genus of herbaceous perennial monocots; the Neotropical clade of Costus radiated rapidly in the past few million years into over 60 species. The Neotropical spiral gingers have a rich history of evolutionary and ecological research that can motivate and inform modern genetic investigations. Here, we present the first 2 chromosome-level genome assemblies in the genus, for C. pulverulentus and C. lasius, and briefly compare their synteny. We assembled the C. pulverulentus genome from a combination of short-read data, Chicago and Dovetail Hi-C chromatin-proximity sequencing, and alignment with a linkage map. We annotated the genome by mapping a C. pulverulentus transcriptome and querying mapped transcripts against a protein database. We assembled the C. lasius genome with Pacific Biosciences HiFi long reads and alignment to the C. pulverulentus genome. These 2 assemblies are the first published genomes for non-cultivated tropical plants. These genomes solidify the spiral gingers as a model system and will facilitate research on the poorly understood genetic basis of tropical plant diversification.

The evolution of hummingbird pollination is common across angiosperms throughout the Americas, presenting an opportunity to examine convergence in both traits and environments to better understand how complex phenotypes arise. Here we examine independent shifts from bee to hummingbird pollination in the Neotropical spiral gingers (Costus) and address common explanations for the prevalence of transitions from bee to hummingbird pollination. We use floral traits of species with observed pollinators to predict pollinators of unobserved species and reconstruct ancestral pollination states on a well-resolved phylogeny. We examine whether independent transitions evolve towards the same phenotypic optimum and whether shifts to hummingbird pollination correlate with elevation or climate. Traits predicting hummingbird pollination include small flower size, brightly colored floral bracts and the absence of nectar guides. We find many shifts to hummingbird pollination and no reversals, a single shared phenotypic optimum across hummingbird flowers, and no association between pollination and elevation or climate. Evolutionary shifts to hummingbird pollination in Costus are highly convergent and directional, involve a surprising set of traits when compared with other plants with analogous transitions and refute the generality of several common explanations for the prevalence of transitions from bee to hummingbird pollination.

PremiseAdaptive divergence across environmental gradients is a key driver of speciation. Precipitation seasonality gradients are common in the tropics, yet drought adaptation is nearly unexplored in neotropical understory herbs. Here, we examined two recently diverged neotropical spiral gingers, one adapted to seasonal drought and one reliant on perennial water, to uncover the basis of drought adaptation.MethodsWe combined ecophysiological trait measurements in the field and greenhouse with experimental and observational assessments of real-time drought response to determine how Costus villosissimus (Costaceae) differs from C. allenii to achieve drought adaptation.ResultsWe found that drought-adapted C. villosissimus has several characteristics indicating flexible dehydration avoidance via semi-drought-deciduousness and a fast economic strategy. Although the two species do not differ in water-use efficiency, C. villosissimus has a more rapid growth rate, lower leaf mass per area, lower stem density, higher leaf nitrogen, and a strong trend of greater light-saturated photosynthetic rates. These fast economic strategy traits align with both field-based observations and experimental dry-down results. During drought, C. villosissimus displays facultative drought-deciduousness, losing lower leaves during the dry season and rapidly growing new leaves in the wet season.ConclusionsWe revealed a drought adaptation strategy that has not, to our knowledge, previously been documented in tropical herbs. This divergent drought adaptation evolved recently and is an important component of reproductive isolation between C. villosissimus and C. allenii, indicating that adaptive shifts to survive seasonal drought may be an underappreciated axis of neotropical understory plant diversification.

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.

The study of plant functional traits and variation among and within species can help illuminate functional coordination and trade-offs in key processes that allow plants to grow, reproduce and survive. We studied 20 leaf, above-ground stem, below-ground stem and fine-root traits of 17 Costus species from forests in Costa Rica and Panama to answer the following questions: (i) Do congeneric species show above-ground and below-ground trait coordination and trade-offs consistent with theory of resource acquisition and conservation? (ii) Is there correlated evolution among traits? (iii) Given the diversity of habitats over which Costus occurs, what is the relative contribution of site and species to trait variation? We performed a principal components analysis (PCA) to assess for the existence of a spectrum of trait variation and found that the first two PCs accounted for 21.4 % and 17.8 % of the total trait variation, respectively, with the first axis of variation being consistent with a continuum of resource-acquisitive and resource-conservative traits in water acquisition and use, and the second axis of variation being related to the leaf economics spectrum. Stomatal conductance was negatively related to both above-ground stem and rhizome specific density, and these relationships became stronger after accounting for evolutionary relatedness, indicating correlated evolution. Despite elevation and climatic differences among sites, high trait variation was ascribed to individuals rather than to sites. We conclude that Costus species present trait coordination and trade-offs that allow species to be categorized as having a resource-acquisitive or resource-conservative functional strategy, consistent with a whole-plant functional strategy with evident coordination and trade-offs between above-ground and below-ground function. Our results also show that herbaceous species and species with rhizomes tend to agree with trade-offs found in more species-rich comparisons.

PremiseEcogeographic 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.MethodsWe 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.ResultsWater 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.ConclusionsOurs 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.

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.

Heteranthery, the presence of two or more anther types in the same flower, is taxonomically widespread among bee-pollinated angiosperms, yet has puzzled botanists since Darwin. We test two competing hypotheses for its evolution: the long-standing 'division of labour' hypothesis, which posits that some anthers are specialized as food rewards for bees whereas others are specialized for surreptitious pollination, and our new hypothesis that heteranthery is a way to gradually release pollen that maximizes pollen delivery. We examine the evolution of heteranthery and associated traits across the genus Clarkia (Onagraceae) and study plant-pollinator interactions in two heterantherous Clarkia species. Across species, heteranthery is associated with bee pollination, delayed dehiscence and colour crypsis of one anther whorl, and movement of that anther whorl upon dehiscence. Our mechanistic studies in heterantherous species show that bees notice, forage on and export pollen from each anther whorl when it is dehiscing, and that heteranthery promotes pollen export. We find no support for division of labour, but multifarious evidence that heteranthery is a mechanism for gradual pollen presentation that probably evolved through indirect male-male competition for siring success.

One of the strongest biological impacts of climate change has been the movement of species poleward and upward in elevation. Yet, what is not clear is the extent to which the spatial distribution of locally adapted lineages and ecologically important traits may also shift with continued climate change. Here, we take advantage of a transplant experiment mimicking up-slope seed dispersal for a suite of ecologically diverse populations of yellow monkeyflower (Mimulus guttatus sensu lato) into a high-elevation common garden during an extreme drought period in the Sierra Nevada mountains, California, USA. We use a demographic approach to quantify fitness and test for selection on life history traits in local versus lower-elevation populations and in normal versus drought years to test the potential for up-slope migration and phenotypic selection to alter the distribution of key life history traits in montane environments. We find that lower-elevation populations tend to outperform local populations, confirming the potential for up-slope migration. Although selection generally favored some local montane traits, including larger flowers and larger stem size at flowering, drought conditions tended to select for earlier flowering typical of lower-elevation genotypes. Taken together, this suggests that monkeyflower lineages moving upward in elevation could experience selection for novel trait combinations, particularly under warmer and drier conditions that are predicted to occur with continued climate change.

One of the strongest biological impacts of climate change has been the movement of species poleward and upward in elevation. Yet, what is not clear is the extent to which the spatial distribution of locally adapted lineages and ecologically important traits may also shift with continued climate change. Here, we take advantage of a transplant experiment mimicking up-slope seed dispersal for a suite of ecologically diverse populations of yellow monkeyflower (Mimulus guttatus sensu lato) into a high-elevation common garden during an extreme drought period in the Sierra Nevada mountains, California, USA. We use a demographic approach to quantify fitness and test for selection on life history traits in local versus lower-elevation populations and in normal versus drought years to test the potential for up-slope migration and phenotypic selection to alter the distribution of key life history traits in montane environments. We find that lower-elevation populations tend to outperform local populations, confirming the potential for up-slope migration. Although selection generally favored some local montane traits, including larger flowers and larger stem size at flowering, drought conditions tended to select for earlier flowering typical of lower-elevation genotypes. Taken together, this suggests that monkeyflower lineages moving upward in elevation could experience selection for novel trait combinations, particularly under warmer and drier conditions that are predicted to occur with continued climate change.

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.

Environmental variation commonly drives functional trait diversity within species, among species, and across communities. Climate and shared evolutionary history can both influence trait–environment relationships. We studied variation in plant functional traits among closely related Costus species occurring across environmental gradients, the extent to which this variation occurs within single species, and how that variation may be influenced by shared evolutionary history. We measured leaf, aboveground stem, rhizome, and fine root traits of 17 species of Costus in eight sites in Costa Rica and Panama, which varied in elevation, temperature, and precipitation. We then assessed the relationships among traits and environmental variables and estimated the phylogenetic signal of the traits. We observed significant relationships between functional traits and climate. Stomatal conductance decreased, but stem density and rhizome dry matter content increased with decreasing mean annual temperature and precipitation seasonality in both cross‐species and single‐species analyses. This suggests that herbaceous species have a similar trade‐off between plant hydraulic efficiency and safety as found in woody plants. Mean annual temperature was a stronger driver of trait variation than mean annual precipitation. We also found phylogenetic signal in leaf and stem structural traits (i.e., closely related species are more similar than distantly related species), but not in physiological or belowground traits. Our results demonstrate significant trait variation within and among species of Costus, a widespread understory and herbaceous genus in the tropics, which is driven by both climate and shared evolutionary history. [ABSTRACT FROM AUTHOR]

Background and aimsPlant populations experiencing divergent pollination environments may be under selection to modify floral traits in ways that increase both attractiveness to and efficiency of novel pollinators. These changes may come at the cost of reducing overall effectiveness of other pollinators. The goal of this study was to examine differences in attractiveness and efficiency between Clarkia concinna and C. breweri, sister species of annual plants with parapatric distributions.MethodsAn assessment was made as to whether observed differences in visitors between natural populations are driven by differences in floral traits or differences in the local pollination environment. Differences in floral attractiveness were quantified by setting out arrays of both species in the geographical range of each species and exposing both species to nocturnal hawkmoths (Hyles lineata) in flight cages. Differences in visitor efficiency were estimated by measuring stigma-visitor contact frequency and pollen loads for diurnal visitors, and pollen deposition on stigmas for hawkmoths.Key resultsThe composition of visitors to arrayed plants was similar between plant species at any particular site, but highly divergent among sites, and reflected differences in visitors to natural populations. Diurnal insects visited both species, but were more common at C. concinna populations. Hummingbirds and hawkmoths were only observed visiting within the range of C. breweri. Despite attracting similar species when artificially presented together, C. concinna and C. breweri showed large differences in pollinator efficiency. All visitors except hawkmoths pollinated C. concinna more efficiently.ConclusionsDifferences in the available pollinator community may play a larger role than differences in floral traits in determining visitors to natural populations of C. concinna and C. breweri. However, floral traits mediate differences in pollinator efficiency. Increased effectiveness of the novel hawkmoth pollinator on C. breweri comes at relatively little cost in attractiveness to other visitors, but at large cost in their efficiency as pollinators.

Abstract Background In a spatially and temporally variable adaptive landscape, mutations operating in opposite directions and mutations of large effect should be commonly fixed due to the shifting locations of phenotypic optima. Similarly, an adaptive landscape with multiple phenotypic optima and deep valleys of low fitness between peaks will favor mutations of large effect. Traits under biotic selection should experience a more spatially and temporally variable adaptive landscape with more phenotypic optima than that experienced by traits under abiotic selection. To test this hypothesis, we assemble information from QTL mapping studies conducted in plants, comparing effect directions and effect sizes of detected QTL controlling traits putatively under abiotic selection to those controlling traits putatively under biotic selection. Results We find no differences in the fraction of antagonistic QTL in traits under abiotic and biotic selection, suggesting similar consistency in selection pressure on these two types of traits. However, we find that QTL controlling traits under biotic selection have a larger effect size than those under abiotic selection, supporting our hypothesis that QTL of large effect are more commonly detected in traits under biotic selection than in traits under abiotic selection. For traits under both abiotic and biotic selection, we find a large number of QTL of large effect, with 10.7% of all QTLs detected controlling more than 20% of the variance in phenotype. Conclusion These results suggest that mutations of large effect are more common in adaptive landscapes strongly determined by biotic forces, but that these types of adaptive landscapes do not result in a higher fraction of mutations acting in opposite directions. The high number of QTL of large effect detected shows that QTL of large effect are more common than predicted by the infinitesimal model of genetic adaptation.

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]