Reproductive strategies and their consequences for divergence, gene flow, and genetic diversity in three taxa of Clarkia.

Differences in reproductive strategies can have important implications for macro- and micro-evolutionary processes. We used a comparative approach through a population genetics lens to evaluate how three distinct reproductive strategies shape patterns of divergence among as well as gene flow and genetic diversity within three closely related taxa in the genus Clarkia. One taxon is a predominantly autonomous self-fertilizer and the other two taxa are predominantly outcrossing but vary in the primary pollinator they attract. In genotyping populations using genotyping-by-sequencing and comparing loci shared across taxa, our results suggest that differences in reproductive strategies in part promote evolutionary divergence among these closely related taxa. Contrary to expectations, we found that the selfing taxon had the highest levels of heterozygosity but a low rate of polymorphism. The high levels of fixed heterozygosity for a subset of loci suggests this pattern is driven by the presence of structural rearrangements in chromosomes common in other Clarkia taxa. In evaluating patterns within taxa, we found a complex interplay between reproductive strategy and geographic distribution. Differences in the mobility of primary pollinators did not translate to a difference in rates of genetic diversity and gene flow within taxa - a pattern likely due to one taxon having a patchier distribution and a less temporally and spatially reliable pollinator. Taken together, this work advances our understanding of the factors that shape gene flow and the distribution of genetic diversity within and among closely related taxa.

Genome assemblies and comparison of two Neotropical spiral gingers: Costus pulverulentus and C. lasius.

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.

Evolutionary convergence on hummingbird pollination in Neotropical Costus provides insight into the causes of pollinator shifts.

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.

The genetic basis of floral mechanical isolation between two hummingbird-pollinated Neotropical understorey herbs.

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.

Flexible drought deciduousness in a neotropical understory herb.

PREMISE: Adaptive 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. METHODS: We 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. RESULTS: We 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. CONCLUSIONS: We 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.

PREMISA DEL ESTUDIO: La divergencia adaptativa a lo largo de gradientes ambientales es un factor clave de la especiación. Los gradientes de estacionalidad de la precipitación son comunes en los trópicos, sin embargo, la adaptación a la sequía es casi inexplorada en las hierbas neotropicales del sotobosque. Examinamos dos especies de caña agria neotropicales que divergieron recientemente, uno adaptado a la sequía estacional y otro que depende del agua perenne, para descubrir la base de la adaptación a la sequía. MÉTODOS: Combinamos mediciones ecofisiológicas en el campo y el invernadero con una evaluación experimental y observacional de la respuesta a la sequía en tiempo real para determinar cómo Costus villosissimus (Costaceae) difiere de C. allenii para lograr la adaptación a la sequía. RESULTADOS CLAVE: Encontramos que C. villosissimus, que está adaptado a la sequía, tiene varias características que indican que evita la deshidratación a través de la caducididad y una estrategia de vida rápida. Aunque las dos especies no difieren en la eficiencia del uso del agua, C. villosissimus tiene una tasa de crecimiento más rápida, menor masa foliar por área, menor densidad del tallo, mayor nitrógeno foliar y una fuerte tendencia de mayores tasas fotosintéticas saturadas de luz. Estos atributos de la estrategia de vida rápida se alinean tanto con las observaciones basadas en el campo como con los resultados experimentales de sequía. Para sobrevivir a la sequía, C. villosissimus es caducifolia facultativa, perdiendo hojas inferiores durante la estación seca y creciendo rápidamente hojas nuevas en la estación húmeda. CONCLUSIONES: Revelamos una estrategia de adaptación a la sequía que, hasta donde sabemos, no ha sido documentada previamente en hierbas tropicales. Esta adaptación divergente a la sequía evolucionó recientemente y es un componente importante del aislamiento reproductivo entre C. villosissimus y C. allenii, lo que indica que los cambios adaptativos para sobrevivir a la sequía estacional pueden ser un eje subestimado de la diversificación de las plantas del sotobosque neotropical.

Parallel evolution of phenological isolation across the speciation continuum in serpentine-adapted annual wildflowers.

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.

A greenhouse experiment partially supports inferences of ecogeographic isolation from niche models of Clarkia sister species.

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.

Darwin's vexing contrivance: a new hypothesis for why some flowers have two kinds of anther.

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.

Experimental sympatry reveals geographic variation in floral isolation by hawkmoths.

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.

Adaptation and divergence in edaphic specialists and generalists: serpentine soil endemics in the California flora occur in barer serpentine habitats with lower soil calcium levels than serpentine tolerators.

PREMISE: Adaptation to harsh edaphic substrates has repeatedly led to the evolution of edaphic specialists and generalists. Yet, it is unclear what factors promote specialization versus generalization. Here, we search for habitat use patterns associated with serpentine endemics (specialists) and serpentine tolerators (generalists) to indirectly test the hypothesis that trade-offs associated with serpentine adaptation promote specialization. We predict that (1) endemics have adapted to chemically harsher and more bare serpentine habitats than tolerators, and (2) edaphic endemics show more habitat divergence from their sister species than tolerators do among on- and off-serpentine populations. METHODS: We selected 8 serpentine endemic and 9 serpentine tolerator species representing independent adaptation to serpentine. We characterized soil chemistry and microhabitat bareness from one serpentine taxon of each species and from a paired nonserpentine sister taxon, resulting in 8 endemic and 9 tolerator sister-taxa pairs. RESULTS: We find endemic serpentine taxa occur in serpentine habitats averaging twice as much bare ground as tolerator serpentine taxa and 25% less soil calcium, a limiting macronutrient in serpentine soils. We do not find strong evidence that habitat divergence between sister taxa of endemic pairs is greater than between sister taxa of tolerator pairs. CONCLUSIONS: These results suggest serpentine endemism is associated with adaptation to chemically harsher and more bare serpentine habitats. It may be that this adaptation trades off with competitive ability, which would support the longstanding, but rarely tested, competitive trade-off hypothesis.

Sympatric serpentine endemic Monardella (Lamiaceae) species maintain habitat differences despite hybridization.

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.

The scale of local adaptation in Mimulus guttatus: comparing life history races, ecotypes, and populations.

Fitness trade-offs between environments are central to the evolution of biodiversity. Although transplant studies often document fitness trade-offs consistent with local adaptation (LA), many have also found an advantage of foreign genotypes (foreign advantage (FA)). Understanding the mechanisms driving the magnitude and distribution of fitness variation requires comparative approaches that test the ecological scales at which these different patterns emerge. We used a common garden transplant experiment to compare the relative fitnesses of native vs foreign genotypes at three nested ecological scales within Mimulus guttatus: annual vs perennial life history races, perennial ecotypes across an elevational range, and populations within perennial elevational ecotypes. We integrated fitness across the life-cycle and decomposed LA vs FA into contributions from different fitness components. We found LA, measured as home-site advantage, between annual and perennial races and a trend towards LA among populations within montane habitats. Conversely, we found strong FA of low-elevation perennials in a montane environment. LA between life history races reflects the fitness advantages of adult survival and vegetative growth in a mesic environment. Within the perennial race, recent climate conditions or nonselective processes, such as dispersal limitation or mutational load, could explain FA of low-elevation perennials in a montane environment.

Mating system plasticity promotes persistence and adaptation of colonizing populations of hermaphroditic angiosperms.

Persistence and adaptation in novel environments are limited by small population size, strong selection, and maladaptive gene flow. Mating system plasticity is common in angiosperms and may provide both demographic and genetic benefits that promote niche evolution, including reproductive assurance and isolation from maladaptive gene flow. Yet increased self-fertilization may also cause inbreeding depression, accumulation of deleterious mutations, and reduced adaptive potential. Here we use individual-based simulations to examine the consequences of mating system plasticity for persistence and adaptation in a novel environment that imposes selection on a quantitative trait. We examine the joint evolution of local adaptation, inbreeding depression, and genetic load. We find that a plastic shift to a mixed mating system generally promotes niche evolution by decreasing the risk of extinction, providing isolation from maladaptive gene flow, and temporarily increasing genetic variance in the trait under selection, whereas obligate self-fertilization reduces adaptive potential. These effects are most pronounced under conditions of mate limitation, strong selection, or maladaptive gene flow. Our results highlight the diverse demographic and genetic consequences of self-fertilization and support the potential role for plastic shifts in mating system to promote niche evolution in flowering plants.

An ultraviolet floral polymorphism associated with life history drives pollinator discrimination in Mimulus guttatus.

UNLABELLED: • PREMISE OF THE STUDY: Ultraviolet (UV) floral patterns are common in angiosperms and mediate pollinator attraction, efficiency, and constancy. UV patterns may vary within species, yet are cryptic to human observers. Thus, few studies have explicitly described the distribution or ecological significance of intraspecific variation in UV floral patterning. Here, we describe the geographic distribution and pattern of inheritance of a UV polymorphism in the model plant species Mimulus guttatus (Phrymaceae). We then test whether naturally occurring UV phenotypes influence pollinator interactions within M. guttatus.• METHODS: We document UV patterns in 18 annual and 19 perennial populations and test whether UV pattern is associated with life history. To examine the pattern of inheritance, we conducted crosses within and between UV phenotypes. Finally, we tested whether bee pollinators discriminate among naturally occurring UV phenotypes in two settings: wild bee communities and captive Bombus impatiens.• KEY RESULTS: Within M. guttatus, perennial populations exhibit a small bulls-eye pattern, whereas a bilaterally symmetric runway pattern occurs mainly in annual populations. Inheritance of UV patterning is consistent with a single-locus Mendelian model in which the runway phenotype is dominant. Bee pollinators discriminate against unfamiliar UV patterns in both natural and controlled settings.• CONCLUSIONS: We describe a widespread UV polymorphism associated with life history divergence within Mimulus guttatus. UV pattern influences pollinator visitation and should be considered when estimating reproductive barriers between life history ecotypes. This work develops a new system to investigate the ecology and evolution of UV floral patterning in a species with extensive genomic resources.

Novel adaptation to hawkmoth pollinators in Clarkia reduces efficiency, not attraction of diurnal visitors.

BACKGROUND AND AIMS: Plant 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. METHODS: An 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 RESULTS: The 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. CONCLUSIONS: Differences 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.

Seasonal reliance on nectar by an insectivorous bat revealed by stable isotopes.

Many animals have seasonally plastic diets to take advantage of seasonally abundant plant resources, such as fruit or nectar. Switches from insectivorous diets that are protein rich to fruits or nectar that are carbohydrate rich present physiological challenges, but are routinely done by insectivorous songbirds during migration. In contrast, insectivorous bat species are not known to switch diets to consume fruit or nectar. Here, we use carbon stable isotope ratios to establish the first known case of a temperate bat species consuming substantial quantities of nectar during spring. We show that pallid bats (Antrozous pallidus) switch from a diet indistinguishable from that of sympatric insectivorous bat species in winter (when no cactus nectar is present) to a diet intermediate between those of insectivorous bats and nectarivorous bats during the spring bloom of a bat-adapted cactus species. Combined with previous results that established that pallid bats are effective pollinators of the cardon cactus (Pachycereus pringlei), our results suggest that the interaction between pallid bats and cardon cacti represents the first-known plant-pollinator mutualism between a plant and a temperate bat. Diet plasticity in pallid bats raises questions about the degree of physiological adaptations of insectivorous bats for incorporation of carbohydrate-rich foods, such as nectar or fruit, into the diet.

Growth-defense trade-offs promote habitat isolation between recently-diverged species.

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.

Genomic Approaches Are Improving Taxonomic Representation in Genetic Studies of Speciation.

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.

Genetics and the Evolution of Prezygotic Isolation.

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.

Insectivorous bat pollinates columnar cactus more effectively per visit than specialized nectar bat.

Plant-pollinator interactions are great model systems to investigate mutualistic relationships. We compared pollinator effectiveness between facultative and obligate nectar-feeding bats to determine how foraging specialization influences mutualistic interactions in a bat-adapted cactus. We predicted that a specialized nectarivorous bat would deliver more pollen than an opportunistic nectar-feeding bat because of specialized adaptations to nectar feeding that indicate close association with their food plants. Counter to our predictions, the opportunistic Antrozous pallidus delivered significantly more pollen grains per visit than the specialized Leptonycteris yerbabuenae. Higher pollinator effectiveness, based on visitation rates and pollen deposition levels, varied between species by site, and although A. pallidus visits flowers much less frequently than L. yerbabuenae over all sites, it is likely an effective and reliable pollinator of Pachycereus pringlei in Baja, Mexico. Our results suggest that morphological adaptations and dietary specialization on nectar do not necessarily confer advantages for pollination over less specialized plant visitors and highlight the reciprocally exploitative nature of mutualisms.