Incipient species often coexist in sympatry before complete reproductive isolation has evolved between them. How do they persist in the face of hybridization and gene flow? The challenge is more acute than ordinary ecological coexistence not only because gene flow erodes and recombines genetic differences, but also because selection against hybrids can destabilise population sizes. We estimated gene flow and selection against hybrid genotypes between sympatric limnetic and benthic species of threespine stickleback in two British Columbia lakes. First-generation hybrids are present at a rate of about 2%. To estimate selection, we compared the frequency distribution of ancestry proportions between juvenile and adult samples. We also used genomic simulation with assortative mating in an ecological model to determine how much selection is required to reproduce observed genotype frequencies. Results from the two approaches were comparable and yielded estimated selection coefficients S against the least fit ancestry proportion (within backcross range) between 0.5 and 0.6. Surprisingly, selection was found to be only slightly weaker than that leading readily to collapse and fusion in our simulations, suggesting that sympatric stickleback species are close to a coexistence boundary. Moderately strong selection appears to be required for coexistence with even low levels of gene flow. We suggest that larger niche differences are required to stabilise coexistence with gene flow than without gene flow. This helps to explain why successful sympatric species that hybridise often show conspicuous ecological and phenotypic differences.

Ecologically mediated selection against hybrids, caused by hybrid phenotypes fitting poorly into available niches, is typically viewed as distinct from selection caused by epistatic Dobzhansky-Muller hybrid incompatibilities. Here, we show how selection against transgressive phenotypes in hybrids manifests as incompatibility. After outlining our logic, we summarize current approaches for studying ecology-based selection on hybrids. We then quantitatively review QTL-mapping studies and find traits differing between parent taxa are typically polygenic. Next, we describe how verbal models of selection on hybrids translate to phenotypic and genetic fitness landscapes, highlighting emerging approaches for detecting polygenic incompatibilities. Finally, in a synthesis of published data, we report that trait transgression-and thus possibly extrinsic hybrid incompatibility in hybrids-escalates with the phenotypic divergence between parents. We discuss conceptual implications and conclude that studying the ecological basis of hybrid incompatibility will facilitate new discoveries about mechanisms of speciation.

Abstract Speciation research—the scientific field focused on understanding the origin and diversity of species—has a long and complex history. While relevant to one another, the specific goals and activities of speciation researchers are highly diverse, and scattered across a collection of different perspectives. Thus, our understanding of speciation will benefit from efforts to bridge scientific findings and the diverse people who do the work. In this paper, we outline two ways of integrating speciation research: (i) scientific integration, through the bringing together of ideas, data, and approaches; and (ii) social integration, by creating ways for a diversity of researchers to participate in the scientific process. We then discuss five challenges to integration: (i) the multidisciplinary nature of speciation research, (ii) the complex language of speciation; (iii) a bias toward certain study systems; (iv) the challenges of working across scales; and (v) inconsistent measures and reporting standards. We provide practical steps that individuals and groups can take to help overcome these challenges, and argue that integration is a team effort in which we all have a role to play.

Plant reproductive assurance describes the ability of a plant to successfully reproduce in an environment that is potentially devoid of conspecifics and/or pollinators. Traditionally, studies have focused on the role of contemporary ecology—such as pollinator or mate availability—in driving spatial patterns in reproductive assurance within species, however, historical processes such as post-glacial range expansion may be an understudied alternative explanation for geographic variation in mating system. This is because during the process of geographic range expansion into novel habitat, selection should favour individuals that possess traits promoting reproductive assurance (i.e., autonomous selfing or clonal reproduction). Here, we used Northern pink monkeyflower— Erythranthe ( Mimulus lewisii —a hermaphroditic, self-compatible, perennial, alpine plant, as a focal species to investigate the historical signatures of geographic range expansion by combining phylogeographic analyses with a greenhouse survey of range-wide reproductive assurance. First, we detected significant geographic variation among populations in two components of reproductive assurance: self-fertilization and clonal propagation. Next, using genome-wide single nucleotide polymorphism (SNP) data, we identified three distinct genetic clusters structured by longitude and estimated geographic coordinates of the most likely origins of range expansion within each cluster. We found that both measures of reproductive assurance significantly increased on average with distance from the inferred biogeographic origin, which is consistent with the hypothesis that reproductive assurance undergoes adaptive evolution during range expansion. This study supports hypotheses underlying Baker's Law and contributes to our understanding of spatial variation in reproductive assurance, which is linked to variation in evolutionary potential, adaptability, and the long-term persistence of populations across large spatial scales. ### Competing Interest Statement The authors have declared no competing interest.

The vertebrate gut microbiota is a critical determinant of organismal function, yet whether and how gut microbial communities affect host fitness under natural conditions remains largely unclear. We characterised associations between a fitness proxy—individual growth rate—and bacterial gut microbiota diversity and composition in threespine stickleback fish introduced to large semi-natural ponds. We detected a 63% higher richness of bacterial taxa (α-diversity) in the guts of high-fitness fish compared to low-fitness fish, which might be driven by stronger bacterial dispersal among high-fitness fish according to the fit of a neutral community model. Further, microbial communities of high-fitness fish were more similar to one another (i.e., exhibited lower β-diversity) than those of low-fitness fish. The lower β-diversity found to be associated with higher host fitness is consistent with the Anna Karenina principle—that there are fewer ways to have a functional microbiota than a dysfunctional microbiota. Our study links differences in α- and β-diversity to a fitness-related trait in a vertebrate species reared under naturalistic conditions and our findings provide a basis for functional tests of the fitness consequences of host-microbiota interactions.

Responses to climate change have often been found to lag behind the rate of warming that has occurred. In addition to dispersal limitation potentially restricting spread at leading range margins, the persistence of species in new and unsuitable conditions is thought to be responsible for apparent time‐lags. Soil seed banks can allow plant communities to temporarily buffer unsuitable environmental conditions, but their potential to slow responses to long‐term climate change is largely unknown. As local forest cover can also buffer the effects of a warming climate, it is important to understand how seed banks might interact with land cover to mediate community responses to climate change. We first related species‐level seed bank persistence and distribution‐derived climatic niches for 840 plant species. We then used a database of plant community data from grasslands, forests and intermediate successional habitats from across Europe to investigate relationships between seed banks and their corresponding herb layers in 2763 plots in the context of climate and land cover. We found that species from warmer climates and with broader distributions are more likely to have a higher seed bank persistence, resulting in seed banks that are composed of species with warmer and broader climatic distributions than their corresponding herb layers. This was consistent across our climatic extent, with larger differences (seed banks from even warmer climates relative to vegetation) found in grasslands. Synthesis . Seed banks have been shown to buffer plant communities through periods of environmental variability, and in a period of climate change might be expected to contain species reflecting past, cooler conditions. Here, we show that persistent seed banks often contain species with relatively warm climatic niches and those with wide climatic ranges. Although these patterns may not be primarily driven by species' climatic adaptations, the prominence of such species in seed banks might still facilitate climate‐driven community shifts. Additionally, seed banks may be related to ongoing trends regarding the spread of widespread generalist species into natural habitats, while cool‐associated species may be at risk from both short‐ and long‐term climatic variability and change.

The vertebrate gut microbiota is a critical determinant of organismal function, yet it remains unclear if and how gut microbial communities affect host fitness under natural conditions. Here, we investigate associations between growth rate (a fitness proxy) and gut microbiota diversity and composition in a field experiment with threespine stickleback fish ( Gasterosteus aculeatus ). We detected on average 63% more bacterial taxa in the guts of high-fitness fish compared to low-fitness fish (i.e., higher α-diversity), suggesting that higher diversity promotes host growth. The microbial communities of high-fitness fish had higher similarity (i.e., lower β-diversity) than low-fitness fish, supporting the Anna Karenina principle— that there are fewer ways to have a functional microbiota than a dysfunctional microbiota. Our findings provide a basis for functional tests of the fitness consequences of host-microbiota interactions. Significance statement The vertebrate gut microbiota is important for many aspects of their hosts’ biology—such as nutrient metabolism and defense against pathogens—that could ultimately affect host fitness. However, studies investigating the effects of gut microbiota composition on vertebrate host fitness under natural conditions remain exceedingly rare. We tested for associations between gut microbiota diversity and growth rate (a fitness proxy) in threespine stickleback fish reared in large outdoor ponds. We found evidence that a more diverse gut microbiota was predictive of higher growth rate and therefore increased host fitness. Notably, high-fitness fish had higher gut microbiota similarity to one another than did low-fitness fish, providing experimental evidence for the Anna Karenina principle—that there are fewer ways to have a functional microbiota than a dysfunctional microbiota—as it relates to host fitness.

In contrast to ecological speciation, where reproductive isolation evolves as a consequence of divergent natural selection, speciation by parallel natural selection has been less thoroughly studied. To test whether parallel evolution drives speciation, we leveraged the repeated evolution of benthic and limnetic ecotypes of threespine stickleback fish and estimated fitness for pure crosses and within-ecotype hybrids in semi-natural ponds and in laboratory aquaria. In ponds, we detected hybrid breakdown in both ecotypes but this was counterbalanced by heterosis and the strength of post-zygotic isolation was nil. In aquaria, we detected heterosis in limnetic crosses and breakdown in benthic crosses, which is suggestive of process- and ecotype-specific environment-dependence. In ponds, heterosis and breakdown were three times greater in limnetic crosses than in benthic crosses, contrasting the prediction that the fitness consequences of hybridization should be greater in crosses among more derived ecotypes. Consistent with a primary role for stochastic processes, patterns differed among crosses between populations from different lakes. Yet, the observation of qualitatively similar patterns of heterosis and hybrid breakdown for both ecotypes when averaging the lake pairs indicates that the outcome of hybridization is repeatable in a general sense.

Selection against mismatched traits in hybrids is the phenotypic analogue of intrinsic hybrid incompatibilities. Mismatch occurs when hybrids resemble one parent population for some phenotypic traits and the other parent population for other traits, and is caused by dominance in opposing directions or from segregation of alleles in recombinant hybrids. In this study, we used threespine stickleback fish (Gasterosteus aculeatus L.) to test the theoretical prediction that trait mismatch in hybrids should increase with the magnitude of phenotypic divergence between parent populations. We measured morphological traits in parents and hybrids in crosses between a marine population representing the ancestral form and twelve freshwater populations that have diverged from this ancestral state to varying degrees according to their environments. We found that trait mismatch was greater in more divergent crosses for both F-1 and F-2 hybrids. In the F-1, the divergence-mismatch relationship was caused by traits having dominance in different directions, whereas it was caused by increasing segregating phenotypic variation in the F-2. Our results imply that extrinsic hybrid incompatibilities accumulate as phenotypic divergence proceeds.

When divergent populations interbreed, their alleles are brought together in hybrids. These hybrids may express novel phenotypes, not previously exposed to selection. In the initial F1 cross, most divergent alleles are present as heterozygotes. Therefore, F1 fitness can be influenced by dominance effects that first appear together in the hybrids, and so could not have been selected to function well together. We present a systematic study of these F1 dominance effects by introducing variable phenotypic dominance into Fisher’s geometric model. We show that dominance often reduces hybrid fitness, which can lead to patterns of optimal outbreeding and a steady decline in F1 fitness at high levels of divergence. We also show that “lucky” beneficial effects sometimes arise by chance, which might be especially important when hybrids can access novel environments. We then explore the interaction of phenotypic dominance with uniparental inheritance, showing that dominance can lead to violations of Haldane’s Rule (reduced fitness of the heterogametic sex) while strengthening Darwin’s Corollary (fitness differences between cross directions). Taken together, our results show that dominance could play an important role in the outcomes of hybridisation after secondary contact, and thus to the maintenance or collapse of isolating barriers. Nevertheless, the telltale signs of dominance are relatively few and subtle. Results also suggest that dominance effects are smaller than the cost of segregation variance, implying that simple additive models may still give good predictions for later-generation recombinant hybrids, even when dominance qualitatively alters outcomes for the F1.

Hybrid incompatibilities occur when interactions between opposite ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are "intrinsic," meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis using sequence data are scarce. In this article, we compiled genetic data for F-2 hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatus L.) that were born and raised in either the field (seminatural experimental ponds) or the laboratory (aquaria). Because selection against incompatibilities results in elevated ancestry heterozygosity, we tested the prediction that ancestry heterozygosity will be higher in pond-raised fish compared to those raised in aquaria. We found that ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Additional analyses support a phenotypic basis for incompatibility and suggest that environment-specific single-locus heterozygote advantage is not the cause of selection on ancestry heterozygosity. Our study provides evidence that, in stickleback, a coarse-albeit indirect-signal of environment-dependent hybrid incompatibility is reliably detectable and suggests that extrinsic incompatibilities can evolve before intrinsic incompatibilities.

Here we provide the 'Global Spectrum of Plant Form and Function Dataset', containing species mean values for six vascular plant traits. Together, these traits -plant height, stem specific density, leaf area, leaf mass per area, leaf nitrogen content per dry mass, and diaspore (seed or spore) mass - define the primary axes of variation in plant form and function. The dataset is based on ca. 1 million trait records received via the TRY database (representing ca. 2,500 original publications) and additional unpublished data. It provides 92,159 species mean values for the six traits, covering 46,047 species. The data are complemented by higher-level taxonomic classification and six categorical traits (woodiness, growth form, succulence, adaptation to terrestrial or aquatic habitats, nutrition type and leaf type). Data quality management is based on a probabilistic approach combined with comprehensive validation against expert knowledge and external information. Intense data acquisition and thorough quality control produced the largest and, to our knowledge, most accurate compilation of empirically observed vascular plant species mean traits to date.

Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.

Hybrid incompatibilities occur when interactions between opposite-ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are ‘intrinsic’, meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis are scarce. In this article, we compiled genetic data for F2hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatusL.) that were born and raised in either the field (semi-natural experimental ponds) or the laboratory (aquaria). We tested for differences in excess heterozygosity between these two environments at ancestry informative loci—a genetic signature of selection against incompatibilities. We found that excess ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Previous results from F1 hybrids in the field suggest that pond-specific (single-locus) heterosis is unlikely to explain this finding. Our study suggests that, in stickleback, a coarse signal of environment-dependent hybrid incompatibilities is reliably detectable and that extrinsic incompatibilities have evolved before intrinsic incompatibilities.

Extrinsic post-zygotic isolating barriers occur when hybrids have poor fitness in the parental habitat(s) and ultimately arise as a consequence of interactions between the alleles underlying adaptation. Most models of speciation via natural selection consider only alleles that have additive phenotypic effects, even though many quantitative trait loci exhibit some dominance. We used computer simulations to evaluate how hybrid fitness differs when parent populations adapt from either (i) mutations that are strictly additive or (ii) mutations with a range of dominance coefficients. Compared to the additive case, we find that introducing dominance invariably reduces hybrid fitness when parents adapt to identical optima (i.e., parallel selection) because hybrids express transgressive phenotypes that are maladaptive in the common parental niche. The effect of dominance becomes less negative as selection tends toward completely divergent. When selection is completely divergent, dominance can increase hybrid fitness over the additive case because chance events result in unequal mean dominance among populations and cause hybrids to resemble one of the parents rather than a maladapted intermediate phenotype. However, when the adapting population has many traits (i.e., high ‘dimensionality’) dominance always reduces hybrid fitness over the additive case because hybrids express maladaptive transgressive phenotypes in traits under stabilizing selection. Our results indicate that dominant alleles facilitate progress toward speciation via parallel natural selection, and might either increase or decrease the efficacy of divergent selection for speciation.

The founder of plant functional ecology.

Aim: Climate and land use are key determinants of biodiversity, with past and ongoing changes posing serious threats to global ecosystems. Unlike most other organism groups, plant species can possess dormant life-history stages such as soil seed banks, which may help plant communities to resist or at least postpone the detrimental impact of global changes. This study investigates the potential for soil seed banks to achieve this. Location: Europe. Time period: 1978–2014. Major taxa studied: Flowering plants. Methods: Using a space-for-time/warming approach, we study plant species richness and composition in the herb layer and the soil seed bank in 2,796 community plots from 54 datasets in managed grasslands, forests and intermediate, successional habitats across a climate gradient. Results: Soil seed banks held more species than the herb layer, being compositionally similar across habitats. Species richness was lower in forests and successional habitats compared to grasslands, with annual temperature range more important than mean annual temperature for determining richness. Climate and land-use effects were generally less pronounced when plant community richness included seed bank species richness, while there was no clear effect of land use and climate on compositional similarity between the seed bank and the herb layer. Main conclusions: High seed bank diversity and compositional similarity between the herb layer and seed bank plant communities may provide a potentially important functional buffer against the impact of ongoing environmental changes on plant communities. This capacity could, however, be by climate warming. Dormant life-history be of in changing potentially observed time-lags in plant community

Are first-generation (F1) hybrids typically intermediate for all traits that differentiate their parents? Or are they similar to one parent for most traits, or even mismatched for divergent traits? Although the phenotype of otherwise viable and fertile hybrids determines their fate, little is known about the general patterns, predictors, and consequences of phenotype expression in hybrids. To address this empirical gap, we compiled data from nearly 200 studies where traits were measured in a common environment for two parent populations and F1 hybrids. We find that individual traits are typically halfway between the parental midpoint and one parental value (i.e., hybrid trait values are typically 0.25 or 0.75 if parents’ values are 0 & 1). When considering pairs of traits together, a hybrid’s multivariate phenotype tends to resemble one parent (pairwise parent-bias) about 50 % more than the other while also exhibiting a similar magnitude of trait mismatch due to different traits having dominance in conflicting directions. We detect no phylogenetic signal nor an effect of parental genetic distance on dominance or mismatch. Using data from an experimental field planting of recombinant hybrid sunflowers—where there is among-individual variation in dominance and mismatch due to segregation of divergent alleles—we illustrate that pairwise parent-bias improves fitness while mismatch reduces fitness. Importantly, the effect of mismatch on fitness was stronger than that of pairwise parent-bias. In sum, our study has three major conclusions. First, hybrids between ecologically divergent natural populations are typically not phenotypically intermediate but rather exhibit substantial mismatch while also resembling one parent more than the other. Second, dominance and mismatch are likely determined by population-specific processes rather than general rules. Finally, selection against hybrids likely results from both selection against somewhat intermediate phenotypes and against mismatched trait combinations.

Vegetation surveys are conducted to obtain a catalogue of the plant species that occupy an area of interest, and are used to inform the decisions of policymakers about conservation, development, and remediation efforts. Currently, vegetation surveys rely on traditional morphology-based taxonomic practices to identify collected specimens. By implementing recent advances in molecular taxonomy, it may be possible to improve upon these methods and reduce the associated costs. In this study, we used both morphological and molecular taxonomic methods to sample 337 forest vegetation plots in northeastern Ontario, Canada. DNA barcoding-a molecular taxonomic tool-was used to identify specimens collected in the molecular taxonomic survey. The molecular taxonomic survey identified a mean of 12.4 species per plot and 202 species in total, whereas the morphological taxonomic survey identified a mean of 9.8 species per plot and 142 species in total; both surveys provided identical estimates of community similarity. The morphological taxonomic survey was 37 % more expensive than molecular taxonomic survey, owing largely to the increased time required in the field to collect specimens that flowered at different times. Our results indicate that molecular taxonomic tools are more cost-effective than traditional morphology-based taxonomic practices for species identification in vegetation surveys. Taxonomy underpins all conservation, and the implementation of molecular taxonomic tools for vegetation surveys has promise to lessen the consequences of the taxonomic impediment and increase the effectiveness of conservation efforts.