Evolvability predicts macroevolution under fluctuating selection.

Heritable variation is a prerequisite for evolutionary change, but the relevance of genetic constraints on macroevolutionary timescales is debated. By using two datasets on fossil and contemporary taxa, we show that evolutionary divergence among populations, and to a lesser extent among species, increases with microevolutionary evolvability. We evaluate and reject several hypotheses to explain this relationship and propose that an effect of evolvability on population and species divergence can be explained by the influence of genetic constraints on the ability of populations to track rapid, stationary environmental fluctuations.

Evolutionary plant-pollinator responses to anthropogenic land-use change: impacts on ecosystem services.

Agricultural intensification at field and landscape scales, including increased use of agrochemicals and loss of semi-natural habitats, is a major driver of insect declines and other community changes. Efforts to understand and mitigate these effects have traditionally focused on ecological responses. At the same time, adaptations to pesticide use and habitat fragmentation in both insects and flowering plants show the potential for rapid evolution. Yet we lack an understanding of how such evolutionary responses may propagate within and between trophic levels with ensuing consequences for conservation of species and ecological functions in agroecosystems. Here, we review the literature on the consequences of agricultural intensification on plant and animal evolutionary responses and interactions. We present a novel conceptualization of evolutionary change induced by agricultural intensification at field and landscape scales and emphasize direct and indirect effects of rapid evolution on ecosystem services. We exemplify by focusing on economically and ecologically important interactions between plants and pollinators. We showcase available eco-evolutionary theory and plant-pollinator modelling that can improve predictions of how agricultural intensification affects interaction networks, and highlight available genetic and trait-focused methodological approaches. Specifically, we focus on how spatial genetic structure affects the probability of propagated responses, and how the structure of interaction networks modulates effects of evolutionary change in individual species. Thereby, we highlight how combined trait-based eco-evolutionary modelling, functionally explicit quantitative genetics, and genomic analyses may shed light on conditions where evolutionary responses impact important ecosystem services.

Sexually concordant selection on floral traits despite greater opportunity for selection through male fitness.

Pollinators are important drivers of floral trait evolution, yet plant populations are not always perfectly adapted to their pollinators. Such apparent maladaptation may result from conflicting selection through male and female sexual functions in hermaphrodites. We studied sex-specific mating patterns and phenotypic selection on floral traits in Aconitum gymnandrum. After genotyping 1786 offspring, we partitioned individual fitness into sex-specific selfed and outcrossed components and estimated phenotypic selection acting through each. Relative fitness increased with increasing mate number, and more so for male function. This led to greater opportunity for selection through outcrossed male fitness, though patterns of phenotypic selection on floral traits tended to be similar, and with better support for selection through female rather than male fitness components. We detected directional selection through one or more fitness component for larger flower number, larger flowers, and more negative nectar gradients within inflorescences. Our results are consistent with Bateman's principles for sex-specific mating patterns and illustrate that, despite the expected difference in opportunity for selection, patterns of variation in selection across traits can be rather similar for the male and female sexual functions. These results shed new light on the effect of sexual selection on the evolution of floral traits.

Pollinator-mediated effects of landscape-scale land use on grassland plant community composition and ecosystem functioning - seven hypotheses.

Environmental change is disrupting mutualisms between organisms worldwide. Reported declines in insect populations and changes in pollinator community compositions in response to land use and other environmental drivers have put the spotlight on the need to conserve pollinators. While this is often motivated by their role in supporting crop yields, the role of pollinators for reproduction and resulting taxonomic and functional assembly in wild plant communities has received less attention. Recent findings suggest that observed and experimental gradients in pollinator availability can affect plant community composition, but we know little about when such shifts are to be expected, or the impact they have on ecosystem functioning. Correlations between plant traits related to pollination and plant traits related to other important ecosystem functions, such as productivity, nitrogen uptake or palatability to herbivores, lead us to expect non-random shifts in ecosystem functioning in response to changes in pollinator communities. At the same time, ecological and evolutionary processes may counteract these effects of pollinator declines, limiting changes in plant community composition, and in ecosystem functioning. Despite calls to investigate community- and ecosystem-level impacts of reduced pollination, the study of pollinator effects on plants has largely been confined to impacts on plant individuals or single-species populations. With this review we aim to break new ground by bringing together aspects of landscape ecology, ecological and evolutionary plant-insect interactions, and biodiversity-ecosystem functioning research, to generate new ideas and hypotheses about the ecosystem-level consequences of pollinator declines in response to land-use change, using grasslands as a focal system. Based on an integrated set of seven hypotheses, we call for more research investigating the putative pollinator-mediated links between landscape-scale land use and ecosystem functioning. In particular, future research should use combinations of experimental and observational approaches to assess the effects of changes in pollinator communities over multiple years and across species on plant communities and on trait distributions both within and among species.

Pollen as the link between floral phenotype and fitness.

Pollen plays a key role in plant reproductive biology. Despite the long history of research on pollen and pollination, recent advances in pollen-tracking methods and statistical approaches to linking plant phenotype, pollination performance, and reproductive fitness yield a steady flow of exciting new insights. In this introduction to the Special Issue "Pollen as the Link Between Phenotype and Fitness," we start by describing a general conceptual model linking functional classes of floral phenotypic traits to pollination-related performance metrics and reproductive fitness. We use this model as a framework for synthesizing the relevant literature, highlighting the studies included in the Special Issue, and identifying gaps in our understanding and opportunities for further development of the field. The papers that follow in this Special Issue provide new insights into the relationships between pollen production, presentation, flower morphology, and pollination performance (e.g., pollen deposition onto stigmas), the role of pollinators in pollen transfer, and the consequences of heterospecific pollen deposition. Several of the studies demonstrate exciting experimental and analytical approaches that should pave the way for continued work addressing the intriguing role of pollen in linking plant phenotypes to reproductive fitness.

Seasonality and competition select for variable germination behavior in perennials.

The occurrence of within-population variation in germination behavior and associated traits such as seed size has long fascinated evolutionary ecologists. In annuals, unpredictable environments are known to select for bet-hedging strategies causing variation in dormancy duration and germination strategies. Variation in germination timing and associated traits is also commonly observed in perennials and often tracks gradients of environmental predictability. Although bet-hedging is thought to occur less frequently in long-lived organisms, these observations suggest a role of bet-hedging strategies in perennials occupying unpredictable environments. We use complementary analytical and evolutionary simulation models of within-individual variation in germination behavior in seasonal environments to show how bet-hedging interacts with fluctuating selection, life-history traits, and competitive asymmetries among germination strategies. We reveal substantial scope for bet-hedging to produce variation in germination behavior in long-lived plants, when "false starts" to the growing season results in either competitive advantages or increased mortality risk for alternative germination strategies. Additionally, we find that lowering adult survival may, in contrast to classic bet-hedging theory, result in less spreading of germination by decreasing density-dependent competition. These models extend insights from bet-hedging theory to perennials and explore how competitive communities may be affected by ongoing changes in climate and seasonality patterns.

Proximity to oilseed rape fields affects plant pollination and pollinator-mediated selection on a co-flowering plant on the Tibetan Plateau.

The ecological effects of mass-flowering crops on pollinator abundance and species richness of neighbouring habitats are well established, yet the potential evolutionary consequences remain unclear. We studied effects of proximity to a mass-flowering crop on the pollination of local co-flowering plants and on patterns of natural selection on a pollination-generalised plant on the Tibetan Plateau. We recorded pollinator visitation rates and community composition at different distances (near vs. far) to oilseed rape (Brassica napus) fields in two habitat types and quantified pollinator-mediated selection on attractive traits of Trollius ranunculoides. The proximity to oilseed rape increased pollinator visitation in neighbouring alpine meadows and changed pollinator composition in neighbouring shrub meadows. Trollius ranunculoides in the alpine meadow near oilseed rape received three times more pollinator visits (mainly bees) and consequently had a 16.5% increase in seed set but also received slightly more heterospecific pollen per stigma. In contrast, pollinator visitation to T. ranunculoides in the shrub meadow near oilseed rape was three times lower (mainly flies), leading to a 10.7% lower seed despite no effect on pollen deposition. The proximity to the oilseed rape field intensified pollinator-mediated selection on flower size and weakened selection on flower height of T. ranunculoides in the alpine meadow but did not affect phenotypic selection on either trait in the shrub meadow. Our study highlights context-dependent variation in plant-pollinator interactions close to mass-flowering oilseed rape, suggesting potential effects on the evolution of flower traits of native plants through altered pollinator-mediated selection. However, context dependence may make these effects difficult to predict.

Analysis of trait-performance-fitness relationships reveals pollinator-mediated selection on orchid pollination traits.

PREMISE: The role of pollinators in evolutionary floral divergence has spurred substantial effort into measuring pollinator-mediated phenotypic selection and its variation in space and time. For such estimates, the fitness consequences of pollination processes must be separated from other factors affecting fitness. METHODS: We built a fitness function linking phenotypic traits of food-deceptive orchids to female reproductive success by including pollinator visitation and pollen deposition as intermediate performance components and used the fitness function to estimate the strength of pollinator-mediated selection through female reproductive success. We also quantified male performance as pollinarium removal and assessed similarity in trait effects on male and female performance. RESULTS: The proportion of plants visited at least once by an effective pollinator was moderate to high, ranging from 53.7% to 85.1%. Tall, many-flowered plants were often more likely to be visited and pollinated. Given effective pollination, pollen deposition onto stigmas tended to be more likely for taller plants. Pollen deposition further depended on traits affecting the physical fit of pollinators to flowers (flower size, spur length), though the exact relationships varied in time and space. Using the fitness function to assess pollinator-mediated selection through female reproductive success acting on multiple traits, we found that selection varied detectably among taxa after accounting for sampling uncertainty. Across taxa, selection on most traits was stronger on average and more variable when pollination was less reliable. CONCLUSIONS: These results support pollination-related trait-performance-fitness relationships and thus pollinator-mediated selection on traits functionally involved in the pollination process.

Evolvability and trait function predict phenotypic divergence of plant populations.

Understanding the causes and limits of population divergence in phenotypic traits is a fundamental aim of evolutionary biology, with the potential to yield predictions of adaptation to environmental change. Reciprocal transplant experiments and the evaluation of optimality models suggest that local adaptation is common but not universal, and some studies suggest that trait divergence is highly constrained by genetic variances and covariances of complex phenotypes. We analyze a large database of population divergence in plants and evaluate whether evolutionary divergence scales positively with standing genetic variation within populations (evolvability), as expected if genetic constraints are evolutionarily important. We further evaluate differences in divergence and evolvability-divergence relationships between reproductive and vegetative traits and between selfing, mixed-mating, and outcrossing species, as these factors are expected to influence both patterns of selection and evolutionary potentials. Evolutionary divergence scaled positively with evolvability. Furthermore, trait divergence was greater for vegetative traits than for floral (reproductive) traits, but largely independent of the mating system. Jointly, these factors explained ~40% of the variance in evolutionary divergence. The consistency of the evolvability-divergence relationships across diverse species suggests substantial predictability of trait divergence. The results are also consistent with genetic constraints playing a role in evolutionary divergence.

Evolvability and constraint in the evolution of three-dimensional flower morphology.

PREMISE: Flower phenotypes evolve to attract pollinators and to ensure efficient pollen transfer to and from the bodies of pollinators or, in self-compatible bisexual flowers, between anthers and stigmas. If functionally interacting traits are genetically correlated, response to selection may be subject to genetic constraints. Genetic constraints can be assessed by quantifying standing genetic variation in (multivariate) phenotypic traits and by asking how much the available variation is reduced under specific assumptions about phenotypic selection on functionally interacting and genetically correlated traits. METHODS: We evaluated multivariate evolvability and potential genetic constraints underlying the evolution of the three-dimensional structure of Dalechampia blossoms. First, we used data from a greenhouse crossing design to estimate the G matrix for traits representing the relative positions of male and female sexual organs (anthers and stigmas) and used the G matrix to ask how genetic variation is distributed in multivariate space. To assess the evolutionary importance of genetic constraints, we related standing genetic variation across phenotypic space to evolutionary divergence of population and species in the same phenotypic directions. RESULTS: Evolvabilities varied substantially across phenotype space, suggesting that certain traits or trait combinations may be subject to strong genetic constraint. Traits involved functionally in flower-pollinator fit and autonomous selfing exhibited considerable independent evolutionary potential, but population and species divergence tended to occur in phenotypic directions associated with greater-than-average evolvability. CONCLUSIONS: These results are consistent with the hypothesis that genetic constraints can hamper joint trait evolution towards optimum flower-pollinator fit and optimum self-pollination rates.

Measuring, comparing and interpreting phenotypic selection on floral scent.

Natural selection on floral scent composition is a key element of the hypothesis that pollinators and other floral visitors drive scent evolution. The measure of such selection is complicated by the high-dimensional nature of floral scent data and uncertainty about the cognitive processes involved in scent-mediated communication. We use dimension reduction through reduced-rank regression to jointly estimate a scent composite trait under selection and the strength of selection acting on this trait. To assess and compare variation in selection on scent across species, time and space, we reanalyse 22 datasets on six species from four previous studies. The results agreed qualitatively with previous analyses in terms of identifying populations and scent compounds subject to stronger selection but also allowed us to evaluate and compare the strength of selection on scent across studies. Doing so revealed that selection on floral scent was highly variable, and overall about as common and as strong as selection on other phenotypic traits involved in pollinator attraction or pollen transfer. These results are consistent with an important role of floral scent in pollinator attraction. Our approach should be useful for further studies of plant-animal communication and for studies of selection on other high-dimensional phenotypes. In particular, our approach will be useful for studies of pollinator-mediated selection on complex scent blends comprising many volatiles, and when no prior information on the physiological responses of pollinators to scent compounds is available.

Genetics of quantitative traits with dominance under stabilizing and directional selection in partially selfing species.

Recurrent self-fertilization is thought to lead to reduced adaptive potential by decreasing the genetic diversity of populations, thus leading selfing lineages down an evolutionary "blind alley." Although well supported theoretically, empirical support for reduced adaptability in selfing species is limited. One limitation of classical theoretical models is that they assume pure additivity of the fitness-related traits that are under stabilizing selection, despite ample evidence that quantitative traits are subject to dominance. Here, we relax this assumption and explore the effect of dominance on a fitness-related trait under stabilizing selection for populations that differ in selfing rates. By decomposing the genetic variance into additional components specific to inbred populations, we show that dominance components can explain a substantial part of the genetic variance of inbred populations. We also show that ignoring these components leads to an upward bias in the predicted response to selection. Finally, we show that when considering the effect of dominance, the short-term evolutionary potential of populations remains comparable across the entire gradient in outcrossing rates, and genetic associations can even make selfing populations more evolvable on the longer term, reconciling theoretical, and empirical results.

Evolutionary and ecological processes influencing chemical defense variation in an aposematic and mimetic Heliconius butterfly.

Chemical defences against predators underlie the evolution of aposematic coloration and mimicry, which are classic examples of adaptive evolution. Surprisingly little is known about the roles of ecological and evolutionary processes maintaining defence variation, and how they may feedback to shape the evolutionary dynamics of species. Cyanogenic Heliconius butterflies exhibit diverse warning color patterns and mimicry, thus providing a useful framework for investigating these questions. We studied intraspecific variation in de novo biosynthesized cyanogenic toxicity and its potential ecological and evolutionary sources in wild populations of Heliconius erato along environmental gradients, in common-garden broods and with feeding treatments. Our results demonstrate substantial intraspecific variation, including detectable variation among broods reared in a common garden. The latter estimate suggests considerable evolutionary potential in this trait, although predicting the response to selection is likely complicated due to the observed skewed distribution of toxicity values and the signatures of maternal contributions to the inheritance of toxicity. Larval diet contributed little to toxicity variation. Furthermore, toxicity profiles were similar along steep rainfall and altitudinal gradients, providing little evidence for these factors explaining variation in biosynthesized toxicity in natural populations. In contrast, there were striking differences in the chemical profiles of H. erato from geographically distant populations, implying potential local adaptation in the acquisition mechanisms and levels of defensive compounds. The results highlight the extensive variation and potential for adaptive evolution in defense traits for aposematic and mimetic species, which may contribute to the high diversity often found in these systems.

Experimental evidence that effects of megaherbivores on mesoherbivore space use are influenced by species' traits.

The extinction of 80% of megaherbivore (>1,000 kg) species towards the end of the Pleistocene altered vegetation structure, fire dynamics and nutrient cycling world-wide. Ecologists have proposed (re)introducing megaherbivores or their ecological analogues to restore lost ecosystem functions and reinforce extant but declining megaherbivore populations. However, the effects of megaherbivores on smaller herbivores are poorly understood. We used long-term exclusion experiments and multispecies hierarchical models fitted to dung counts to test (a) the effect of megaherbivores (elephant and giraffe) on the occurrence (dung presence) and use intensity (dung pile density) of mesoherbivores (2-1,000 kg), and (b) the extent to which the responses of each mesoherbivore species was predictable based on their traits (diet and shoulder height) and phylogenetic relatedness. Megaherbivores increased the predicted occurrence and use intensity of zebras but reduced the occurrence and use intensity of several other mesoherbivore species. The negative effect of megaherbivores on mesoherbivore occurrence was stronger for shorter species, regardless of diet or relatedness. Megaherbivores substantially reduced the expected total use intensity (i.e. cumulative dung density of all species) of mesoherbivores, but only minimally reduced the expected species richness (i.e. cumulative predicted occurrence probabilities of all species) of mesoherbivores (by <1 species). Simulated extirpation of megaherbivores altered use intensity by mesoherbivores, which should be considered during (re)introductions of megaherbivores or their ecological proxies. Species' traits (in this case shoulder height) may be more reliable predictors of mesoherbivores' responses to megaherbivores than phylogenetic relatedness, and may be useful for predicting responses of data-limited species.

Using ecological context to interpret spatiotemporal variation in natural selection.

Spatiotemporal variation in natural selection is expected, but difficult to estimate. Pollinator-mediated selection on floral traits provides a good system for understanding and linking variation in selection to differences in ecological context. We studied pollinator-mediated selection in five populations of Dalechampia scandens (Euphorbiaceae) in Costa Rica and Mexico. Using a nonlinear path-analytical approach, we assessed several functional components of selection, and linked variation in pollinator-mediated selection across time and space to variation in pollinator assemblages. After correcting for estimation error, we detected moderate variation in net selection on two out of four blossom traits. Both the opportunity for selection and the mean strength of selection decreased with increasing reliability of cross-pollination. Selection for pollinator attraction was consistently positive and stronger on advertisement than reward traits. Selection on traits affecting pollen transfer from the pollinator to the stigmas was strong only when cross-pollination was unreliable and there was a mismatch between pollinator and blossom size. These results illustrate how consideration of trait function and ecological context can facilitate both the detection and the causal understanding of spatiotemporal variation in natural selection.

Host-plant availability drives the spatiotemporal dynamics of interacting metapopulations across a fragmented landscape.

The dynamics of ecological communities depend partly on species interactions within and among trophic levels. Experimental work has demonstrated the impact of species interactions on the species involved, but it remains unclear whether these effects can also be detected in long-term time series across heterogeneous landscapes. We analyzed a 19-yr time series of patch occupancy by the Glanville fritillary butterfly Melitaea cinxia, its specialist parasitoid wasp Cotesia melitaearum, and the specialist fungal pathogen Podosphaera plantaginis infecting Plantago lanceolata, a host plant of the Glanville fritillary. These species share a network of more than 4,000 habitat patches in the Åland islands, providing a metacommunity data set of unique spatial and temporal resolution. To assess the influence of interactions among the butterfly, parasitoid, and mildew on metacommunity dynamics, we modeled local colonization and extinction rates of each species while including or excluding the presence of potentially interacting species in the previous year as predictors. The metapopulation dynamics of all focal species varied both along a gradient in host plant abundance, and spatially as indicated by strong effects of local connectivity. Colonization and to a lesser extent extinction rates depended also on the presence of interacting species within patches. However, the directions of most effects differed from expectations based on previous experimental and modeling work, and the inferred influence of species interactions on observed metacommunity dynamics was limited. These results suggest that although local interactions among the butterfly, parasitoid, and mildew occur, their roles in metacommunity spatiotemporal dynamics are relatively weak. Instead, all species respond to variation in plant abundance, which may in turn fluctuate in response to variation in climate, land use, or other environmental factors.

Refining predictions of metacommunity dynamics by modeling species non-independence.

Predicting the dynamics of biotic communities is difficult because species' environmental responses are not independent, but covary due to shared or contrasting ecological strategies and the influence of species interactions. We used latent-variable joint species distribution models to analyze paired historical and contemporary inventories of 585 vascular plant species on 471 islands in the southwest Finnish archipelago. Larger, more heterogeneous islands were characterized by higher colonization rates and lower extinction rates. Ecological and taxonomical species groups explained small but detectable proportions of variance in species' environmental responses. To assess the potential influence of species interactions on community dynamics, we estimated species associations as species-to-species residual correlations for historical occurrences, for colorizations, and for extinctions. Historical species associations could to some extent predict joint colonization patterns, but the overall estimated influence of species associations on community dynamics was weak. These results illustrate the benefits of considering metacommunity dynamics within a joint framework, but also suggest that any influence of species interactions on community dynamics may be hard to detect from observational data.

Joint species distribution modelling with the r-package Hmsc.

Joint Species Distribution Modelling (JSDM) is becoming an increasingly popular statistical method for analysing data in community ecology. Hierarchical Modelling of Species Communities (HMSC) is a general and flexible framework for fitting JSDMs. HMSC allows the integration of community ecology data with data on environmental covariates, species traits, phylogenetic relationships and the spatio-temporal context of the study, providing predictive insights into community assembly processes from non-manipulative observational data of species communities.The full range of functionality of HMSC has remained restricted to Matlab users only. To make HMSC accessible to the wider community of ecologists, we introduce Hmsc 3.0, a user-friendly r implementation.We illustrate the use of the package by applying Hmsc 3.0 to a range of case studies on real and simulated data. The real data consist of bird counts in a spatio-temporally structured dataset, environmental covariates, species traits and phylogenetic relationships. Vignettes on simulated data involve single-species models, models of small communities, models of large species communities and models for large spatial data. We demonstrate the estimation of species responses to environmental covariates and how these depend on species traits, as well as the estimation of residual species associations. We demonstrate how to construct and fit models with different types of random effects, how to examine MCMC convergence, how to examine the explanatory and predictive powers of the models, how to assess parameter estimates and how to make predictions. We further demonstrate how Hmsc 3.0 can be applied to normally distributed data, count data and presence-absence data.The package, along with the extended vignettes, makes JSDM fitting and post-processing easily accessible to ecologists familiar with r.

Linking Plant Functional Ecology to Island Biogeography.

The study of insular systems has a long history in ecology and biogeography. Island plants often differ remarkably from their noninsular counterparts, constituting excellent models for exploring eco-evolutionary processes. Trait-based approaches can help to answer important questions in island biogeography, yet plant trait patterns on islands remain understudied. We discuss three key hypotheses linking functional ecology to island biogeography: (i) plants in insular systems are characterized by distinct functional trait syndromes (compared with noninsular environments); (ii) these syndromes differ between true islands and terrestrial habitat islands; and (iii) island characteristics influence trait syndromes in a predictable manner. We are convinced that implementing trait-based comparative approaches would considerably further our understanding of plant ecology and evolution in insular systems.