A user-friendly method to get automated pollen analysis from environmental samples.

Automated pollen analysis is not yet efficient on environmental samples containing many pollen taxa and debris, which are typical in most pollen-based studies. Contrary to classification, detection remains overlooked although it is the first step from which errors can propagate. Here, we investigated a simple but efficient method to automate pollen detection for environmental samples, optimizing workload and performance. We applied the YOLOv5 algorithm on samples containing debris and c. 40 Mediterranean plant taxa, designed and tested several strategies for annotation, and analyzed variation in detection errors. About 5% of pollen grains were left undetected, while 5% of debris were falsely detected as pollen. Undetected pollen was mainly in poor-quality images, or of rare and irregular morphology. Pollen detection remained effective when applied to samples never seen by the algorithm, and was not improved by spending time to provide taxonomic details. Pollen detection of a single model taxon reduced annotation workload, but was only efficient for morphologically differentiated taxa. We offer guidelines to plant scientists to analyze automatically any pollen sample, providing sound criteria to apply for detection while using common and user-friendly tools. Our method contributes to enhance the efficiency and replicability of pollen-based studies.

Assortative mating can help adaptation of flowering time to a changing climate: Insights from a polygenic model.

Several empirical studies report fast evolutionary changes in flowering time in response to contemporary climate change. Flowering time is a polygenic trait under assortative mating, since flowering time of mates must overlap. Here, we test whether assortative mating, compared with random mating, can help better track a changing climate. For each mating pattern, our individual-based model simulates a population evolving in a climate characterized by stabilizing selection around an optimal flowering time, which can change directionally and/or fluctuate. We also derive new analytical predictions from a quantitative genetics model for the expected genetic variance at equilibrium, and its components, the lag of the population to the optimum and the population mean fitness. We compare these predictions between assortative and random mating, and to our simulation results. Assortative mating, compared with random mating, has antagonistic effects on genetic variance: it generates positive associations among similar allelic effects, which inflates the genetic variance, but it decreases genetic polymorphism, which depresses the genetic variance. In a stationary environment with substantial stabilizing selection, assortative mating affects little the genetic variance compared with random mating. In a changing climate, assortative mating however increases genetic variance compared to random mating, which diminishes the lag of the population to the optimum, and in most scenarios translates into a fitness advantage relative to random mating. The magnitude of this fitness advantage depends on the extent to which genetic variance limits adaptation, being larger for faster environmental changes and weaker stabilizing selection.

Long-term effects of global change on occupancy and flight period of wild bees in Belgium.

Global change affects species by modifying their abundance, spatial distribution, and activity period. The challenge is now to identify the respective drivers of those responses and to understand how those responses combine to affect species assemblages and ecosystem functioning. Here we correlate changes in occupancy and mean flight date of 205 wild bee species in Belgium with temporal changes in temperature trend and interannual variation, agricultural intensification, and urbanization. Over the last 70 years, bee occupancy decreased on average by 33%, most likely because of agricultural intensification, and flight period of bees advanced on average by 4 days, most likely because of interannual temperature changes. Those responses resulted in a synergistic effect because species which increased in occupancy tend to be those that have shifted their phenologies earlier in the season. This leads to an overall advancement and shortening of the pollination season by 9 and 15 days respectively, with lower species richness and abundance compared to historical pollinator assemblages, except at the early start of the season. Our results thus suggest a strong decline in pollination function and services.

Mating systems and avoidance of inbreeding depression as evolutionary drivers of pollen limitation in animal-pollinated self-compatible plants.

Background and Aims: Most theory addressing the evolution of pollen limitation in flowering plants focuses on stochasticity in the relative abundance of plant and pollinator populations affecting trade-offs in resource allocation to ovule production or pollinator attraction vs. seed maturation. Mating system evolution is an underappreciated but potentially widespread additional mechanism for the evolutionary emergence of pollen limitation in animal-pollinated self-compatible plants. Methods: We model individual plant flowering phenologies influencing both pollinator attraction and geitonogamous self-fertilization caused by pollinator movements among flowers within plants, incorporating demographic but not environmental stochasticity. Plant phenology and the resulting pollen limitation are analysed at evolutionarily stable equilibria (ESS). Pollen limitation is measured by two quantities: the proportion of unpollinated flowers and the reduction in maternal fitness caused by inbreeding depression in selfed seeds. Key Results: When pollinators visit multiple flowers per plant, pollen limitation is never minimized at an ESS and results from the evolution of flowering phenologies balancing the amount and genetic composition (outbred vs. inbred) of pollen receipt. Conclusions: Results are consistent with previous theory demonstrating that pollen limitation can be an evolved property, not just a constraint; they complement existing models by showing that plant avoidance of inbreeding depression constitutes a genetic mechanism contributing to evolution of pollen limitation, in addition to ecological mechanisms previously studied.

Effects of host plant on life-history traits in the polyphagous spider mite Tetranychus urticae.

Studying antagonistic coevolution between host plants and herbivores is particularly relevant for polyphagous species that can experience a great diversity of host plants with a large range of defenses. Here, we performed experimental evolution with the polyphagous spider mite Tetranychus urticae to detect how mites can exploit host plants. We thus compared on a same host the performance of replicated populations from an ancestral one reared for hundreds of generations on cucumber plants that were shifted to either tomato or cucumber plants. We controlled for maternal effects by rearing females from all replicated populations on either tomato or cucumber leaves, crossing this factor with the host plant in a factorial design. About 24 generations after the host shift and for all individual mites, we measured the following fitness components on tomato leaf fragments: survival at all stages, acceptance of the host plant by juvenile and adult mites, longevity, and female fecundity. The host plant on which mite populations had evolved did not affect the performance of the mites, but only affected their sex ratio. Females that lived on tomato plants for circa 24 generations produced a higher proportion of daughters than did females that lived on cucumber plants. In contrast, maternal effects influenced juvenile survival, acceptance of the host plant by adult mites and female fecundity. Independently of the host plant species on which their population had evolved, females reared on the tomato maternal environment produced offspring that survived better on tomato as juveniles, but accepted less this host plant as adults and had a lower fecundity than did females reared on the cucumber maternal environment. We also found that temporal blocks affected mite dispersal and both female longevity and fecundity. Taken together, our results show that the host plant species can affect critical parameters of population dynamics, and most importantly that maternal and environmental conditions can facilitate colonization and exploitation of a novel host in the polyphagous T. urticae, by affecting dispersal behavior (host acceptance) and female fecundity.

Pollination ecology and inbreeding depression control individual flowering phenologies and mixed mating.

We analyze evolution of individual flowering phenologies by combining an ecological model of pollinator behavior with a genetic model of inbreeding depression for plant viability. The flowering phenology of a plant genotype determines its expected daily floral display which, together with pollinator behavior, governs the population rate of geitonogamous selfing (fertilization among flowers on the same plant). Pollinators select plant phenologies in two ways: they are more likely to visit plants displaying more flowers per day, and they influence geitonogamous selfing and consequent inbreeding depression via their abundance, foraging behavior, and pollen carry-over among flowers on a plant. Our model predicts two types of equilibria at stable intermediate selfing rates for a wide range of pollinator behaviors and pollen transfer parameters. Edge equilibria occur at maximal or minimal selfing rates and are constrained by pollinators. Internal equilibria occur between edge equilibria and are determined by a trade-off between pollinator attraction to large floral displays and avoidance of inbreeding depression due to selfing. We conclude that unavoidable geitonogamous selfing generated by pollinator behavior can contribute to the common occurrence of stable mixed mating in plants.

Evaluation of genetic isolation within an island flora reveals unusually widespread local adaptation and supports sympatric speciation.

It is now recognized that speciation can proceed even when divergent natural selection is opposed by gene flow. Understanding the extent to which environmental gradients and geographical distance can limit gene flow within species can shed light on the relative roles of selection and dispersal limitation during the early stages of population divergence and speciation. On the remote Lord Howe Island (Australia), ecological speciation with gene flow is thought to have taken place in several plant genera. The aim of this study was to establish the contributions of isolation by environment (IBE) and isolation by community (IBC) to the genetic structure of 19 plant species, from a number of distantly related families, which have been subjected to similar environmental pressures over comparable time scales. We applied an individual-based, multivariate, model averaging approach to quantify IBE and IBC, while controlling for isolation by distance (IBD). Our analyses demonstrated that all species experienced some degree of ecologically driven isolation, whereas only 12 of 19 species were subjected to IBD. The prevalence of IBE within these plant species indicates that divergent selection in plants frequently produces local adaptation and supports hypotheses that ecological divergence can drive speciation in sympatry.

Flowering plants under global pollinator decline.

There is now compelling evidence of a reduction of pollinator richness and density at a global scale. In this opinion article, we argue that such pollinator decline intensifies pollen limitation and reduces plant reproductive success, threatening natural populations of extinction. We use genetic architecture and selection experiments on floral traits and evaluate the potential for plant reproductive strategies to adapt rapidly to new pollination environments. We propose that plant reproductive strategies could adapt to the current pollinator decline by decreasing or increasing their reliance to pollinators, for example, increasing autonomous selfing or reinforcing interactions with pollinators. We further discuss if and how adaptation of plant reproductive strategies can buffer the demographic consequences of pollinator decline, and possibly rescue plant populations from extinction.

Selection on variance in flowering time within and among individuals.

We model the impact of pollinator visitation rate and behavior on the short-term evolution of population flowering phenologies determined by the distributions of flowering times within and among individual plants. Evolution of population flowering phenologies depends on the phenotypic variances and heritabilities of the within-individual mean and variance of flowering time. In the ecological scenarios we investigate selection does not produce a correlation of the mean and variance of individual flowering time. Self-incompatibility causes weak stabilizing selection on flowering time that acts to reduce the within-individual variance in flowering time. Disruptive selection due to pollinator limitation acts mostly to increase the among-individual variance in flowering time. Stabilizing selection due to pollinator attraction, or short reproductive season, acts mostly to decrease the within-individual variance in flowering time. Temporal autocorrelation of environmental stochasticity in pollinator visitation rate strongly selects to increase the within-individual variance in flowering time. These predictions can be tested by measuring the causal factors described above, partitioning the variance in population phenology within and among individuals, and estimating the inheritance of, and selection on, within-individual mean and variance of flowering time.

Displacement of flowering phenologies among plant species by competition for generalist pollinators.

We model the evolution of allochronic isolation between sympatric animal-pollinated plant species via displacement of their flowering times. The plant species share generalist pollinators and either produce inviable hybrid seeds or do not hybridize at all. Displacement of flowering times between reproductively isolated species reduces competition for pollinators and the formation of inviable hybrid seeds. Under strong pollen limitation, competition for pollinators causes rapid evolution of allochronic isolation both for hybridizing and nonhybridizing species. Under weak pollen limitation, allochronic isolation evolves rapidly for hybridizing species but more slowly for nonhybridizing species. Positive density-dependent pollinator visitation rate at low flower densities facilitates allochronic isolation under weak pollen limitation. Allochronic isolation among sympatric species sharing generalist pollinators could be common under any intensity of pollen limitation if the flowering season is sufficiently long.

Incipient allochronic speciation due to non-selective assortative mating by flowering time, mutation and genetic drift.

We model the evolution of flowering time using a multilocus quantitative genetic model with non-selective assortative mating and mutation to investigate incipient allochronic speciation in a finite population. For quantitative characters with evolutionary parameters satisfying empirical observations and two approximate inequalities that we derived, disjunct clusters in the population flowering phenology originated within a few thousand generations in the absence of disruptive natural or sexual selection. Our simulations and the conditions we derived showed that cluster formation was promoted by limited population size, high mutational variance of flowering time, short individual flowering phenology and a long flowering season. By contrast, cluster formation was hindered by inbreeding depression, stabilizing selection and pollinator limitation. Our results suggest that incipient allochronic speciation in populations of limited size (satisfying two inequalities) could be a common phenomenon.