Ongoing convergent evolution of a selfing syndrome threatens plant-pollinator interactions.

Plant-pollinator interactions evolved early in the angiosperm radiation. Ongoing environmental changes are however leading to pollinator declines that may cause pollen limitation to plants and change the evolutionary pressures shaping plant mating systems. We used resurrection ecology methodology to contrast ancestors and contemporary descendants in four natural populations of the field pansy (Viola arvensis) in the Paris region (France), a depauperate pollinator environment. We combine population genetics analysis, phenotypic measurements and behavioural tests on a common garden experiment. Population genetics analysis reveals 27% increase in realized selfing rates in the field during this period. We documented trait evolution towards smaller and less conspicuous corollas, reduced nectar production and reduced attractiveness to bumblebees, with these trait shifts convergent across the four studied populations. We demonstrate the rapid evolution of a selfing syndrome in the four studied plant populations, associated with a weakening of the interactions with pollinators over the last three decades. This study demonstrates that plant mating systems can evolve rapidly in natural populations in the face of ongoing environmental changes. The rapid evolution towards a selfing syndrome may in turn further accelerate pollinator declines, in an eco-evolutionary feedback loop with broader implications to natural ecosystems.

Rapid evolution of selfing syndrome traits in Viola arvensis revealed by resurrection ecology.

PREMISE: As part of global change, climate warming and pollinator decline are expected to affect plant phenology and plant-pollinator interactions. This paper aims at characterizing rapid evolution of life history traits and floral traits over two decades in the wild pansy (Viola arvensis), a common weed in agrosystems. METHODS: We used a resurrection ecology approach with genotypes sampled in 1991 and 2012 from a population in Burgundy (France). The species has a mixed mating system (hereafter: mixed selfer) and presents a floral polymorphism. To correct for maternal effects, we measured plant traits in the second generation in a common garden (after a refreshing generation) to characterize plant evolution during the two decades. In addition, historical population selfing rates in 1991 and 2012 were inferred from microsatellites markers through heterozygote deficiency and identity disequilibrium. RESULTS: Phenotypic data revealed a significant advance in flowering date, reduced flower sizes and a higher propensity of plants to set seed by autonomous selfing. Moreover, we detected a change in color morph frequency with an increase of the pale morph frequency. In accordance with phenotypic data, the neutral genetic data revealed an increase in historical selfing rates from 0.68 in 1991 to 0.86 in 2012. CONCLUSIONS: Taken together, such data suggest that the wild pansy, a mixed selfer, is evolving a selfing syndrome that may be the consequence of reduced pollinator activity in agrosystems.

Season-dependent effect of cleistogamy in Lamium amplexicaule: flower type origin versus inbreeding status.

PREMISE: Inbreeding depression is traditionally considered a major factor favoring outcrossing in hermaphrodites. Recent experiments have shown that environmental conditions can influence the magnitude of inbreeding depression, but their relevance in natural populations is unclear. To investigate this, we studied the cleistogamous species Lamium amplexicaule, an annual species with individuals experiencing either spring or autumn environmental conditions. In this species, the proportion of cleistogamous/chasmogamous flowers changes according to seasonal cues (e.g., temperature, photoperiod). Our hypothesis was that the plasticity of cleistogamy is an adaptation to seasonal fitness variation in different flower progenies. METHODS: To test this hypothesis, we produced the three possible types of progenies through controlled crosses: (1) selfed progeny from cleistogamous flowers; (2) chasmogamous selfed progeny; and (3) chasmogamous outcrossed progeny. Progeny fitness was then measured in a common garden in the two reproduction seasons (autumn and spring). RESULTS: The results showed that season had a major impact on fitness. The fitness of the different progeny types changed across seasons, indicating that the effect of cleistogamy on progeny performance is season-dependent, consistent with a previous study in a similar environment. Surprisingly, the flower from which the progeny issued (cleistogamous or chasmogamous) had more impact on fitness than the inbred status of the progeny (selfed versus outcrossed), suggesting a potential role of epigenetic processes. CONCLUSIONS: The observed patterns of variation were not consistent either with adaptation to environment-dependent inbreeding depression or to variation in resource availability, but were possibly consistent with adaptation to seasonal pollinator activity.

A spatial Markovian framework for estimating regional and local dynamics of annual plants with dormancy.

Many species have a dormant stage in their life cycle, including seeds for plants. The dormancy stage influences the species dynamics but is often undetectable. One way to include dormancy is to model it as a hidden dynamical state within a Markovian framework. Models within this framework have already been proposed but with different limitations: only presence/absence observations are modelled, the dormancy stage is limited to one year, or colonisation from neighbouring patches is not taken into account. We propose a hidden Markov model that describes the local and regional dynamics of a species that can undergo dormancy with a potentially infinite dormancy time. Populations are modelled with abundance classes. Our model considers the colonisation process as the indistinguishable influence of neighbour non-dormant population states on a dormant population state in a patch. It would be expected that parameter estimation, hidden state estimation and prediction of the next non-dormant populations would have an exponential computational time in terms of the number of patches. However, we demonstrate that estimation, hidden state estimation and prediction are all achievable in a linear computational time. Numerical experiments on simulated data show that the state of dormant populations can easily be retrieved, as well as the state of future non-dormant populations. Our framework provides a simple and efficient tool that could be further used to analyse and compare annual plants dynamics like weed species survival strategies in crop fields.

A general method for estimating seed dormancy and colonisation in annual plants from the observation of existing flora.

In plant ecology, characterising colonisation and extinction in plant metapopulations is challenging due to the non-detectable seed bank that allows plants to emerge after several years of absence. In this study, we used a Hidden Markov Model to characterise seed dormancy, colonisation and germination solely from the presence-absence of standing flora. Applying the model to data from a long-term survey of 38 annual weeds across France, we identified three homogeneous functional groups: (1) species persisting preferentially through spatial colonisation, (2) species persisting preferentially through seed dormancy and (3) a mix of both strategies. These groups are consistent with existing ecological knowledge, demonstrating that ecologically meaningful parameters can be estimated from simple presence-absence observations. These results indicate that such studies could contribute to the design of weed management strategies. They also open the possibility of testing life-history theories such as the dormancy/colonisation trade-off in natura.

Dividing a Maternal Pie among Half-Sibs: Genetic Conflicts and the Control of Resource Allocation to Seeds in Maize.

Resource allocation to offspring is the battleground for various intrafamilial conflicts. Understanding these conflicts requires knowledge of how the different actors (mother, siblings with different paternal genotypes) influence resource allocation. In angiosperms, allocation of resources to seeds happens postfertilization, and the paternally inherited genome in offspring can therefore influence resource allocation. However, the precise mode of resource allocation-and, in particular, the occurrence of sibling rivalry-has rarely been investigated in plants. In this article, we develop a new method for analyzing the resource-allocation traits of the different actors (maternal sporophyte and half-sibs) using data obtained from a large-scale diallel cross experiment in maize involving mixed hand pollination and color markers to assess seed weight of known paternity. We found strong evidence for the occurrence of sibling rivalry: resources invested in an ear were allocated competitively, and offspring with different paternal genotypes aggressively competed for these resources, entailing a measurable direct cost to the mother. We also show how resource allocation can be described for each genotype by two maternal traits (source effect, average sink responsiveness) and two offspring traits (ability to attract maternal resources, competitive ability toward siblings). We will discuss how these findings help to understand how genetic conflicts shape resource-allocation traits in angiosperms.

Global biogeography of mating system variation in seed plants.

Latitudinal gradients in biotic interactions have been suggested as causes of global patterns of biodiversity and phenotypic variation. Plant biologists have long speculated that outcrossing mating systems are more common at low than high latitudes owing to a greater predictability of plant-pollinator interactions in the tropics; however, these ideas have not previously been tested. Here, we present the first global biogeographic analysis of plant mating systems based on 624 published studies from 492 taxa. We found a weak decline in outcrossing rate towards higher latitudes and among some biomes, but no biogeographic patterns in the frequency of self-incompatibility. Incorporating life history and growth form into biogeographic analyses reduced or eliminated the importance of latitude and biome in predicting outcrossing or self-incompatibility. Our results suggest that biogeographic patterns in mating system are more likely a reflection of the frequency of life forms across latitudes rather than the strength of plant-pollinator interactions.

Self-compatibility is over-represented on islands.

Because establishing a new population often depends critically on finding mates, individuals capable of uniparental reproduction may have a colonization advantage. Accordingly, there should be an over-representation of colonizing species in which individuals can reproduce without a mate, particularly in isolated locales such as oceanic islands. Despite the intuitive appeal of this colonization filter hypothesis (known as Baker's law), more than six decades of analyses have yielded mixed findings. We assembled a dataset of island and mainland plant breeding systems, focusing on the presence or absence of self-incompatibility. Because this trait enforces outcrossing and is unlikely to re-evolve on short timescales if it is lost, breeding system is especially likely to reflect the colonization filter. We found significantly more self-compatible species on islands than mainlands across a sample of > 1500 species from three widely distributed flowering plant families (Asteraceae, Brassicaceae and Solanaceae). Overall, 66% of island species were self-compatible, compared with 41% of mainland species. Our results demonstrate that the presence or absence of self-incompatibility has strong explanatory power for plant geographical patterns. Island floras around the world thus reflect the role of a key reproductive trait in filtering potential colonizing species in these three plant families.

The scope of Baker's law.

Baker's law refers to the tendency for species that establish on islands by long-distance dispersal to show an increased capacity for self-fertilization because of the advantage of self-compatibility when colonizing new habitat. Despite its intuitive appeal and broad empirical support, it has received substantial criticism over the years since it was proclaimed in the 1950s, not least because it seemed to be contradicted by the high frequency of dioecy on islands. Recent theoretical work has again questioned the generality and scope of Baker's law. Here, we attempt to discern where the idea is useful to apply and where it is not. We conclude that several of the perceived problems with Baker's law fall away when a narrower perspective is adopted on how it should be circumscribed. We emphasize that Baker's law should be read in terms of an enrichment of a capacity for uniparental reproduction in colonizing situations, rather than of high selfing rates. We suggest that Baker's law might be tested in four different contexts, which set the breadth of its scope: the colonization of oceanic islands, metapopulation dynamics with recurrent colonization, range expansions with recurrent colonization, and colonization through species invasions.

High lifetime inbreeding depression counteracts the reproductive assurance benefit of selfing in a mass-flowering shrub.

BACKGROUND: Decreases in mate and/or pollinator availability would be expected to affect the selective pressure on plant mating systems. An increase in self-fertilization may evolve to compensate for the negative effects of pollination failure. However, the benefit of selfing in variable pollination environments depends on the relative fitnesses of selfed and outcrossed progeny. We investigated the potential for selfing to provide reproductive assurance over the lifetime of a long-lived perennial species and its variation between plant patches of various sizes. Patch size is likely to affect mate and pollinator availabilities, thereby affecting pollination success and the rate of selfing. We estimated fruit and seed set, reproductive assurance, self-compatibility, the multilocus patch selfing rate and lifetime inbreeding depression in natural patches of Rhododendron ferrugineum (Ericaceae), a mass-flowering species characterized by considerable patch size variation (as estimated by the total number of inflorescences). RESULTS: Open seed set declined linearly with increasing patch size, whereas pollinator-mediated seed set (emasculated flowers) was not significantly affected. Progeny array analysis indicated that the selfing rate declined with increasing patch size, consistent with greater reproductive assurance in small sparse patches than in large, dense patches. However, fruit set and adult fitness decreased with decreasing patch size, with an estimated mean lifetime inbreeding depression of 0.9 (obtained by comparing F values in adults and progenies). CONCLUSIONS: Lifetime inbreeding depression strongly counteracts the advantage of reproductive assurance due to selfing in this long-lived species. The poor fitness of selfed offspring should counteract any evolution towards selfing, despite its potential to alleviate the negative consequences of pollen limitation. This study highlights the need to estimate lifetime inbreeding depression, together with mating system and pollination parameters, if we are to understand the actual benefit of selfing and avoid the overestimation of reproductive assurance.

A hemizygous supergene controls homomorphic and heteromorphic self-incompatibility systems in Oleaceae.

Self-incompatibility (SI) has evolved independently multiple times and prevents self-fertilization in hermaphrodite angiosperms. Several groups of Oleaceae such as jasmines exhibit distylous flowers, with two compatibility groups each associated with a specific floral morph.1 Other Oleaceae species in the olive tribe have two compatibility groups without associated morphological variation.2,3,4,5 The genetic basis of both homomorphic and dimorphic SI systems in Oleaceae is unknown. By comparing genomic sequences of three olive subspecies (Olea europaea) belonging to the two compatibility groups, we first locate the genetic determinants of SI within a 700-kb hemizygous region present only in one compatibility group. We then demonstrate that the homologous hemizygous region also controls distyly in jasmine. Phylogenetic analyses support a common origin of both systems, following a segmental genomic duplication in a common ancestor. Examination of the gene content of the hemizygous region in different jasmine and olive species suggests that the mechanisms determining compatibility groups and floral phenotypes (whether homomorphic or dimorphic) in Oleaceae rely on the presence/absence of two genes involved in gibberellin and brassinosteroid regulation.

Competition/colonization syndrome mediated by early germination in non-dispersing achenes in the heteromorphic species Crepis sancta.

BACKGROUND AND AIMS: The competition-colonization trade-off theory postulates that the competitive and colonizing abilities of organisms are negatively related; this trade-off has been proposed as a major force in the maintenance of diversity. In plants, the competition-colonization trade-off is often considered to result from variation in resource partitioning, thus generating heavy competitive (non-dispersing) seeds and light (dispersing) non-competitive seeds. Here, the possibility is explored that early germination provides a competitive advantage, thus mediating competitive interactions. METHODS: Using eight populations of the heterocarpic species Crepis sancta (Asteraceae), the possibility was tested that dispersing and non-dispersing achenes differ in germination timing, and the impact of early germination on individual fitness components was analysed in the context of intraspecific competition. To evaluate whether seed reserve varies among achene types, endosperm size was also measured by analysing photographs of cross-sections taken under a binocular microscope. KEY RESULTS AND CONCLUSIONS: The results show that non-dispersing achenes germinated 4 d earlier (on average) than dispersing achenes. It is also shown that early germination provides a positive advantage for the survival and final biomass of individuals, a pattern that was consistent over the eight populations and independent of achene type. Dispersing and non-dispersing achenes did not differ in terms of seed reserve (endosperm size). It is proposed that germination phenology may mediate the competition-colonization trade-off in Crepis sancta and the evolutionary significance of this phenomenon is discussed.

Determinants of extinction in fragmented plant populations: Crepis sancta (Asteraceae) in urban environments.

Local populations are subject to recurrent extinctions, and small populations are particularly prone to extinction. Both demographic (stochasticity and the Allee effect) and genetic factors (drift load and inbreeding depression) potentially affect extinction. In fragmented populations, regular dispersal may boost population sizes (demographic rescue effect) or/and reduce the local inbreeding level and genetic drift (genetic rescue effect), which can affect extinction risks. We studied extinction processes in highly fragmented populations of the common species Crepis sancta (Asteraceae) in urban habitats exhibiting a rapid turnover of patches. A four-year demographic monitoring survey and microsatellite genotyping of individuals allowed us to study the determinants of extinction. We documented a low genetic structure and an absence of inbreeding (estimated by multilocus heterozygosity), which suggest that genetic factors were not a major cause of patch extinction. On the contrary, local population size was the main factor in extinction, whereas connectivity was shown to decrease patch extinction, which we interpreted as a demographic rescue effect that was likely due to better pollination services for reproduction. This coupling of demographic and genetic tools highlighted the importance of dispersal in local patch extinctions of small fragmented populations connected by gene flow.

Environment-dependent inbreeding depression: its ecological and evolutionary significance.

Inbreeding depression is a major evolutionary and ecological force that influences population dynamics and the evolution of inbreeding-avoidance traits such as mating systems and dispersal. There is now compelling evidence that inbreeding depression is environment-dependent. Here, we discuss ecological and evolutionary consequences of environment-dependent inbreeding depression. The environmental dependence of inbreeding depression may be caused by environment-dependent phenotypic expression, environment-dependent dominance, and environment-dependent natural selection. The existence of environment-dependent inbreeding depression challenges classical models of inbreeding as caused by unconditionally deleterious alleles, and suggests that balancing selection may shape inbreeding depression in natural populations; loci associated with inbreeding depression in some environments may even contribute to adaptation to others. Environment-dependent inbreeding depression also has important, often neglected, ecological and evolutionary consequences: it can influence the demography of marginal or colonizing populations and alter adaptive optima of mating systems, dispersal, and their associated traits. Incorporating the environmental dependence of inbreeding depression into theoretical models and empirical studies is necessary for understanding the genetic and ecological basis of inbreeding depression and its consequences in natural populations.

Does seed mass drive interspecies variation in the effect of management practices on weed demography?

Optimizing the effect of management practices on weed population dynamics is challenging due to the difficulties in inferring demographic parameters in seed banks and their response to disturbance. Here, we used a long-term plant survey between 2006 and 2012 in 46 French vineyards and quantified the effects of management practices (tillage, mowing, and herbicide) on colonization, germination, and seed survival of 30 weed species in relation to their seed mass. To do so, we used a recent statistical approach to reliably estimate demographic parameters for plant populations with a seed bank using time series of presence-absence data, which we extended to account for interspecies variation in the effects of management practices on demographic parameters. Our main finding was that when the level of disturbance increased (i.e., in plots with a higher number of herbicides, tillage, or mowing treatments), colonization success and survival in large-seeded species increased faster than in small-seeded species. High disturbance through tillage increased survival in the seed bank of species with high seed mass. The application of herbicides increased germination, survival, and colonization probabilities of species with high seed mass. Mowing, representing habitats more competitive for light, increased the survival of species with high seed mass. Overall, the strong relationships between the effects of management practices and seed mass provide an indicator for predicting the dynamics of weed communities under disturbance.

Rapid divergent evolution of an annual plant across a latitudinal gradient revealed by seed resurrection.

Global change is expected to drive short-term evolution of natural populations. However, it remains unclear whether different populations are changing in unison. Here, we study contemporary evolution of growth-related and reproductive traits of three populations of Cyanus segetum facing warming and pollinator decline across a latitudinal gradient in France. We resurrected stored seeds sampled up to 24 years apart from northern, central-western, and southern populations and conducted an in situ common-garden experiment. To disentangle neutral from selection-driven differentiation, we calculated neutral genetic differentiation (FST ) and quantitative trait differentiation (QST ) between temporal samples. We found that phenotypic evolution was divergent across populations exhibiting different trends for rosette size, date of flowering, and capitula size. By measuring seed set as a proxy of fitness, we showed that samples with larger mean capitula size outperformed samples with smaller mean capitula size in the western and southern populations. Regression of traits on seed set showed that flowering date and capitula size are the primary determinants of fitness, and QST -FST comparisons indicated that natural selection has likely contributed to the shifts in flowering phenology and rosette size. These findings outline the potential for rescue of natural populations through contemporary evolution and emphasize the complex interplay between spatial and temporal variation in species' responses to global change.

Weeds: Against the Rules?

Establishing laws of plant and ecosystems functioning has been an overarching objective of functional and evolutionary ecology. However, most theories neglect the role of human activities in creating novel ecosystems characterized by species assemblages and environmental factors that are not observed in natural systems. We argue that agricultural weeds, as an emblematic case of such an 'ecological novelty', constitute an original and underutilized model for challenging current concepts in ecology and evolution. We highlight key aspects of weed ecology and evolutionary biology that can help to test and recast ecological and evolutionary laws in a changing world. We invite ecologists to seize upon weeds as a model system to improve our understanding of the short-term and long-term dynamics of ecological systems in the Anthropocene.

Paternity tests support a diallelic self-incompatibility system in a wild olive (Olea europaea subsp. laperrinei, Oleaceae).

Self-incompatibility (SI) is the main mechanism that favors outcrossing in plants. By limiting compatible matings, SI interferes in fruit production and breeding of new cultivars. In the Oleeae tribe (Oleaceae), an unusual diallelic SI system (DSI) has been proposed for three distantly related species including the olive (Olea europaea), but empirical evidence has remained controversial for this latter. The olive domestication is a complex process with multiple origins. As a consequence, the mixing of S-alleles from two distinct taxa, the possible artificial selection of self-compatible mutants and the large phenological variation of blooming may constitute obstacles for deciphering SI in olive. Here, we investigate cross-genotype compatibilities in the Saharan wild olive (O. e. subsp. laperrinei). As this taxon was geographically isolated for thousands of years, SI should not be affected by human selection. A population of 37 mature individuals maintained in a collection was investigated. Several embryos per mother were genotyped with microsatellites in order to identify compatible fathers that contributed to fertilization. While the pollination was limited by distance inside the collection, our results strongly support the DSI hypothesis, and all individuals were assigned to two incompatibility groups (G1 and G2). No self-fertilization was observed in our conditions. In contrast, crosses between full or half siblings were frequent (ca. 45%), which is likely due to a nonrandom assortment of related trees in the collection. Finally, implications of our results for orchard management and the conservation of olive genetic resources are discussed.

The rise of research on futures in ecology: rebalancing scenarios and predictions.

Concern about the ecological consequences of global change has increasingly stimulated ecologists to examine the futures of ecological systems. Studying futures is not only a crucial element of the interaction between science, management and decision making, but also a critical research challenge per se, especially because futures cannot be observed or experimented on. In addition, researchers can encounter methodological and theoretical difficulties, which make interpretations and predictions problematic. In the literature which deals with futures of ecological systems two main lines of research can be distinguished: a predictive approach, which dominates the literature, can be contrasted with a rarer number of studies that elaborate potential scenarios for ecological systems. Scenario approaches currently concern mainly contacts with stakeholders or decision makers, or the use of climate scenarios to derive projections about ecological futures. We argue that a new direction for ecological futures research could be explored by using ecological scenarios in combination with predictive models to further fundamental ecological research, in addition to enhancing its applied value.

Pollination fluctuations drive evolutionary syndromes linking dispersal and mating system.

The existence of a syndrome linking dispersal rate and mating system has long been debated in evolutionary ecology, especially in plants. Some verbal models hypothesize that the ability to self-fertilize may be associated with high dispersal, since completely outcrossing species cannot reproduce when they disperse to an empty destination site. However, empirical observations fail to support a clear trend, and an association of high colonizing ability with high outcrossing has been reported. Here we develop a general metapopulation model for the joint evolution of seed dispersal and self-fertilization when local pollen limitation varies stochastically over time. Under these assumptions, we study how dispersal and mating system influence each other through selection. We predict the existence of two consistent syndromes of traits: dispersing outcrossers and nondispersing (partial) selfers. These theoretical expectations contradict the classical view and shed new light on an old problem, allowing us to reinterpret empirical data. Finally, our predictions are discussed in light of empirical data concerning the association of seed dispersal mechanism and breeding system.