Pierre-Olivier Cheptou

Plant mating systems in a changing world

There is increasing evidence that human disturbance can negatively impact plant-pollinator interactions such as outcross pollination. We present a meta-analysis of 22 studies involving 27 plant species showing a significant reduction in the proportion of seeds outcrossed in response to anthropogenic habitat modifications. We discuss the evolutionary consequences of disturbance on plant mating systems, and in particular whether reproductive assurance through selfing effectively compensates for reduced outcrossing. The extent to which disturbance reduces pollinator versus mate availability could generate diverse selective forces on reproductive traits. Investigating how anthropogenic change influences plant mating will lead to new opportunities for better understanding of how mating systems evolve, as well as of the ecological and evolutionary consequences of human activities and how to mitigate them.

Analysis of Inbreeding Depression in Mixed-Mating Plants Provides Evidence for Selective Interference and Stable Mixed Mating

Hermaphroditic individuals can produce both selfed and outcrossed progeny, termed mixed mating. General theory predicts that mixed‐mating populations should evolve quickly toward high rates of selfing, driven by rapid purging of genetic load and loss of inbreeding depression (ID), but the substantial number of mixed‐mating species observed in nature calls this prediction into question. Lower average ID reported for selfing than for outcrossing populations is consistent with purging and suggests that mixed‐mating taxa in evolutionary transition will have intermediate ID. We compared the magnitude of ID from published estimates for highly selfing (r > 0.8), mixed‐mating (0.2 ≤r≥ 0.8), and highly outcrossing (r < 0.2) plant populations across 58 species. We found that mixed‐mating and outcrossing taxa have equally high average lifetime ID (δ= 0.58 and 0.54, respectively) and similar ID at each of four life‐cycle stages. These results are not consistent with evolution toward selfing in most mixed‐mating taxa. We suggest that prevention of purging by selective interference could explain stable mixed mating in many natural populations. We identify critical gaps in the empirical data on ID and outline key approaches to filling them.

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.

Enemy release but no evolutionary loss of defence in a plant invasion: an inter-continental reciprocal transplant experiment

When invading new regions exotic species may escape from some of their natural enemies. Reduced top–down control (“enemy release”) following this escape is often invoked to explain demographic expansion of invasive species and also may alter the selective regime for invasive species: reduced damage can allow resources previously allocated to defence to be reallocated to other functions like growth and reproduction. This reallocation may provide invaders with an “evolution of increased competitive ability” over natives that defend themselves against specialist enemies. We tested for enemy release and the evolution of increased competitive ability in the North American native ragweed (Ambrosia artemisiifolia: Asteraceae), which currently is invading France. We found evidence of enemy release in natural field populations from the invaded and native ranges. Further we carried out a reciprocal transplant experiment, comparing several life history traits of plants from two North American (Ontario and South Carolina) and one French population in four common gardens on both continents. French and Canadian plants had similar flowering phenologies, flowering earlier than plants from further south in the native range. This may suggest that invasive French plants originated from similar latitudes to the Canadian population sampled. As with natural populations, experimental plants suffered far less herbivore damage in France than in Ontario. This difference in herbivory translated into increased growth but not into increased size or vigour. Moreover, we found that native genotypes were as damaged as invading ones in all experimental sites, suggesting no evolutionary loss of defence against herbivores.

Clarifying Baker's Law

BACKGROUND Bakers Law states that colonization by self-compatible organisms is more likely to be successful than colonization by self-incompatible organisms because of the ability for self-compatible organisms to produce offspring without pollination agents. This simple model has proved very successful in plant ecology and has been applied to various contexts, including colonizing or ruderal species, islands colonizers, invasive species or mating system variation across distribution ranges. Moreover, it is one of the only models in population biology linking two traits of major importance in ecology, namely dispersal and mating system. Although Bakers Law has stimulated a large number of empirical studies reporting the association of self-fertilization and colonizing ability in various contexts, the data have not established a general pattern for the association of traits. SCOPE In this paper, a critical position is adopted to discuss and clarify Bakers Law. From the literature referring to Bakers Law, an analysis made regarding how mating success is considered in such studies and discrepancies with population genetics theory of mating systems are highlighted. The data reporting the association of self-fertilization and colonizing ability are also briefly reviewed and the potential bias in interpretation is discussed. Lastly, a recent theoretical model analysing the link between colonizing ability and self-fertilization is considered. CONCLUSIONS Evolutionary predictions are actually more complex than Bakers intuitive arguments. It appears that Bakers Law encompasses a variety of ecological scenarios, which cannot be considered a priori as equivalent. Questioning what has been considered as self-evident for more than 50 years seems a reasonable objective to analyse in-depth dispersal and mating system traits.

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.

Correlations among Fertility Components Can Maintain Mixed Mating in Plants

Classical models studying the evolution of self‐fertilization in plants conclude that only complete selfing and complete outcrossing are evolutionarily stable. In contrast with this prediction, 42% of seed‐plant species are reported to have rates of self‐fertilization between 0.2 and 0.8. We propose that many previous models fail to predict intermediate selfing rates because they do not allow for functional relationships among three components of reproductive fitness: self‐fertilized ovules, outcrossed ovules, and ovules sired by successful pollen export. Because the optimal design for fertility components may differ, conflicts among the alternative pathways to fitness are possible, and the greatest fertility may be achieved with some self‐fertilization. Here we develop and analyze a model to predict optimal selfing rates that includes a range of possible relationships among the three components of reproductive fitness, as well as the effects of evolving inbreeding depression caused by deleterious mutations and of selection on total seed number. We demonstrate that intermediate selfing is optimal for a wide variety of relationships among fitness components and that inbreeding depression is not a good predictor of selfing‐rate evolution. Functional relationships subsume the myriad effects of individual plant traits and thus offer a more general and simpler perspective on mating system evolution.

Allee effect and self-fertilization in hermaphrodites: reproductive assurance in demographically stable populations.

Abstract The fact that selfing increases seed set (reproductive assurance) has often been put forward as an important selective force for the evolution of selfing. However, the role of reproductive assurance in hermaphroditic populations is far from being clear because of a lack of theoretical work. Here, I propose a theoretical model that analyzes selffertilization in the presence of reproductive assurance. Because reproductive assurance directly influences the per capita growth rate, I developed an explicit demographic model for partial selfers in the presence of reproductive assurance, specifically when outcrossing is limited by the possibility of pollen transfer (Allee effect). Mating system parameters are derived as a function of the underlying demographical parameters. The functional link between population demography and mating system parameters (reproductive assurance, selfing rate) can be characterized. The demographic model permits the analysis of the evolution of self‐fertilization in stable populations when reproductive assurance occurs. The model reveals some counterintuitive results such as the fact that increasing the fraction of selfed ovules can, in certain circumstances, increase the fraction of outcrossed ovules. Moreover, I demonstrate that reproductive assurance per se cannot account for the evolution of stable mixed selfing rates. Also, the model reveals that the extinction of outcrossing populations depends on small changes in population density (ecological perturbations), while the transition from outcrossing to selfing can, in certain cases, lead the population to extinction (evolutionary suicide). More generally, this paper highlights the fact that self‐fertilization affects both the dynamics of individuals and the dynamics of selfing genes in hermaphroditic populations.

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.

The effect of drought stress on inbreeding depression in four populations of the Mediterranean outcrossing plant Crepis sancta (Asteraceae)

The effect of physiological stress on the magnitude of inbreeding depression in plants has been the subject of few studies and is currently controversial because of contradictory results. We measured the inbreeding depression at three drought stress levels, precisely defined by a preliminary physiological experiment. We also tested the hypothesis that more highly self-compatible populations exhibit reduced inbreeding depression due to purging of deleterious mutations. The study was conducted on two populations of the annual and allogamous plant Crepis sancta collected from the French Mediterranean region and two other populations from marginal areas with various self-incompatibility levels. Drought stress did not increase inbreeding depression in terms of plant mortality but significantly increased the inbreeding depression for the date of first flowering, number of heads per plant and relative growth rate. The most self-fertile marginal population showed an absence of inbreeding depression in most of the measured traits indicating that purging could have taken place in this population. The three others populations showed relatively low and similar estimates of inbreeding depression (δ ≈ 0.35). The relatively low values obtained compared to the results found in allogamous plants suggests that the absence of competition for C. sancta in our experiment probably underestimated the effects of inbreeding in natural populations where competition occurs.