The homomorphic self-incompatibility system in Oleaceae is controlled by a hemizygous genomic region expressing a gibberellin pathway gene.

In flowering plants, outcrossing is commonly ensured by self-incompatibility (SI) systems. These can be homomorphic (typically with many different allelic specificities) or can accompany flower heteromorphism (mostly with just two specificities and corresponding floral types). The SI system of the Oleaceae family is unusual, with the long-term maintenance of only two specificities but often without flower morphology differences. To elucidate the genomic architecture and molecular basis of this SI system, we obtained chromosome-scale genome assemblies of Phillyrea angustifolia individuals and related them to a genetic map. The S-locus region proved to have a segregating 543-kb indel unique to one specificity, suggesting a hemizygous region, as observed in all distylous systems so far studied at the genomic level. Only one of the predicted genes in this indel region is found in the olive tree, Olea europaea, genome, also within a segregating indel. We describe complete association between the presence/absence of this gene and the SI types determined for individuals of seven distantly related Oleaceae species. This gene is predicted to be involved in catabolism of the gibberellic acid (GA) hormone, and experimental manipulation of GA levels in developing buds modified the male and female SI responses of the two specificities in different ways. Our results provide a unique example of a homomorphic SI system, where a single conserved gibberellin-related gene in a hemizygous indel underlies the long-term maintenance of two groups of reproductive compatibility.

Human-environment feedback and the consistency of proenvironmental behavior.

Addressing global environmental crises such as anthropogenic climate change requires the consistent adoption of proenvironmental behavior by a large part of a population. Here, we develop a mathematical model of a simple behavior-environment feedback loop to ask how the individual assessment of the environmental state combines with social interactions to influence the consistent adoption of proenvironmental behavior, and how this feeds back to the perceived environmental state. In this stochastic individual-based model, individuals can switch between two behaviors, 'active' (or actively proenvironmental) and 'baseline', differing in their perceived cost (higher for the active behavior) and environmental impact (lower for the active behavior). We show that the deterministic dynamics and the stochastic fluctuations of the system can be approximated by ordinary differential equations and a Ornstein-Uhlenbeck type process. By definition, the proenvironmental behavior is adopted consistently when, at population stationary state, its frequency is high and random fluctuations in frequency are small. We find that the combination of social and environmental feedbacks can promote the spread of costly proenvironmental behavior when neither, operating in isolation, would. To be adopted consistently, strong social pressure for proenvironmental action is necessary but not sufficient-social interactions must occur on a faster timescale compared to individual assessment, and the difference in environmental impact must be small. This simple model suggests a scenario to achieve large reductions in environmental impact, which involves incrementally more active and potentially more costly behavior being consistently adopted under increasing social pressure for proenvironmentalism.

Opposing effects of plant traits on diversification.

Species diversity can vary dramatically across lineages due to differences in speciation and extinction rates. Here, we explore the effects of several plant traits on diversification, finding that most traits have opposing effects on diversification. For example, outcrossing may increase the efficacy of selection and adaptation but also decrease mate availability, two processes with contrasting effects on lineage persistence. Such opposing trait effects can manifest as differences in diversification rates that depend on ecological context, spatiotemporal scale, and associations with other traits. The complexity of pathways linking traits to diversification suggests that the mechanistic underpinnings behind their correlations may be difficult to interpret with any certainty, and context dependence means that the effects of specific traits on diversification are likely to differ across multiple lineages and timescales. This calls for taxonomically and context-controlled approaches to studies that correlate traits and diversification.

Balancing selection and the crossing of fitness valleys in structured populations: diversification in the gametophytic self-incompatibility system.

The self-incompatibility locus (S-locus) of flowering plants displays a striking allelic diversity. How such a diversity has emerged remains unclear. In this article, we performed numerical simulations in a finite island population genetics model to investigate how population subdivision affects the diversification process at a S-locus, given that the two-gene architecture typical of S-loci involves the crossing of a fitness valley. We show that population structure slightly reduces the parameter range allowing for the diversification of self-incompatibility haplotypes (S-haplotypes), but at the same time also increases the number of these haplotypes maintained in the whole metapopulation. This increase is partly due to a higher rate of diversification and replacement of S-haplotypes within and among demes. We also show that the two-gene architecture leads to a higher diversity in structured populations compared with a simpler genetic architecture, where new S-haplotypes appear in a single mutation step. Overall, our results suggest that population subdivision can act in two opposite directions: it renders S-haplotypes diversification easier, although it also increases the risk that the self-incompatibility system is lost.

Revisiting the number of self-incompatibility alleles in finite populations: From old models to new results.

Under gametophytic self-incompatibility (GSI), plants are heterozygous at the self-incompatibility locus (S-locus) and can only be fertilized by pollen with a different allele at that locus. The last century has seen a heated debate about the correct way of modelling the allele diversity in a GSI population that was never formally resolved. Starting from an individual-based model, we derive the deterministic dynamics as proposed by Fisher (The genetical theory of natural selection - A complete, Variorum edition, Oxford University Press, 1958) and compute the stationary S-allele frequency distribution. We find that the stationary distribution proposed by Wright (Evolution, 18, 609, 1964) is close to our theoretical prediction, in line with earlier numerical confirmation. Additionally, we approximate the invasion probability of a new S-allele, which scales inversely with the number of resident S-alleles. Lastly, we use the stationary allele frequency distribution to estimate the population size of a plant population from an empirically obtained allele frequency spectrum, which complements the existing estimator of the number of S-alleles. Our expression of the stationary distribution resolves the long-standing debate about the correct approximation of the number of S-alleles and paves the way for new statistical developments for the estimation of the plant population size based on S-allele frequencies.

Widespread coexistence of self-compatible and self-incompatible phenotypes in a diallelic self-incompatibility system in Ligustrum vulgare (Oleaceae).

The breakdown of self-incompatibility (SI) in angiosperms is one of the most commonly observed evolutionary transitions. While multiple examples of SI breakdown have been documented in natural populations, there is strikingly little evidence of stable within-population polymorphism with both inbreeding (self-compatible) and outcrossing (self-incompatible) individuals. This absence of breeding system polymorphism corroborates theoretical expectations that predict that in/outbreeding polymorphism is possible only under very restricted conditions. However, theory also predicts that a diallelic sporophytic SI system should facilitate the maintenance of such polymorphism. We tested this prediction by studying the breeding system of Ligustrum vulgare L., an insect-pollinated hermaphroditic species of the Oleaceae family. Using stigma tests with controlled pollination and paternity assignment of open-pollinated progenies, we confirmed the existence of two self-incompatibility groups in this species. We also demonstrated the occurrence of self-compatible individuals in different populations of Western Europe arising from a mutation affecting the functioning of the pollen component of SI. Our results show that the observed low frequency of self-compatible individuals in natural populations is compatible with theoretical predictions only if inbreeding depression is very high.

The integrative biology of genetic dominance.

Dominance is a basic property of inheritance systems describing the link between a diploid genotype at a single locus and the resulting phenotype. Models for the evolution of dominance have long been framed as an opposition between the irreconcilable views of Fisher in 1928 supporting the role of largely elusive dominance modifiers and Wright in 1929, who viewed dominance as an emerging property of the structure of enzymatic pathways. Recent theoretical and empirical advances however suggest that these opposing views can be reconciled, notably using models investigating the regulation of gene expression and developmental processes. In this more comprehensive framework, phenotypic dominance emerges from departures from linearity between any levels of integration in the genotype-to-phenotype map. Here, we review how these different models illuminate the emergence and evolution of dominance. We then detail recent empirical studies shedding new light on the diversity of molecular and physiological mechanisms underlying dominance and its evolution. By reconciling population genetics and functional biology, we hope our review will facilitate cross-talk among research fields in the integrative study of dominance evolution.

On Deleterious Mutations in Perennials: Inbreeding Depression, Mutation Load, and Life-History Evolution.

AbstractIn angiosperms, perennials typically present much higher levels of inbreeding depression than annuals. One hypothesis to explain this pattern stems from the observation that inbreeding depression is expressed across multiple life stages in angiosperms. It posits that increased inbreeding depression in more long-lived species could be explained by differences in the way mutations affect fitness, through the life stages at which they are expressed. In this study, we investigate this hypothesis. We combine a physiological growth model and multilocus population genetics approaches to describe a full genotype-to-phenotype-to-fitness map. We study the behavior of mutations affecting growth or survival and explore their consequences in terms of inbreeding depression and mutation load. Although our results agree with empirical data only within a narrow range of conditions, we argue that they may point us toward the type of traits capable of generating high inbreeding depression in long-lived species-that is, traits under sufficiently strong selection, on which selection decreases sharply as life expectancy increases. Then we study the role deleterious mutations maintained at mutation-selection balance may play in the joint evolution of growth and survival strategies.

Inference with selection, varying population size, and evolving population structure: application of ABC to a forward-backward coalescent process with interactions.

Genetic data are often used to infer demographic history and changes or detect genes under selection. Inferential methods are commonly based on models making various strong assumptions: demography and population structures are supposed a priori known, the evolution of the genetic composition of a population does not affect demography nor population structure, and there is no selection nor interaction between and within genetic strains. In this paper, we present a stochastic birth-death model with competitive interactions and asexual reproduction. We develop an inferential procedure for ecological, demographic, and genetic parameters. We first show how genetic diversity and genealogies are related to birth and death rates, and to how individuals compete within and between strains. This leads us to propose an original model of phylogenies, with trait structure and interactions, that allows multiple merging. Second, we develop an Approximate Bayesian Computation framework to use our model for analyzing genetic data. We apply our procedure to simulated data from a toy model, and to real data by analyzing the genetic diversity of microsatellites on Y-chromosomes sampled from Central Asia human populations in order to test whether different social organizations show significantly different fertilities.

Evolution of self-incompatibility in the Brassicaceae: Lessons from a textbook example of natural selection.

Self-incompatibility (SI) is a self-recognition genetic system enforcing outcrossing in hermaphroditic flowering plants and results in one of the arguably best understood forms of natural (balancing) selection maintaining genetic variation over long evolutionary times. A rich theoretical and empirical population genetics literature has considerably clarified how the distribution of SI phenotypes translates into fitness differences among individuals by a combination of inbreeding avoidance and rare-allele advantage. At the same time, the molecular mechanisms by which self-pollen is specifically recognized and rejected have been described in exquisite details in several model organisms, such that the genotype-to-phenotype map is also pretty well understood, notably in the Brassicaceae. Here, we review recent advances in these two fronts and illustrate how the joint availability of detailed characterization of genotype-to-phenotype and phenotype-to-fitness maps on a single genetic system (plant self-incompatibility) provides the opportunity to understand the evolutionary process in a unique perspective, bringing novel insight on general questions about the emergence, maintenance, and diversification of a complex genetic system.

Stochastic Dynamics of Three Competing Clones: Conditions and Times for Invasion, Coexistence, and Fixation.

In large clonal populations, several clones generally compete, resulting in complex evolutionary and ecological dynamics: experiments show successive selective sweeps of favorable mutations as well as long-term coexistence of multiple clonal strains. The mechanisms underlying either coexistence or fixation of several competing strains have rarely been studied altogether. Conditions for coexistence have mostly been studied by population and community ecology, while rates of invasion and fixation have mostly been studied by population genetics. To provide a global understanding of the complexity of the dynamics observed in large clonal populations, we develop a stochastic model where three clones compete. Competitive interactions can be intransitive, and we suppose that strains enter the population via mutations or rare immigrations. We first describe all possible final states of the population, including stable coexistence of two or three strains or the fixation of a single strain. Second, we estimate the invasion and fixation times of a favorable mutant (or immigrant) entering the population in a single copy. We show that invasion and fixation can be slower or faster when considering complex competitive interactions. Third, we explore the parameter space assuming prior distributions of reproduction, death, and competition rates, and we estimate the likelihood of the possible dynamics. We show that when mutations can affect competitive interactions even slightly, stable coexistence is likely. We discuss our results in the context of the evolutionary dynamics of large clonal populations.

The joint evolution of lifespan and self-fertilization.

In Angiosperms, there exists a strong association between mating system and lifespan. Most self-fertilizing species are short-lived, and most predominant or obligate outcrossers are long-lived. This association is generally explained by the influence of lifespan on the evolution of the mating system, considering lifespan as fixed. Yet, lifespan can itself evolve, and the mating system may as well influence the evolution of lifespan, as is suggested by joint evolutionary shifts of lifespan and mating system between sister species. In this paper, we build modifier models to study the joint evolution of self-fertilization and lifespan, including both juvenile and adult inbreeding depression. We show that provided that inbreeding depression affects adult survival, self-fertilization is expected to promote evolution towards shorter lifespan, and that the range of conditions under which selfing can evolve rapidly shrinks as lifespan increases. We study the effects of inbreeding depression affecting various steps in the life cycle and discuss how extrinsic mortality conditions are expected to affect evolutionary associations. In particular, we show that selfers may sometimes remain short-lived even in a very stable habitat, as a strategy to avoid the deleterious effects of inbreeding.

Breakdown of gametophytic self-incompatibility in subdivided populations.

In many hermaphroditic flowering plants, self-fertilization is prevented by self-incompatibility (SI), often controlled by a single locus, the S-locus. In single isolated populations, the maintenance of SI depends chiefly on inbreeding depression and the number of SI alleles at the S-locus. In subdivided populations, however, population subdivision has complicated effects on both the number of SI alleles and the level of inbreeding depression, rendering the maintenance of SI difficult to predict. Here, we explore the conditions for the invasion of a self-compatible mutant in a structured population. We find that the maintenance of SI is strongly compromised when a population becomes subdivided. We show that this effect is mainly caused by the decrease in the local diversity of SI alleles rather than by a change in the dynamics of inbreeding depression. Strikingly, we also find that the diversity of SI alleles at the whole population level is a poor predictor of the maintenance of SI. We discuss the implications of our results for the interpretation of empirical data on the loss of SI in natural populations.

Rejuvenating functional responses with renewal theory.

Functional responses are widely used to describe interactions and resource exchange between individuals in ecology. The form given to functional responses dramatically affects the dynamics and stability of populations and communities. Despite their importance, functional responses are generally considered with a phenomenological approach, without clear mechanistic justifications from individual traits and behaviours. Here, we develop a bottom-up stochastic framework grounded in renewal theory that shows how functional responses emerge from the level of the individuals through the decomposition of interactions into different activities. Our framework has many applications for conceptual, theoretical and empirical purposes. First, we show how the mean and variance of classical functional responses are obtained with explicit ecological assumptions, for instance regarding foraging behaviours. Second, we give examples in specific ecological contexts, such as in nuptial-feeding species or size-dependent handling times. Finally, we demonstrate how to analyse data with our framework, especially highlighting that observed variability in the number of interactions can be used to infer parameters and compare functional response models.

Stochastic dynamics of an epidemic with recurrent spillovers from an endemic reservoir.

Most emerging human infectious diseases have an animal origin. While zoonotic diseases originate from a reservoir, most theoretical studies have principally focused on single-host processes, either exclusively humans or exclusively animals, without considering the importance of animal to human transmission (i.e. spillover transmission) for understanding the dynamics of emerging infectious diseases. Here we aim to investigate the importance of spillover transmission for explaining the number and the size of outbreaks. We propose a simple continuous time stochastic Susceptible-Infected-Recovered model with a recurrent infection of an incidental host from a reservoir (e.g. humans by a zoonotic species), considering two modes of transmission, (1) animal-to-human and (2) human-to-human. The model assumes that (i) epidemiological processes are faster than other processes such as demographics or pathogen evolution and that (ii) an epidemic occurs until there are no susceptible individuals left. The results show that during an epidemic, even when the pathogens are barely contagious, multiple outbreaks are observed due to spillover transmission. Overall, the findings demonstrate that the only consideration of direct transmission between individuals is not sufficient to explain the dynamics of zoonotic pathogens in an incidental host.

Polygamy or subdioecy? The impact of diallelic self-incompatibility on the sexual system in Fraxinus excelsior (Oleaceae).

How flowering plants have recurrently evolved from hermaphroditism to separate sexes (dioecy) is a central question in evolutionary biology. Here, we investigate whether diallelic self-incompatibility (DSI) is associated with sexual specialization in the polygamous common ash (Fraxinus excelsior), which would ultimately facilitate the evolution towards dioecy. Using interspecific crosses, we provide evidence of strong relationships between the DSI system and sexual phenotype. The reproductive system in F. excelsior that was previously viewed as polygamy (co-occurrence of unisexuals and hermaphrodites with varying degrees of allocation to the male and female functions) and thus appears to actually behave as a subdioecious system. Hermaphrodites and females belong to one SI group and functionally reproduce as females, whereas males and male-biased hermaphrodites belong to the other SI group and are functionally males. Our results offer an alternative mechanism for the evolution of sexual specialization in flowering plants.

Elucidation of the genetic architecture of self-incompatibility in olive: Evolutionary consequences and perspectives for orchard management.

The olive (Olea europaea L.) is a typical important perennial crop species for which the genetic determination and even functionality of self-incompatibility (SI) are still largely unresolved. It is still not known whether SI is under gametophytic or sporophytic genetic control, yet fruit production in orchards depends critically on successful ovule fertilization. We studied the genetic determination of SI in olive in light of recent discoveries in other genera of the Oleaceae family. Using intra- and interspecific stigma tests on 89 genotypes representative of species-wide olive diversity and the compatibility/incompatibility reactions of progeny plants from controlled crosses, we confirmed that O. europaea shares the same homomorphic diallelic self-incompatibility (DSI) system as the one recently identified in Phillyrea angustifolia and Fraxinus ornus. SI is sporophytic in olive. The incompatibility response differs between the two SI groups in terms of how far pollen tubes grow before growth is arrested within stigma tissues. As a consequence of this DSI system, the chance of cross-incompatibility between pairs of varieties in an orchard is high (50%) and fruit production may be limited by the availability of compatible pollen. The discovery of the DSI system in O. europaea will undoubtedly offer opportunities to optimize fruit production.

Stochasticity in cultural evolution: a revolution yet to happen.

Over the last 40 years or so, there has been an explosion of cultural evolution research in anthropology and archaeology. In each discipline, cultural evolutionists investigate how interactions between individuals translate into group level patterns, with the aim of explaining the diachronic dynamics and diversity of cultural traits. However, while much attention has been given to deterministic processes (e.g. cultural transmission biases), we contend that current evolutionary accounts of cultural change are limited because they do not adopt a systematic stochastic approach (i.e. accounting for the role of chance). First, we show that, in contrast with the intense debates in ecology and population genetics, the importance of stochasticity in evolutionary processes has generated little discussion in the sciences of cultural evolution to date. Second, we speculate on the reasons, both ideological and methodological, why that should be so. Third, we highlight the inadequacy of genetically-inspired stochastic models in the context of cultural evolution modelling, and ask which fundamental stochastic processes might be more relevant to take up. We conclude that the field of cultural evolution would benefit from a stochastic revolution. For that to occur, stochastic models ought to be developed specifically for cultural data and not through a copy-pasting of neutral models from population genetics or ecology.

The double edged sword: The demographic consequences of the evolution of self-fertilization.

Phylogenies indicate that the transition from outcrossing to selfing is frequent, with selfing populations being more prone to extinction. The rates of transition to selfing and extinction, acting on different timescales, could explain the observed distributions of extant selfing species among taxa. However, phylogenetic and theoretical studies consider these mechanisms independently, that is transitions do not cause extinction. Here, we theoretically explore the demographic consequences of the evolution of self-fertilization. Deleterious mutations and mutations modifying the selfing rate are recurrently introduced and the number of offspring depends on individual fitness, allowing for a demographic feedback. We show that mutational meltdowns can be triggered in populations evolving near strict selfing. Populations having survived a demographic crash are more stable than ancestral outcrossing populations once deleterious mutations are purged. The relatively rapid time-scales at which extinctions occur indicate that during evolutionary transitions the accumulation of deleterious mutations may not be the cause of extinctions observed on longer time scales, but could lead to the underestimation of transition rates from outcrossing to selfing.

Correction: Beyond Rational Decision-Making: Modelling the Influence of Cognitive Biases on the Dynamics of Vaccination Coverage.

[This corrects the article DOI: 10.1371/journal.pone.0142990.].