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.

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.

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.

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.

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.

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.

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.

Evidence for the long-term maintenance of a rare self-incompatibility system in Oleaceae.

A rare homomorphic diallelic self-incompatibility (DSI) system discovered in Phillyrea angustifolia (family Oleaceae, subtribe Oleinae) can promote the transition from hermaphroditism to androdioecy. If widespread and stable in Oleaceae, DSI may explain the exceptionally high rate of androdioecious species reported in this plant family. Here, we set out to determine whether DSI occurs in another Oleaceae lineage. We tested for DSI in subtribe Fraxininae, a lineage that diverged from subtribe Oleinae c. 40 million yr ago. We explored the compatibility relationships in Fraxinus ornus using 81 hermaphrodites and 25 males from one natural stand and two naturalized populations using intra- and interspecific stigma tests performed on F. ornus and P. angustifolia testers. We uncovered a DSI system with hermaphrodites belonging to one of two self-incompatibility (SI) groups and males compatible with both groups, making for a truly androdioecious reproductive system. The two human-founded populations contained only one of the two SI groups. Our results provide evidence for the evolutionary persistence of DSI. We discuss how its stability over time may have affected transitions to other sexual systems, such as dioecy.

The effect of competition and horizontal trait inheritance on invasion, fixation, and polymorphism.

Horizontal transfer (HT) of heritable information or 'traits' (carried by genetic elements, plasmids, endosymbionts, or culture) is widespread among living organisms. Yet current ecological and evolutionary theory addressing HT is scant. We present a modeling framework for the dynamics of two populations that compete for resources and horizontally exchange (transfer) an otherwise vertically inherited trait. Competition influences individual demographics, thereby affecting population size, which feeds back on the dynamics of transfer. This feedback is captured in a stochastic individual-based model, from which we derive a general model for the contact rate, with frequency-dependent (FD) and density-dependent (DD) rates as special cases. Taking a large-population limit on the stochastic individual-level model yields a deterministic Lotka-Volterra competition system with additional terms accounting for HT. The stability analysis of this system shows that HT can revert the direction of selection: HT can drive invasion of a deleterious trait, or prevent invasion of an advantageous trait. Due to HT, invasion does not necessarily imply fixation. Two trait values may coexist in a stable polymorphism even if their invasion fitnesses have opposite signs, or both are negative. Addressing the question of how the stochasticity of individual processes influences population fluctuations, we identify conditions on competition and mode of transfer (FD versus DD) under which the stochasticity of transfer events overwhelms demographic stochasticity. Assuming that one trait is initially rare, we derive invasion and fixation probabilities and time. In the case of costly plasmids, which are transfered unilaterally, invasion is always possible if the transfer rate is large enough; under DD and for intermediate values of the transfer rate, maintenance of the plasmid in a polymorphic population is possible. In conclusion, HT interacts with ecology (competition) in non-trivial ways. Our model provides a basis to model the influence of HT on evolutionary adaptation.

Functional analyses of cellulose synthase genes in flax (Linum usitatissimum) by virus-induced gene silencing.

Flax (Linum usitatissimum) bast fibres are located in the stem cortex where they play an important role in mechanical support. They contain high amounts of cellulose and so are used for linen textiles and in the composite industry. In this study, we screened the annotated flax genome and identified 14 distinct cellulose synthase (CESA) genes using orthologous sequences previously identified. Transcriptomics of 'primary cell wall' and 'secondary cell wall' flax CESA genes showed that some were preferentially expressed in different organs and stem tissues providing clues as to their biological role(s) in planta. The development for the first time in flax of a virus-induced gene silencing (VIGS) approach was used to functionally evaluate the biological role of different CESA genes in stem tissues. Quantification of transcript accumulation showed that in many cases, silencing not only affected targeted CESA clades, but also had an impact on other CESA genes. Whatever the targeted clade, inactivation by VIGS affected plant growth. In contrast, only clade 1- and clade 6-targeted plants showed modifications in outer-stem tissue organization and secondary cell wall formation. In these plants, bast fibre number and structure were severely impacted, suggesting that the targeted genes may play an important role in the establishment of the fibre cell wall. Our results provide new fundamental information about cellulose biosynthesis in flax that should facilitate future plant improvement/engineering.

The joint evolution and maintenance of self-incompatibility with gynodioecy or androdioecy.

Mating systems show two kinds of frequent transitions: from hermaphroditism to dioecy, gynodioecy or androdioecy, or from self-incompatibility (SI) to self-compatibility (SC). While models have mostly investigated these two kinds of transitions as independent, empirical observations suggest that, to some extent, they can evolve jointly. Here, we study the joint evolution and maintenance of SI and androdioecy or SI and gynodioecy by the means of phenotypic models. Our models focus on three parameters: the unisexuals׳ advantage relative to that of the hermaphrodites due to resource reallocation, inbreeding depression and the selfing rate. We assume no pollen limitation or discounting. We show that SI helps the maintenance of androdioecy, but favors the loss of gynodioecy, and also that androdioecy facilitates the maintenance of SI, whereas gynodioecy does not affect it. We finally investigate how gynodioecy and androdioecy may affect the diversification of SI groups, especially considering an evolutionary pathway through SC intermediates. We show that while androdioecy prevents the increase of the number of SI groups, under certain conditions of inbreeding depression and selfing rates, gynodioecy allows it.

Stochastic dynamics of adaptive trait and neutral marker driven by eco-evolutionary feedbacks.

How the neutral diversity is affected by selection and adaptation is investigated in an eco-evolutionary framework. In our model, we study a finite population in continuous time, where each individual is characterized by a trait under selection and a completely linked neutral marker. Population dynamics are driven by births and deaths, mutations at birth, and competition between individuals. Trait values influence ecological processes (demographic events, competition), and competition generates selection on trait variation, thus closing the eco-evolutionary feedback loop. The demographic effects of the trait are also expected to influence the generation and maintenance of neutral variation. We consider a large population limit with rare mutation, under the assumption that the neutral marker mutates faster than the trait under selection. We prove the convergence of the stochastic individual-based process to a new measure-valued diffusive process with jumps that we call Substitution Fleming-Viot Process (SFVP). When restricted to the trait space this process is the Trait Substitution Sequence first introduced by Metz et al. (1996). During the invasion of a favorable mutation, a genetical bottleneck occurs and the marker associated with this favorable mutant is hitchhiked. By rigorously analysing the hitchhiking effect and how the neutral diversity is restored afterwards, we obtain the condition for a time-scale separation; under this condition, we show that the marker distribution is approximated by a Fleming-Viot distribution between two trait substitutions. We discuss the implications of the SFVP for our understanding of the dynamics of neutral variation under eco-evolutionary feedbacks and illustrate the main phenomena with simulations. Our results highlight the joint importance of mutations, ecological parameters, and trait values in the restoration of neutral diversity after a selective sweep.

Evidence for Fisher's dominance theory: how many 'special cases'?

Dominance, its genetic basis and evolution has been at the heart of one of the most intense controversies in the history of genetics. For more than eighty years the existence of dominance modifiers, genetic elements controlling dominance-recessivity interactions, has been suggested as a theoretical possibility, but the modifier elements themselves have remained elusive. A recent study of the self-incompatibility locus in flowering plants provided the first empirical evidence for such genetic elements: small non-coding RNAs that control dominance-recessivity by mediating methylation of the promoter of the recessive allele. Theory has shown that several biological situations are favorable for the evolution of dominance modifiers. We argue that the elucidation of this mechanism of dominance opens up new research avenues that could lead to uncovering dominance modifiers in other genetic systems, such as genes controlling Batesian and Müllerian mimicry or host-parasite interactions, thereby shedding light on the generality of the proposed mechanism.

Impact of ecological doses of the most widespread phthalate on a terrestrial species, the ant Lasius niger.

Phthalates are synthetic contaminants released into the environment notably by plastic waste. Semi-volatile, they adsorb to atmospheric particles and get distributed in all ecosystems. Effects of this major anthropogenic pollution in economical species in aquatic habitats have attracted large interest. On the contrary, very few studies have focused on wild terrestrial species. Yet, these lipophilic molecules are easily trapped by insect cuticle; ants and other insects have been shown to permanently bear among their cuticular components a non-negligible proportion of phthalates, meaning that they suffer from chronic exposure to these pollutants. Oral route could also be an additional way of contamination, as phthalates tend to stick to any organic particle. We show here via a food choice experiment that Lasius niger workers can detect, and avoid feeding on, food contaminated with DEHP (DiEthyl Hexyl Phthalate), the most widespread phthalate found in nature. This suggests that the main source of contamination for ants is atmosphere and that doses measured on the cuticle correspond to the chronic exposure levels for these animals. Such an ecologically relevant dose of DEHP was used to contaminate ants in lab and to investigate their physiological impact. Over a chronic exposure (1 dose per week for 5 weeks), the egg-laying rate of queens was significantly reduced lending credence to endocrine disruptive properties of such a pollutant, as also described for aquatic invertebrates. On the contrary, short term exposure (24h) to a single dose of DEHP does not induce oxidative stress in ant workers as expected, but leads to activation of the immune system. Because of their very large distribution, their presence in virtually all terrestrial ecosystems and their representation at all trophic levels, ants could be useful indicators of contamination by phthalates, especially via monitoring the level of activation of their immune state.

Trait transitions in explicit ecological and genomic contexts: plant mating systems as case studies.

Plants are astonishingly diverse in how they reproduce sexually, and the study of plant mating systems provides some of the most compelling cases of parallel and independent evolutionary transitions. In this chapter, we review how the massive amount of genomic data being produced is allowing long-standing predictions from ecological and evolutionary theory to be put to test. After a review of theoretical predictions about the importance of considering the genomic architecture of the mating system, we focus on a set of recent discoveries on how the mating system is controlled in a variety of model and non-model species. In parallel, genomic approaches have revealed the complex interaction between the evolution of genes controlling mating systems and genome evolution, both genome-wide and in the mating system control region. In several cases, major transitions in the mating system can be clearly associated with important ecological changes, hence illuminating an important interplay between ecological and genomic approaches. We also list a number of major unsolved questions that remain for the field, and highlight foreseeable conceptual developments that are likely to play a major role in our understanding of how plant mating systems evolve in Nature.

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.

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.

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.