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Lesaffre, T.

Publications and source records attributed to Lesaffre, T..

7 recordsLinked to original sources

The evolutionary interplay between self-fertilisation and sex allocation in flowering plants

Flowering plants vary in sex allocation (resource division between male and female function) and in selfing rate. These traits should evolve together: selfing changes fitness returns from pollen and ovules, whereas sex allocation changes the pollen available for selfing and export. Yet most models allow only one trait to evolve, leaving their evolutionary feedback unresolved. Here we model the joint evolution of sex allocation, pollen export and maternal control of competition between self- and cross-pollen. We show that selfing and sex allocation strongly influence one another, as selection favours associations between sex allocation and mating-system traits. When maternal control is fixed to recover classical mass-action, evolution can lead to the stable coexistence of selfing hermaphrodites and males specialised in pollen export. This androdioecy persists because hermaphrodites cannot prevent fertilisation by males. When maternal control of pollen competition also evolves, we find that where a mixed-mating equilibrium exists, selection again favours the emergence of androdioecy. As hermaphrodites evolve to favour their own pollen, however, they progressively exclude pollen from males, driving them extinct. The population may then return to mixed mating and repeat the process, or evolve complete selfing. We discuss these results with reference to known variation in the mating and sexual systems of plants.

evolutionary biology↗

The evolution of condition-dependent self-fertilisation

Self-fertilisation is common in cosexuals, but selfing rates vary among species, among populations and among individuals within populations. Most evolutionary theory seeking to explain this variation assumes genetically determined selfing rates. Here we study the evolution and consequences of condition-dependent selfing, where individuals adjust their selfing rate in response to their deleterious mutation load. We analyse a two-locus population-genetic model in which one locus determines condition and the other is a modifier locus that determines condition-dependent selfing rates, and then extend the analysis to a polygenic background in which condition is determined by many loci. Our results show that selection favours positive condition dependence: high-condition individuals self-fertilise whereas low-condition individuals outcross. The resulting reaction norm generates stable within-population variation in realised selfing rates at evolutionary equilibrium and reduces the mutation load. We further show that it persists under environmental heterogeneity, and that pollen discounting favours a gradual increase in selfing with condition, leading to a continuum of selfing phenotypes. Altogether, our results indicate that condition-dependent selfing can generate substantial within-population variation in selfing rates. It may therefore contribute to mating-system diversity, and in particular to the maintenance of mixed mating.

evolutionary biology↗

The joint evolution of separate sexes and sexual dimorphism

Dioecious plants are frequently sexually dimorphic. Such dimorphism, which reflects responses to selection acting in opposite directions for male and female components of fitness, is commonly thought to emerge after separate sexes evolved from hermaphroditism. But associations between allocation to male and female function and traits under sexual conflict may well also develop in hermaphroditic ancestors. Here, we show that variation in sex allocation and a trait under sexual conflict inevitably generates an advantage to sexual specialisation, fueling the transition to dioecy. In the absence of constraints, this leads to the joint evolution of separate sexes and sexual dimorphism through the build-up of an association between sex allocation and the conflict trait, such that eventually the population consists of unisexuals expressing their sex-specific optima. We then investigate how such association might materialise genetically, either via recombination suppression or via sex-dependent expression, and show that the genetic architecture of sex allocation and the conflict trait readily evolves to produce the association favoured by selection. Finally and in agreement with previous theory, we demonstrate that limited dispersal and self-fertilisation, which are pervasive ecological characteristics of flowering plants, can offset the advantage of sexual specialisation generated by sexual conflict and thus maintain hermaphroditism. Taken together, our results indicate that advantages to sexual specialisation are inevitable when there is conflict between sexual functions in hermaphrodites, but these advantages can be counterbalanced by ecological benefits of hermaphroditism.

evolutionary biology↗

On the origins of Y and W chromosomes as an outcome of sex allocation evolution

In plants with separate sexes, the development of an individual as male or female is controlled by a dominant allele at a sex-determining locus - the fundamental basis of XY and ZW systems. The many independent transitions from hermaphroditism to dioecy that have taken place in flowering plants must therefore often have entailed the emergence of such a locus. One proposition is that this evolution occurs in two steps, with the initial invasion of a male-sterility mutation at one locus followed by mutations causing female sterility at a second closely linked locus. Here, we show how dioecy with heterogametic sex determination can also emerge in a gradual adaptive process, involving the co-evolution of resource allocation to different sexual functions jointly with its genetic architecture. Our model reveals that whether an XY or a ZW system evolves depends on the mating system of the ancestral hermaphrodites as well as the trade-off they face between allocation to male and female functions. In particular, the evolution of dioecy in response to selection to avoid selfing and inbreeding depression favours the emergence of XY systems, which characterise the vast majority of dioecious flowering plants. Selection favouring female specialisation also favours XY over ZW sex determination. Taken together, our results throw new light on the possible origins of dioecy from hermaphroditism by revealing a hitherto unrecognised link between the ecology and economics of sex allocation and the genetic basis of sex determination.

evolutionary biology↗

Population-level consequences of inheritable somatic mutations and the evolution of mutation rates in plants

Inbreeding depression, that is the decrease in fitness of inbred relative to outbred individuals, was shown to increase strongly as life expectancy increases in plants. Because plants are thought to not have a separated germline, it was proposed that this pattern could be generated by somatic mutations accumulating during growth, since larger and more long-lived species have more opportunities for mutations to accumulate. A key determinant of the role of somatic mutations is the rate at which they occur, which likely differs between species because mutation rates may evolve differently in species with constrasting life-histories. In this paper, we study the evolution of the mutation rates in plants, and consider the population-level consequences of inheritable somatic mutations given this evolution. We show that despite substantially lower per year mutation rates, more long-lived species still tend to accumulate larger amounts of deleterious mutations because of higher per generation, leading to higher levels of inbreeding depression in these species. However, the magnitude of this increase depends strongly on how mutagenic meiosis is relative to growth.

evolutionary biology↗

On deleterious mutations in perennials: inbreeding depression, mutation load and life-history evolution

In 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 in these species, 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 behaviour of mutations affecting growth or survival, and explore their consequences in terms of inbreeding depression and mutation load. Although our results only agree with empirical data within a narrow range of conditions, we argue that they may point us towards the type of traits susceptible to underlie 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 coevolution between growth and survival strategies. Description of the manuscriptThe main text of the manuscript, excluding captions and headers, is 5712 words long. There are 4 figures in the main text, numbered from 1 to 4. In the present file, pages 1 to 33 correspond to the main text (including title page, abstract and litterature cited), while the remaining pages (33 to 72) correspond to appendices. There are 5 sections in Appendices, which are all available at the end of the manuscript file. There are 12 figures in Appendices, numbered from S1 to S12.

evolutionary biology↗

The joint evolution of lifespan and self-fertilisation

In Angiosperms, there exists a strong association between mating system and lifespan. Most self-fertilising 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-fertilisation and lifespan, including both juvenile and adult inbreeding depression. We show that self-fertilisation 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.

evolutionary biology↗