Sylvain Billiard

Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types.

The advantage of sex has been among the most debated issues in biology. Surprisingly, the question of why sexual reproduction generally requires the combination of distinct gamete classes, such as small and large gametes, or gametes with different mating types, has been much less investigated. Why do systems with alternative gamete classes (i.e. systems with either anisogamy or mating types or both) appear even though they restrict the probability of finding a compatible mating partner? Why does the number of gamete classes vary from zero to thousands, with most often only two classes? We review here the hypotheses proposed to explain the origin, maintenance, number, and loss of gamete classes. We argue that fungi represent highly suitable models to help resolve issues related to the evolution of distinct gamete classes, because the number of mating types vary from zero to thousands across taxa, anisogamy is present or not, and because there are frequent transitions between these conditions. We review the nature and number of gamete classes in fungi, and we attempt to draw inferences from these data on the evolutionary forces responsible for their appearance, loss or maintenance, and number.

Sex, outcrossing and mating types: unsolved questions in fungi and beyond

Variability in the way organisms reproduce raises numerous, and still unsolved, questions in evolutionary biology. In this study, we emphasize that fungi deserve a much greater emphasis in efforts to address these questions because of their multiple advantages as model eukaryotes. A tremendous diversity of reproductive modes and mating systems can be found in fungi, with many evolutionary transitions among closely related species. In addition, fungi show some peculiarities in their mating systems that have received little attention so far, despite the potential for providing insights into important evolutionary questions. In particular, selfing can occur at the haploid stage in addition to the diploid stage in many fungi, which is generally not possible in animals and plants but has a dramatic influence upon the structure of genetic systems. Fungi also present several advantages that make them tractable models for studies in experimental evolution. Here, we briefly review the unsolved questions and extant hypotheses about the evolution and maintenance of asexual vs. sexual reproduction and of selfing vs. outcrossing, focusing on fungal life cycles. We then propose how fungi can be used to address these long‐standing questions and advance our understanding of sexual reproduction and mating systems across all eukaryotes.

Variation in the frequency of left-handedness in traditional societies

charlotte faurie , wulf schiefenhövel , sylvie le bomin, sylvain bill iard, and michel raymond Université Montpellier II, CC 065, Place Eugène Bataillon, 34095 Montpellier cedex 5, France (faurie@isem.univ-montp2.fr) (Faurie)/Institut des Sciences de l’Evolution (CNRS UMR 5554), Montpellier, France (Faurie, Billiard, Raymond)/MaxPlanck-Gesellschaft, Human Ethology Group, Andechs, Germany (Schiefenhövel)/Langues, Musiques et Sociétés (CNRS UMR 8099), Villejuif, France (Le Bomin). 10 vi 04

EVOLUTION OF MIGRATION UNDER KIN SELECTION AND LOCAL ADAPTATION

Abstract We present here a stochastic two‐locus, two‐habitat model for the evolution of migration with local adaptation and kin selection. One locus determines the migration rate while the other causes local adaptation. We show that the opposing forces of kin competition and local adaptation can lead to the existence of one or two convergence stable migration rates, notably depending on the recombination rate between the two loci. We show that linkage between migration and local adaptation loci has two antagonist effects: when linkage is tight, cost of local adaptation increases, leading to smaller equilibrium migration rates. However, when linkage is tighter, the population structure at the migration locus tends to be very high because of the indirect selection, and thus equilibrium migration rates increases. This result, qualitatively different from results obtained with other models of migration evolution, indicates that ignoring drift or the detail of the genetic architecture may lead to incorrect conclusions.

A general model to explore complex dominance patterns in plant sporophytic self-incompatibility systems

We developed a general model of sporophytic self-incompatibility under negative frequency-dependent selection allowing complex patterns of dominance among alleles. We used this model deterministically to investigate the effects on equilibrium allelic frequencies of the number of dominance classes, the number of alleles per dominance class, the asymmetry in dominance expression between pollen and pistil, and whether selection acts on male fitness only or both on male and on female fitnesses. We show that the so-called “recessive effect” occurs under a wide variety of situations. We found emerging properties of finite population models with several alleles per dominance class such as that higher numbers of alleles are maintained in more dominant classes and that the number of dominance classes can evolve. We also investigated the occurrence of homozygous genotypes and found that substantial proportions of those can occur for the most recessive alleles. We used the model for two species with complex dominance patterns to test whether allelic frequencies in natural populations are in agreement with the distribution predicted by our model. We suggest that the model can be used to test explicitly for additional, allele-specific, selective forces.

Hitchhiking Both Ways: Effect of Two Interfering Selective Sweeps on Linked Neutral Variation

The neutral polymorphism pattern in the vicinity of a selective sweep can be altered by both stochastic and deterministic factors. Here, we focus on the impact of another selective sweep in the region of influence of a first one. We study the signature left on neutral polymorphism by positive selection at two closely linked loci, when both beneficial mutations reach fixation. We show that, depending on the timing of selective sweeps and on their selection coefficients, the two hitchhiking effects can interfere with each other, leading to less reduction in heterozygosity than a single selective sweep of the same magnitude and more importantly to an excess of intermediate-frequency variants relative to neutrality under some parameter values. This pattern can be sustained and potentially alter the detection of positive selection, including by provoking spurious detection of balancing selection. In situations where positive selection is suspected a priori at several closely linked loci, the polymorphism pattern in the region may also be informative about their selective histories.

Does Frequency-Dependent Selection with Complex Dominance Interactions Accurately Predict Allelic Frequencies at the Self-Incompatibility Locus in Arabidopsis halleri?

Abstract Frequency-dependent selection is a major force determining the evolutionary dynamics of alleles at the self-incompatibility locus (S-locus) in flowering plants. We introduce a general method using numerical simulations to test several alternative models of frequency-dependent selection on S-locus data from sporophytic systems, taking into account both genetic drift and observed patterns of dominance interactions among S-locus haplotypes (S-haplotypes). Using a molecular typing method, we estimated S-haplotype frequencies in a sample of 322 adult plants and of 245 offspring obtained from seeds sampled on 22 maternal plants, collected in a single population of Arabidopsis halleri (Brassicaceae). We found eight different S-haplotypes and characterized their dominance interactions by controlled pollinations. We then compared the likelihood of different models of frequency-dependent selection: we found that the observed haplotype frequencies and observed frequency changes in one generation best fitted a model with (1) the observed dominance interactions and (2) no pollen limitation. Overall, our population genetic models of frequency-dependent selection, including patterns of dominance interactions among S-haplotypes and genetic drift, can reliably predict polymorphism at the S-locus. We discuss how these approaches allow detecting additional processes influencing the evolutionary dynamics of the S-locus, such as purifying selection on linked loci.

Evolution of uni- and bifactorial sexual compatibility systems in fungi

Mating systems, that is, whether organisms give rise to progeny by selfing, inbreeding or outcrossing, strongly affect important ecological and evolutionary processes. Large variations in mating systems exist in fungi, allowing the study of their origin and consequences. In fungi, sexual incompatibility is determined by molecular recognition mechanisms, controlled by a single mating-type locus in most unifactorial fungi. In Basidiomycete fungi, however, which include rusts, smuts and mushrooms, a system has evolved in which incompatibility is controlled by two unlinked loci. This bifactorial system probably evolved from a unifactorial system. Multiple independent transitions back to a unifactorial system occurred. It is still unclear what force drove evolution and maintenance of these contrasting inheritance patterns that determine mating compatibility. Here, we give an overview of the evolutionary factors that might have driven the evolution of bifactoriality from a unifactorial system and the transitions back to unifactoriality. Bifactoriality most likely evolved for selfing avoidance. Subsequently, multiallelism at mating-type loci evolved through negative frequency-dependent selection by increasing the chance to find a compatible mate. Unifactoriality then evolved back in some species, possibly because either selfing was favoured or for increasing the chance to find a compatible mate in species with few alleles. Owing to the existence of closely related unifactorial and bifactorial species and the increasing knowledge of the genetic systems of the different mechanisms, Basidiomycetes provide an excellent model for studying the different forces that shape breeding systems.

An experimental study of the S-Allee effect in the self-incompatible plant Biscutella neustriaca.

Homomorphic self-incompatibility (SI) evolved in many plant families to enforce selfing avoidance, and is controlled by a single multiallelic locus (the S-locus). In a fragmented landscape, strong variation in population size and in local density is expected to cause strong variation in allelic diversity at the S-locus, which could generate an Allee effect on female reproductive success by constraining compatible pollen availability. In this experimental study, we aimed at detecting this SI-specific Allee effect (or S-Allee effect) in the endangered species Biscutella neustriaca. We demonstrated the occurrence of a SI mating system in the species and determined compatibility relationships among genotypes through a large set of controlled pollinations. For the experiment, we chose three different pollen receptor genotypes, each compatible with respectively 100, 75 and 25% of four other genotypes, which constituted the pollen sources. We placed different ramets of each receptor at different distances from the pollen sources to control for pollen limitation due to low local density, and we measured the seed set on each receptor plant three times consecutively. Analyses performed with generalized linear mixed models showed that both the distance to the pollen sources and the mate availability due to SI had a significant effect on seed set, with a strong reduction observed when mate availability was limited to 25%. Our results suggest that pollen limitation due to a restriction in compatible mate availability could occur in small or scattered populations exhibiting low allelic diversity at the S-locus.

Dominance hierarchy arising from the evolution of a complex small RNA regulatory network

The prevention of fertilization through self-pollination (or pollination by a close relative) in the Brassicaceae plant family is determined by the genotype of the plant at the self-incompatibility locus (S locus). The many alleles at this locus exhibit a dominance hierarchy that determines which of the two allelic specificities of a heterozygous genotype is expressed at the phenotypic level. Here, we uncover the evolution of how at least 17 small RNA (sRNA)–producing loci and their multiple target sites collectively control the dominance hierarchy among alleles within the gene controlling the pollen S-locus phenotype in a self-incompatible Arabidopsis species. Selection has created a dynamic repertoire of sRNA-target interactions by jointly acting on sRNA genes and their target sites, which has resulted in a complex system of regulation among alleles. Hierarchical interactions among alleles in a mustard plant explain how self-incompatibility evolved and is maintained. Dominance cascades in self-incompatibility Plants often cannot use their own pollen to set seed. This is known as self-incompatibility. Although some of the underlying genetics and mechanisms of self-incompatibility are understood, the evolution and maintenance of the system have remained mysterious. Durand et al. identified a collection of small RNAs and their respective matching targets within a self-incompatibility locus in Arabidopsis halleri. A subset of these alleles functioned in a dominant manner, which helps to explain how self-incompatibility is maintained. Science, this issue p. 1200