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.

Causes and consequences of linkage disequilibrium among transposable elements within eukaryotic genomes.

Sex and recombination can affect the dynamics of transposable elements (TEs) in various ways: while sex is expected to help TEs to spread within populations, the deleterious effect of ectopic recombination among transposons represents a possible source of purifying selection limiting their number. Furthermore, recombination may also increase the efficiency of selection against TEs by reducing selective interference among loci. In order to better understand the effects of recombination and reproductive systems on TE dynamics, this article provides analytical expressions for the linkage disequilibrium among TEs in a classical model in which TE number is stabilized by synergistic purifying selection. The results show that positive linkage disequilibrium is predicted in infinite populations despite negative epistasis, due to the effect of the transposition process. Positive linkage disequilibrium may substantially inflate the variance in the number of elements per genome in the case of partially selfing or partially clonal populations. Finite population size tends to generate negative linkage disequilibrium (Hill-Robertson effect), the relative importance of this effect increasing with the degree of linkage among loci. The model is then extended in order to explore how TEs may affect selection for recombination. While positive linkage disequilibrium generated by transposition generally disfavors recombination, the Hill-Robertson effect may represent a non-negligible source of indirect selection for recombination when TEs are abundant. However, the direct fitness cost imposed by ectopic recombination among elements generally drives the population towards low-recombination regimes, at which TEs cannot be maintained at a stable equilibrium.

The evolution of recombination in self-fertilizing organisms.

Cytological data from flowering plants suggest that the evolution of recombination rates is affected by the mating system of organisms, as higher chiasma frequencies are often observed in self-fertilizing species compared with their outcrossing relatives. Understanding the evolutionary cause of this effect is of particular interest, as it may shed light on the selective forces favoring recombination in natural populations. While previous models showed that inbreeding may have important effects on selection for recombination, existing analytical treatments are restricted to the case of loosely linked loci and weak selfing rates, and ignore the stochastic effect of genetic interference (Hill-Robertson effect), known to be an important component of selection for recombination in randomly mating populations. In this article, we derive general expressions quantifying the stochastic and deterministic components of selection acting on a mutation affecting the genetic map length of a whole chromosome along which deleterious mutations occur, valid for arbitrary selfing rates. The results show that selfing generally increases selection for recombination caused by interference among mutations as long as selection against deleterious alleles is sufficiently weak. While interference is often the main driver of selection for recombination under tight linkage or high selfing rates, deterministic effects can play a stronger role under intermediate selfing rates and high recombination, selecting against recombination in the absence of epistasis, but favoring recombination when epistasis is negative. Individual-based simulation results indicate that our analytical model often provides accurate predictions for the strength of selection on recombination under partial selfing.

Y recombination arrest and degeneration in the absence of sexual dimorphism.

Current theory proposes that degenerated sex chromosomes-such as the mammalian Y-evolve through three steps: (i) recombination arrest, linking male-beneficial alleles to the Y chromosome; (ii) Y degeneration, resulting from the inefficacy of selection in the absence of recombination; and (iii) dosage compensation, correcting the resulting low expression of X-linked genes in males. We investigate a model of sex chromosome evolution that incorporates the coevolution of cis and trans regulators of gene expression. We show that the early emergence of dosage compensation favors the maintenance of Y-linked inversions by creating sex-antagonistic regulatory effects. This is followed by degeneration of these nonrecombining inversions caused by regulatory divergence between the X and Y chromosomes. In contrast to current theory, the whole process occurs without any selective pressure related to sexual dimorphism.

The spatio-temporal dynamics of interacting genetic incompatibilities. Part I: the case of stacked underdominant clines.

We explore the interaction between two genetic incompatibilities (underdominant loci in diploid organisms) in a population occupying a one-dimensional space. We derive a system of partial differential equations describing the dynamics of allele frequencies and linkage disequilibrium between the two loci, and use a quasi-linkage equilibrium approximation in order to reduce the number of variables. We investigate the solutions of this system and demonstrate the existence of a solution in which the two clines in allele frequency remain stacked together. In the case of asymmetric incompatibilities (i.e. when one homozygote is favored over the other at each locus), these stacked clines propagate in the form of a traveling wave. We obtain an approximation for the speed of this wave which, in particular, is decreased by recombination between the two loci but is always larger than the speed of "one cline alone".

Evolution of life cycles and reproductive traits: Insights from the brown algae.

A vast diversity of types of life cycles exists in nature, and several theories have been advanced to explain how this diversity has evolved and how each type of life cycle is retained over evolutionary time. Here, we exploited the diversity of life cycles and reproductive traits of the brown algae (Phaeophyceae) to test several hypotheses on the evolution of life cycles. We investigated the evolutionary dynamics of four life-history traits: life cycle, sexual system, level of gamete dimorphism and gamete parthenogenetic capacity. We assigned states to up to 77 representative species of the taxonomic diversity of the brown algal group, in a multi-gene phylogeny. We used maximum likelihood and Bayesian analyses of correlated evolution, while taking the phylogeny into account, to test for correlations between traits and to investigate the chronological sequence of trait acquisition. Our analyses are consistent with the prediction that diploid growth evolves when sexual reproduction is preferred over asexual reproduction, possibly because it allows the complementation of deleterious mutations. We also found that haploid sex determination is ancestral in relation to diploid sex determination. However, our results could not address whether increased zygotic and diploid growth are associated with increased sexual dimorphism. Our analyses suggest that in the brown algae, isogamous species evolved from anisogamous ancestors, contrary to the commonly reported pattern where evolution proceeds from isogamy to anisogamy.

A simple expression for the strength of selection on recombination generated by interference among mutations.

One of the most widely cited hypotheses to explain the evolutionary maintenance of genetic recombination states that the reshuffling of genotypes at meiosis increases the efficiency of natural selection by reducing interference among selected loci. However, and despite several decades of theoretical work, a quantitative estimation of the possible selective advantage of a mutant allele increasing chromosomal map length (the average number of cross-overs at meiosis) remains difficult. This article derives a simple expression for the strength of selection acting on a modifier gene affecting the genetic map length of a whole chromosome or genome undergoing recurrent mutation. In particular, it shows that indirect selection for recombination caused by interference among mutations is proportional to [Formula: see text], where [Formula: see text] is the effective population size, U is the deleterious mutation rate per chromosome, and R is the chromosome map length. Indirect selection is relatively insensitive to the fitness effects of deleterious alleles, epistasis, or the genetic architecture of recombination rate variation and may compensate for substantial costs associated with recombination when linkage is tight. However, its effect generally stays weak in large, highly recombining populations.

The evolution of sex along an environmental gradient.

Although temporally changing environments generally favor sex and recombination, the effects of spatial environmental heterogeneity have been less explored. In this article, we use a classical model of adaptation along with an environmental gradient to study the selective forces acting on reproductive mode evolution in the central and marginal parts of the distribution range of a species. The model considers a polygenic trait under stabilizing selection (the optimal trait value changing across space) and includes a demographic component imposing range limits. The results show that in the central part of the range (where populations are well adapted), recombination tends to increase the mean fitness of offspring in regimes where drift is sufficiently strong (generating a benefit for sex), while it has the opposite effect when the effect of drift stays negligible. However, these effects remain weak and are easily overwhelmed by slight intrinsic fitness differences between sexuals and asexuals. In agreement with previous results, asexuality may be favored in marginal populations, as it can preserve adaptation to extreme conditions. However, a substantial advantage of asexuality is possible only in conditions maintaining a strong maladaptation of sexuals at range limits (high effective environmental gradient, weak selection at loci coding for the trait).

The geometry and genetics of hybridization.

When divergent populations form hybrids, hybrid fitness can vary with genome composition, current environmental conditions, and the divergence history of the populations. We develop analytical predictions for hybrid fitness, which incorporate all three factors. The predictions are based on Fisher's geometric model, and apply to a wide range of population genetic parameter regimes and divergence conditions, including allopatry and parapatry, local adaptation, and drift. Results show that hybrid fitness can be decomposed into intrinsic effects of admixture and heterozygosity, and extrinsic effects of the (local) adaptedness of the parental lines. Effect sizes are determined by a handful of geometric distances, which have a simple biological interpretation. These distances also reflect the mode and amount of divergence, such that there is convergence toward a characteristic pattern of intrinsic isolation. We next connect our results to the quantitative genetics of line crosses in variable or patchy environments. This means that the geometrical distances can be estimated from cross data, and provides a simple interpretation of the "composite effects." Finally, we develop extensions to the model, involving selectively induced disequilibria, and variable phenotypic dominance. The geometry of fitness landscapes provides a unifying framework for understanding speciation, and wider patterns of hybrid fitness.

Sex Chromosome Degeneration by Regulatory Evolution.

In many species, the Y (or W) sex chromosome is degenerate. Current theory proposes that this degeneration follows the arrest of recombination and results from the accumulation of deleterious mutations due to selective interference-the inefficacy of natural selection on non-recombining genomic regions. This theory requires very few assumptions, but it does not robustly predict fast erosion of the Y (or W) in large populations or the stepwise degeneration of several small non-recombining strata. We propose a new mechanism for Y/W erosion that works over faster timescales, in large populations, and for small non-recombining regions (down to a single sex-linked gene). The mechanism is based on the instability and divergence of cis-regulatory sequences in non-recombining genome regions, which become selectively haploidized to mask deleterious mutations on coding sequences. This haploidization is asymmetric, because cis-regulators on the X cannot be silenced (otherwise there would be no expression in females). This process causes rapid Y/W degeneration and simultaneous evolution of dosage compensation, provided that autosomal trans-regulatory sequences with sex-limited effects are available to compensate for cis-regulatory divergence. Although this "degeneration by regulatory evolution" does not require selective interference, both processes may act in concert to further accelerate Y degeneration.

Epistasis, inbreeding depression, and the evolution of self-fertilization.

Inbreeding depression resulting from partially recessive deleterious alleles is thought to be the main genetic factor preventing self-fertilizing mutants from spreading in outcrossing hermaphroditic populations. However, deleterious alleles may also generate an advantage to selfers in terms of more efficient purging, while the effects of epistasis among those alleles on inbreeding depression and mating system evolution remain little explored. In this article, we use a general model of selection to disentangle the effects of different forms of epistasis (additive-by-additive, additive-by-dominance, and dominance-by-dominance) on inbreeding depression and on the strength of selection for selfing. Models with fixed epistasis across loci, and models of stabilizing selection acting on quantitative traits (generating distributions of epistasis) are considered as special cases. Besides its effects on inbreeding depression, epistasis may increase the purging advantage associated with selfing (when it is negative on average), while the variance in epistasis favors selfing through the generation of linkage disequilibria that increase mean fitness. Approximations for the strengths of these effects are derived, and compared with individual-based simulation results.

Genetic variability and transgenerational regulation of investment in sex in the monogonont rotifer Brachionus plicatilis.

In cyclical parthenogens such as aphids, cladocerans and rotifers, the coupling between sexual reproduction and the production of resting stages (diapausing eggs) imposes strong constraints on the timing of sex. Whereas induction of sex is generally triggered by environmental cues, the response to such cues may vary across individuals according to genetic and nongenetic factors. In this study, we explored genetic and epigenetic causes of variation for the propensity for sex using a collection of strains from a Spanish population of monogonont rotifers (Brachionus plicatilis) in which variation for the threshold population density at which sex is induced (mixis threshold) had been documented previously. Our results show significant variation for the mixis threshold among 20 clones maintained under controlled conditions for 15 asexual generations. The effect of the number of clonal generations since hatching of the diapausing egg on the mixis ratio (proportion of sexual offspring produced) was tested on 4 clones with contrasted mixis thresholds. The results show a negative correlation between the mixis threshold and mixis ratio, as well as a significant effect of the number of clonal generations since fertilization, sex being repressed during the first few generations after hatching of the diapausing egg.

Asexual reproduction reduces transposable element load in experimental yeast populations.

Theory predicts that sexual reproduction can either facilitate or restrain transposable element (TE) accumulation by providing TEs with a means of spreading to all individuals in a population, versus facilitating TE load reduction via purifying selection. By quantifying genomic TE loads over time in experimental sexual and asexual Saccharomyces cerevisiae populations, we provide direct evidence that TE loads decrease rapidly under asexual reproduction. We show, using simulations, that this reduction may occur via evolution of TE activity, most likely via increased excision rates. Thus, sex is a major driver of genomic TE loads and at the root of the success of TEs.

Stabilizing selection, mutational bias, and the evolution of sex.

Stabilizing selection around a fixed phenotypic optimum is expected to disfavor sexual reproduction, since asexually reproducing organisms can maintain a higher fitness at equilibrium, while sex disrupts combinations of compensatory mutations. This conclusion rests on the assumption that mutational effects on phenotypic traits are unbiased, that is, mutation does not tend to push phenotypes in any particular direction. In this article, we consider a model of stabilizing selection acting on an arbitrary number of polygenic traits coded by bialellic loci, and show that mutational bias may greatly reduce the mean fitness of asexual populations compared with sexual ones in regimes where mutations have weak to moderate fitness effects. Indeed, mutation and drift tend to push the population mean phenotype away from the optimum, this effect being enhanced by the low effective population size of asexual populations. In a second part, we present results from individual-based simulations showing that positive rates of sex are favored when mutational bias is present, while the population evolves toward complete asexuality in the absence of bias. We also present analytical (QLE) approximations for the selective forces acting on sex in terms of the effect of sex on the mean and variance in fitness among offspring.

Genetic Diversity in the UV Sex Chromosomes of the Brown Alga Ectocarpus.

Three types of sex chromosome system exist in nature: diploid XY and ZW systems and haploid UV systems. For many years, research has focused exclusively on XY and ZW systems, leaving UV chromosomes and haploid sex determination largely neglected. Here, we perform a detailed analysis of DNA sequence neutral diversity levels across the U and V sex chromosomes of the model brown alga Ectocarpus using a large population dataset. We show that the U and V non-recombining regions of the sex chromosomes (SDR) exhibit about half as much neutral diversity as the autosomes. This difference is consistent with the reduced effective population size of these regions compared with the rest of the genome, suggesting that the influence of additional factors such as background selection or selective sweeps is minimal. The pseudoautosomal region (PAR) of this UV system, in contrast, exhibited surprisingly high neutral diversity and there were several indications that genes in this region may be under balancing selection. The PAR of Ectocarpus is known to exhibit unusual genomic features and our results lay the foundation for further work aimed at understanding whether, and to what extent, these structural features underlie the high level of genetic diversity. Overall, this study fills a gap between available information on genetic diversity in XY/ZW systems and UV systems and significantly contributes to advancing our knowledge of the evolution of UV sex chromosomes.

Effects of partial selfing on the equilibrium genetic variance, mutation load, and inbreeding depression under stabilizing selection.

The mating system of a species is expected to have important effects on its genetic diversity. In this article, we explore the effects of partial selfing on the equilibrium genetic variance Vg , mutation load L, and inbreeding depression δ under stabilizing selection acting on a arbitrary number n of quantitative traits coded by biallelic loci with additive effects. When the U/n ratio is low (where U is the total haploid mutation rate on selected traits) and effective recombination rates are sufficiently high, genetic associations between loci are negligible and the genetic variance, mutation load, and inbreeding depression are well predicted by approximations based on single-locus models. For higher values of U/n and/or lower effective recombination, moderate genetic associations generated by epistasis tend to increase Vg , L, and δ, this regime being well predicted by approximations including the effects of pairwise associations between loci. For yet higher values of U/n and/or lower effective recombination, a different regime is reached under which the maintenance of coadapted gene complexes reduces Vg , L, and δ. Simulations indicate that the values of Vg , L, and δ are little affected by assumptions regarding the number of possible alleles per locus.

Mutation Rate Evolution in Partially Selfing and Partially Asexual Organisms.

Different factors can influence the evolution of the mutation rate of a species: costs associated with DNA replication fidelity, indirect selection caused by the mutations produced (that should generally favor lower mutation rates, given that most mutations affecting fitness are deleterious), and genetic drift, which may render selection acting on weak mutators inefficient. In this paper, we use a two-locus model to compute the strength of indirect selection acting on a modifier locus that affects the mutation rate toward a deleterious allele at a second, linked, locus, in a population undergoing partial selfing or partial clonality. The results show that uniparental reproduction increases the effect of indirect selection for lower mutation rates. Extrapolating to the case of a whole genome with many deleterious alleles, and introducing a direct cost to DNA replication fidelity, the results can be used to compute the evolutionarily stable mutation rate, U In the absence of mutational bias toward higher U, the analytical prediction fits well with individual-based, multilocus simulation results. When such a bias is added into the simulations, however, genetic drift may lead to the maintenance of higher mutation rates, and this effect may be amplified in highly selfing or highly clonal populations due to their reduced effective population size.

The genetics of speciation: Insights from Fisher's geometric model.

Research in speciation genetics has uncovered many robust patterns in intrinsic reproductive isolation, and fitness landscape models have been useful in interpreting these patterns. Here, we examine fitness landscapes based on Fisher's geometric model. Such landscapes are analogous to models of optimizing selection acting on quantitative traits, and have been widely used to study adaptation and the distribution of mutational effects. We show that, with a few modifications, Fisher's model can generate all of the major findings of introgression studies (including "speciation genes" with strong deleterious effects, complex epistasis and asymmetry), and the major patterns in overall hybrid fitnesses (including Haldane's Rule, the speciation clock, heterosis, hybrid breakdown, and male-female asymmetry in the F1). We compare our approach to alternative modeling frameworks that assign fitnesses to genotypes by identifying combinations of incompatible alleles. In some cases, the predictions are importantly different. For example, Fisher's model can explain conflicting empirical results about the rate at which incompatibilities accumulate with genetic divergence. In other cases, the predictions are identical. For example, the quality of reproductive isolation is little affected by the manner in which populations diverge.

Interactions between Genetic and Ecological Effects on the Evolution of Life Cycles.

Sexual reproduction leads to an alternation between haploid and diploid phases, whose relative length varies widely across taxa. Previous genetical models showed that diploid or haploid life cycles may be favored, depending on dominance interactions and on effective recombination rates. By contrast, niche differentiation between haploids and diploids may favor biphasic life cycles, in which development occurs in both phases. In this article, we explore the interplay between genetical and ecological factors, assuming that deleterious mutations affect the competitivity of individuals within their ecological niche and allowing different effects of mutations in haploids and diploids (including antagonistic selection). We show that selection on a modifier gene affecting the relative length of both phases can be decomposed into a direct selection term favoring the phase with the highest mean fitness (due to either ecological differences or differential effects of mutations) and an indirect selection term favoring the phase in which selection is more efficient. When deleterious alleles occur at many loci and in the presence of ecological differentiation between haploids and diploids, evolutionary branching often occurs and leads to the stable coexistence of alleles coding for haploid and diploid cycles, while temporal variations in niche sizes may stabilize biphasic cycles.

Background Selection in Partially Selfing Populations.

Self-fertilizing species often present lower levels of neutral polymorphism than their outcrossing relatives. Indeed, selfing automatically increases the rate of coalescence per generation, but also enhances the effects of background selection and genetic hitchhiking by reducing the efficiency of recombination. Approximations for the effect of background selection in partially selfing populations have been derived previously, assuming tight linkage between deleterious alleles and neutral loci. However, loosely linked deleterious mutations may have important effects on neutral diversity in highly selfing populations. In this article, I use a general method based on multilocus population genetics theory to express the effect of a deleterious allele on diversity at a linked neutral locus in terms of moments of genetic associations between loci. Expressions for these genetic moments at equilibrium are then computed for arbitrary rates of selfing and recombination. An extrapolation of the results to the case where deleterious alleles segregate at multiple loci is checked using individual-based simulations. At high selfing rates, the tight linkage approximation underestimates the effect of background selection in genomes with moderate to high map length; however, another simple approximation can be obtained for this situation and provides accurate predictions as long as the deleterious mutation rate is not too high.