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 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.

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.

The Pseudoautosomal Regions of the U/V Sex Chromosomes of the Brown Alga Ectocarpus Exhibit Unusual Features.

The recombining regions of sex chromosomes (pseudoautosomal regions, PARs) are predicted to exhibit unusual features due to their being genetically linked to the nonrecombining, sex-determining region. This phenomenon is expected to occur in both diploid (XY, ZW) and haploid (UV) sexual systems, with slightly different consequences for UV sexual systems because of the absence of masking during the haploid phase (when sex is expressed) and because there is no homozygous sex in these systems. Despite a considerable amount of theoretical work on PAR genetics and evolution, these genomic regions have remained poorly characterized empirically. We show here that although the PARs of the U/V sex chromosomes of the brown alga Ectocarpus recombine at a similar rate to autosomal regions of the genome, they exhibit many genomic features typical of nonrecombining regions. The PARs were enriched in clusters of genes that are preferentially, and often exclusively, expressed during the sporophyte generation of the life cycle, and many of these genes appear to have evolved since the Ectocarpales diverged from other brown algal lineages. A modeling-based approach was used to investigate possible evolutionary mechanisms underlying this enrichment in sporophyte-biased genes. Our results are consistent with the evolution of the PAR in haploid systems being influenced by differential selection pressures in males and females acting on alleles that are advantageous during the sporophyte generation of the life cycle.

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.

Masculinization of the x chromosome in the pea aphid.

Evolutionary theory predicts that sexually antagonistic mutations accumulate differentially on the X chromosome and autosomes in species with an XY sex-determination system, with effects (masculinization or feminization of the X) depending on the dominance of mutations. Organisms with alternative modes of inheritance of sex chromosomes offer interesting opportunities for studying sexual conflicts and their resolution, because expectations for the preferred genomic location of sexually antagonistic alleles may differ from standard systems. Aphids display an XX/X0 system and combine an unusual inheritance of the X chromosome with the alternation of sexual and asexual reproduction. In this study, we first investigated theoretically the accumulation of sexually antagonistic mutations on the aphid X chromosome. Our results show that i) the X is always more favourable to the spread of male-beneficial alleles than autosomes, and should thus be enriched in sexually antagonistic alleles beneficial for males, ii) sexually antagonistic mutations beneficial for asexual females accumulate preferentially on autosomes, iii) in contrast to predictions for standard systems, these qualitative results are not affected by the dominance of mutations. Under the assumption that sex-biased gene expression evolves to solve conflicts raised by the spread of sexually antagonistic alleles, one expects that male-biased genes should be enriched on the X while asexual female-biased genes should be enriched on autosomes. Using gene expression data (RNA-Seq) in males, sexual females and asexual females of the pea aphid, we confirm these theoretical predictions. Although other mechanisms than the resolution of sexual antagonism may lead to sex-biased gene expression, we argue that they could hardly explain the observed difference between X and autosomes. On top of reporting a strong masculinization of the aphid X chromosome, our study highlights the relevance of organisms displaying an alternative mode of sex chromosome inheritance to understanding the forces shaping chromosome evolution.

Disentangling the benefits of sex.

Understanding the evolutionary advantage of sexual reproduction remains one of the most fundamental questions in evolutionary biology. Most of the current hypotheses rely on the fact that sex increases genetic variation, thereby enhancing the efficiency of natural selection; an important body of theoretical work has defined the conditions under which sex can be favoured through this effect. Over the last decade, experimental evolution in model organisms has provided evidence that sex indeed allows faster rates of adaptation. A new study on facultatively sexual rotifers shows that increased rates of sex can be favoured during adaptation to new environmental conditions and explores the cause of this effect. The results provide support for the idea that the benefits of increasing genetic variation may compensate for the short-term costs of sexual reproduction.

Pervasive selection or is it ? Why are FST outliers sometimes so frequent?

It is now common for population geneticists to estimate FST for a large number of loci across the genome, before testing for selected loci as being outliers to the FST distribution. One surprising result of such FST scans is the often high proportion (>1% and sometimes >10%) of outliers detected, and this is often interpreted as evidence for pervasive local adaptation. In this issue of Molecular Ecolog, Fourcade et al. (2013) observe that a particularly high rate of FST outliers has often been found in river organisms, such as fishes or damselflies, despite there being no obvious reason why selection should affect a larger proportion of the genomes of these organisms. Using computer simulations, Fourcade et al. (2013) show that the strong correlation in co-ancestry produced in long onedimensional landscapes (such as rivers, valleys, peninsulas, oceanic ridges or coastlines) greatly increases the neutral variance in FST, especially when the landscape is further reticulated into fractal networks. As a consequence, outlier tests have a high rate of false positives, unless this correlation can be taken into account. Fourcade et al.'s study highlights an extreme case of the general problem, first noticed by Robertson (1975a,b) and Nei & Maruyama (1975), that correlated co-ancestry inflates the neutral variance in FST when compared to its expectation under an island model of population structure. Similar warnings about the validity of outlier tests have appeared regularly since then but have not been widely cited in the recent genomics literature. We further emphasize that FST outliers can arise in many different ways and that outlier tests are not designed for situations where the genetic architecture of local adaptation involves many loci.

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.

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.

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 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.

Daily temporal structure in African savanna flower visitation networks and consequences for network sampling.

Ecological interaction networks are a valuable approach to understanding plant-pollinator interactions at the community level. Highly structured daily activity patterns are a feature of the biology of many flower visitors, particularly provisioning female bees, which often visit different floral sources at different times. Such temporal structure implies that presence/absence and relative abundance of specific flower-visitor interactions (links) in interaction networks may be highly sensitive to the daily timing of data collection. Further, relative timing of interactions is central to their possible role in competition or facilitation of seed set among coflowering plants sharing pollinators. To date, however, no study has examined the network impacts of daily temporal variation in visitor activity at a community scale. Here we use temporally structured sampling to examine the consequences of daily activity patterns upon network properties using fully quantified flower-visitor interaction data for a Kenyan savanna habitat. Interactions were sampled at four sequential three-hour time intervals between 06:00 and 18:00, across multiple seasonal time points for two sampling sites. In all data sets the richness and relative abundance of links depended critically on when during the day visitation was observed. Permutation-based null modeling revealed significant temporal structure across daily time intervals at three of the four seasonal time points, driven primarily by patterns in bee activity. This sensitivity of network structure shows the need to consider daily time in network sampling design, both to maximize the probability of sampling links relevant to plant reproductive success and to facilitate appropriate interpretation of interspecific relationships. Our data also suggest that daily structuring at a community level could reduce indirect competitive interactions when coflowering plants share pollinators, as is commonly observed during flowering in highly seasonal habitats.

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).

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.

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.

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.

Diploidy, population structure, and the evolution of recombination.

In diploids, sex affects genetic variation through segregation and recombination. Several recent models on the advantage of recombination have focused on the effect of interaction between selection and drift in finite or structured populations; however, these models considered haploid organisms. In this article, I present a three-locus model of the evolution of recombination in structured diploid populations, including dominance and epistatic effects among alleles. This model shows that dominance generates a selective force against recombination due to the fact that recombination reduces correlations in homozygosity that are generated by population structure. This result is confirmed by multilocus simulations (representing deleterious mutations occurring over a whole genome), showing that when mutations are sufficiently recessive, the population evolves to zero recombination. In the presence of epistasis, the same effect of recombination on correlations in homozygosity generates an advantage for recombination under negative dominance by dominance epistasis (e(d x d)). Additive by additive epistasis (e(a x a)) favors recombination when it is negative and sufficiently weak, while additive by dominance epistasis has less effect. Some of these effects, however, are reversed when the deleterious mutation rate U is sufficiently high: in that case, strongly negative (e(a x a)) can favor recombination, while negative (e(d x d)) disfavors it. Interpretation of these results is given.

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.