The evolution of obligate sex: the roles of sexual selection and recombination

The evolution of sex is one of the greatest mysteries in evolutionary biology. An even greater mystery is the evolution of obligate sex, particularly when competing with facultative sex and not with complete asexuality. Here, we develop a stochastic simulation of an obligate allele invading a facultative population, where males are subject to sexual selection. We identify a range of parameters where sexual selection can contribute to the evolution of obligate sex: Especially when the cost of sex is low, mutation rate is high, and the facultative individuals do not reproduce sexually very often. The advantage of obligate sex becomes larger in the absence of recombination. Surprisingly, obligate sex can take over even when the population has a lower mean fitness as a result. We show that this is due to the high success of obligate males that can compensate the cost of sex.     

Facultative sexual reproduction under frequency-dependent selection on a single locus

The evolution of a facultative sexual strategy that simultaneously produced sexual and asexual individuals was studied theoretically, under negative frequency-dependence of fitness. The organism was considered to be diploid, characterized by two loci concerning fitness and determining sexual strategy, between which a certain degree of linkage existed. The locus concerning fitness was assumed to involve two alleles, resulting in three genotypes, the relative fitness of an individual being defined by a decreasing function of frequency of its own genotype on this locus in the population. The sexual reproductive strategy was considered to be determined by three alleles; asexual, obligate sexual and facultative sexual. Simulations under various linkages between loci and level of frequency dependence of fitness showed that a facultative sexual strategy was generally able to invade and increase in the population. In particular, when the level of frequency dependence was high to some degree, the facultative strain producing many sexual individuals tended to exclusively occupy the population. Namely, the frequency-dependent selection resulted in a predominance of obligate sexual strategy over asexual strategy, simultaneously causing a subordination of the former to the facultative sexual strategy. This indicated that the evolution of sex should be considered carefully with respect to the possibility of invasion of facultative sex.     

The consequences of facultative sex in a prey adapting to predation

A species reproductive mode, along with its associated costs and benefits, can play a significant role in its evolution and survival. Facultative sexuality, being able to reproduce both sexually and asexually, has been deemed evolutionary favourable as the benefits of either mode may be fully realized. In fact, many studies have focused on identifying the benefits of sex and/or the forces selecting for increased rates of sex using facultative sexual species. The costs of either mode, however, can also have a profound impact on a population's evolutionary trajectory. Here, we used experimental evolution and fitness assays to investigate the consequences of facultative sexuality in prey adapting to predation. Specifically, we compared the adaptive response of algal prey populations exposed to constant rotifer predation and which had alternating cycles of asexual and sexual reproduction where sexual episodes were either facultative (sexual and asexual progeny simultaneously propagated) or obligate (only sexual progeny propagated). We found that prey populations with facultative sexual episodes reached a lower final relative fitness and suffered a greater trade‐off in traits under selection, that is defence and competitive ability, as compared to prey populations with obligate sexual episodes. Our results suggest that costs associated with sexual reproduction (germination time) and asexual reproduction (selection interference) were amplified in the facultative sexual prey populations, leading to a reduction in the net advantage of sexuality. Additionally, we found evidence that the cost of sex was reduced in the obligate sexual prey populations because increased selection for sex was observed via the spontaneous production of sexual cells. These results show that certain costs associated with facultative sexuality can affect an organism's evolutionary trajectory.     

"Husband and Wife Do It Together": Sex/Gender Allocation of Labor among the Qhawqhat Lahu of Lancang, Southwest China

In this article, I explore both the diversity and commonality of human labor organization in response to sex difference through an ethnographic study of the sex/gender allocation of labor among the Qhawqhat Lahu of Lancang, China. I argue that the principle of "unity," rather than the more commonly discussed "division," predominantly governs the gendered allocation of labor in Qhawqhat. I demonstrate that the Lahu ideal of gender unity, combined with their practical pursuit of optimal use of household laborers, foster an extraordinarily high degree of joint gender roles in child rearing, as well as in reproductive and productive activities in general. I also show that such an extreme sociocultural system minimizes (although it does not entirely negate) the impact of sex differences. This study may shed some light on the diversity and commonality of human labor organization in response to sex difference by bringing into dialogue more recent approaches to the issue and earlier studies of the "sexual division of labor." [sex/gender allocation of labor, sexual division of labor, anthropology of work, Lahu, China]     

The evolution of apomixis in angiosperms: A reappraisal

Abstract

Apomixis, the asexual reproduction via seed, has long been regarded a blind alley of evolution. This hypothesis was based on the assumption that apomixis is an irreversible, phylogenetically derived trait that would rapidly lead to extinction of the respective lineages. However, recent updates of the taxonomic distribution of apomixis in angiosperms suggest an alternative evolutionary scenario. Apomixis is taxonomically scattered and occurs in both early and late branching lineages, with several reversals from apomixis to obligate sex along phylogeny. Genetic control of apomixis is based on altered expression patterns of the same genes that control sexual development; epigenetic changes following polyploidization and/or hybridization may trigger shifts from sexuality to apomixis. Mendelian inheritance confirms the facultative nature and possible reversibility of apomixis to sexual reproduction. Apomixis, therefore, could represent a transition period in the evolution of polyploid complexes, with polyspory in paleopolyploids being a remnant of lost apomixis. In neopolyploids, apomixis helps to overcome sterility and allows for geographical range expansions of agamic polyploid complexes. The facultative nature of apomixis allows for reversal to sexuality and further speciation of paleopolyploid lineages. Thus, apomixis may facilitate diversification of polyploid complexes and evolution in angiosperms.     

Jealousy in a small-scale,natural fertility population: the roles of paternity,investment and love in jealous response

Evolutionary scientists have predicted a universal sex difference in response to different forms of infidelity, with men expected to be more upset than women by a sexual infidelity when both a sexual transgression and an emotional transgression occur. Although this finding has proven to be robust, the vast majority of studies have occurred in industrialized countries and student populations. Here I present the first test of the jealousy hypothesis among a small-scale, natural fertility population, the Himba of Namibia. In this population, the majority of both men and women report greater distress over a sexual infidelity, with men reaching an almost unanimous consensus (96%). Despite the skew for both men and women, there is a significant sex difference in the direction predicted by the evolutionary hypothesis, providing further support for this view. The increased risks of both pregnancy and paternity loss that occur in this natural fertility population may help to explain why these results differ from previously studied populations. More broadly, these data suggest that both the type and the intensity of jealousy expressed may be facultative responses and that further investigation of correlates related to life history trade-offs, forms of investment, and the sexual division of labor can help us to understand the inter-cultural variation in jealous response.     

Pseudohomothallism and Evolution of the Mating-Type Chromosome in Neurospora Tetrasperma

Ascospores of Neurospora tetrasperma normally contain nuclei of both mating-type idiomorphs (a and A), resulting in self-fertile heterokaryons (a type of sexual reproduction termed pseudohomothallism). Occasional homokaryotic self-sterile strains (either a or A) behave as heterothallics and, in principle, provide N. tetrasperma with a means for facultative outcrossing. This study was conceived as an investigation of the population biology of N. tetrasperma to assess levels of intrastrain heterokaryosis (heterozygosity). The unexpected result was that the mating-type chromosome and autosomes exhibited very different patterns of evolution, apparently because of suppressed recombination between mating-type chromosomes. Analysis of sequences on the mating-type chromosomes of wild-collected self-fertile strains revealed high levels of genetic variability between sibling A and a nuclei. In contrast, sequences on autosomes of sibling A and a nuclei exhibited nearly complete homogeneity. Conservation of distinct haplotype combinations on A and a mating-type chromosomes in strains from diverse locations further suggested an absence of recombination over substantial periods of evolutionary time. The suppression of recombination on the N. tetrasperma mating-type chromosome, expected to ensure a high frequency of self fertility, presents an interesting parallel with, and possible model for studying aspects of, the evolution of mammalian sex chromosomes.     

Reproductive strategy and population variability in the facultative apomict Hieracium pilosella (Asteraceae)

Molecular studies of apomictic plant species often detect more genotypic variation than predicted from their assumed reproductive mode. The two most commonly invoked mechanisms to explain these high levels of variation are recombination, via facultative sexuality, and mutation. The potential for sexual reproduction in the facultative apomict Hieracium pilosella (Asteraceae) was determined at three field sites by artificially pollinating with the closely related, but morphologically distinct, H. aurantiacum. The level of genotypic variation at the three sites was recorded using inter-simple sequence repeats (ISSRs). There was a significant, positive relationship between the measured potential for sexual reproduction and population genotypic variability, indicating that sex has played a role in the structuring of these populations; however, a causal relationship cannot be stated because of the use of regression. We also applied the recently developed method of compatibility analysis. Compatibility analysis can determine, using the occurrence of "character incompatibilities," whether patterns of variation observed in populations are most parsimoniously explained by mutation or recombination. Compatibility analysis also indicated that sexual reproduction had played a role in generating genotypic diversity in these populations. Combining these different types of data may give a greater understanding of the potential for the generation of genotypic diversity in facultative apomictic populations.     

Genetic tests of ancient asexuality in Root Knot Nematodes reveal recent hybrid origins

Background  

The existence of "ancient asexuals", taxa that have persisted for long periods of evolutionary history without sexual recombination, is both controversial and important for our understanding of the evolution and maintenance of sexual reproduction. A lack of sex has consequences not only for the ecology of the asexual organism but also for its genome. Several genetic signatures are predicted from long-term asexual (apomictic) reproduction including (i) large "allelic" sequence divergence (ii) lack of phylogenetic clustering of "alleles" within morphological species and (iii) decay and loss of genes specific to meiosis and sexual reproduction. These genetic signatures can be hard to assess since it is difficult to demonstrate the allelic nature of very divergent sequences, divergence levels may be complicated by processes such as inter-specific hybridization, and genes may have secondary roles unrelated to sexual reproduction. Apomictic species of Meloidogyne root knot nematodes have been suggested previously to be ancient asexuals. Their relatives reproduce by meiotic parthenogenesis or facultative sexuality, which in combination with the abundance of nematode genomic sequence data, makes them a powerful system in which to study the consequences of reproductive mode on genomic divergence.     

Coalescent Times and Patterns of Genetic Diversity in Species with Facultative Sex: Effects of Gene Conversion,Population Structure,and Heterogeneity

Many diploid organisms undergo facultative sexual reproduction. However, little is currently known concerning the distribution of neutral genetic variation among facultative sexual organisms except in very simple cases. Understanding this distribution is important when making inferences about rates of sexual reproduction, effective population size, and demographic history. Here we extend coalescent theory in diploids with facultative sex to consider gene conversion, selfing, population subdivision, and temporal and spatial heterogeneity in rates of sex. In addition to analytical results for two-sample coalescent times, we outline a coalescent algorithm that accommodates the complexities arising from partial sex; this algorithm can be used to generate multisample coalescent distributions. A key result is that when sex is rare, gene conversion becomes a significant force in reducing diversity within individuals. This can reduce genomic signatures of infrequent sex (i.e., elevated within-individual allelic sequence divergence) or entirely reverse the predicted patterns. These models offer improved methods for assessing null patterns of molecular variation in facultative sexual organisms.     

A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis

Sexual reproduction in eukaryotes is accomplished by meiosis, a complex and specialized process of cell division that results in haploid cells (e.g., gametes). The stereotypical reductive division in meiosis is a major evolutionary innovation in eukaryotic cells, and delineating its history is key to understanding the evolution of sex. Meiosis arose early in eukaryotic evolution, but when and how meiosis arose and whether all eukaryotes have meiosis remain open questions. The known phylogenetic distribution of meiosis comprises plants, animals, fungi, and numerous protists. Diplomonads including Giardia intestinalis (syn. G. lamblia) are not known to have a sexual cycle; these protists may be an early-diverging lineage and could represent a premeiotic stage in eukaryotic evolution. We surveyed the ongoing G. intestinalis genome project data and have identified, verified, and analyzed a core set of putative meiotic genes-including five meiosis-specific genes-that are widely present among sexual eukaryotes. The presence of these genes indicates that: (1) Giardia is capable of meiosis and, thus, sexual reproduction, (2) the evolution of meiosis occurred early in eukaryotic evolution, and (3) the conserved meiotic machinery comprises a large set of genes that encode a variety of component proteins, including those involved in meiotic recombination.     

The evolution of sex: empirical insights into the roles of epistasis and drift

Despite many years of theoretical and experimental work, the explanation for why sex is so common as a reproductive strategy continues to resist understanding. Recent empirical work has addressed key questions in this field, especially regarding rates of mutation accumulation in sexual and asexual organisms, and the roles of negative epistasis and drift as sources of adaptive constraint in asexually reproducing organisms. At the same time, new ideas about the evolution of sexual recombination are being tested, including intriguing suggestions of an important interplay between sex and genetic architecture, which indicate that sex and recombination could have affected their own evolution.     

Sex as a response to oxidative stress: the effect of antioxidants on sexual induction in a facultatively sexual lineage

The evolution of sex is one of the long-standing unsolved problems in biology. Although in many lineages sex is an obligatory part of the life cycle and is associated with reproduction, in prokaryotes and many lower eukaryotes, sex is facultative, occurs in response to stress and often involves the formation of a stress-resistant dormant form. The proximate and ultimate causes of the connection between stress and sex in facultatively sexual lineages are unclear. Because most forms of stress result in the overproduction of cellular reactive oxygen species (ROS), we address the hypothesis that this connection involves ROS and possibly reflects the ancestral role of sex as an adaptive response to the damaging effects of stress-induced ROS (i.e. oxidative stress). Here, we report that two antioxidants inhibit sexual induction in a facultatively sexual species - the multicellular green alga, Volvox carteri. Furthermore, the nature of the sex response and the effect of an iron chelator on sexual induction are consistent with sex being a response to the DNA-damaging effects of ROS. In addition, we present preliminary data to suggest that sex, cell-cycle arrest and apoptosis are alternative responses to increased levels of oxidative stress.     

Relative effects of segregation and recombination on the evolution of sex in finite diploid populations

The mechanism of reproducing more viable offspring in response to selection is a major factor influencing the advantages of sex. In diploids, sexual reproduction combines genotype by recombination and segregation. Theoretical studies of sexual reproduction have investigated the advantage of recombination in haploids. However, the potential advantage of segregation in diploids is less studied. This study aimed to quantify the relative contribution of recombination and segregation to the evolution of sex in finite diploids by using multilocus simulations. The mean fitness of a sexually or asexually reproduced population was calculated to describe the long-term effects of sex. The evolutionary fate of a sex or recombination modifier was also monitored to investigate the short-term effects of sex. Two different scenarios of mutations were considered: (1) only deleterious mutations were present and (2) a combination of deleterious and beneficial mutations. Results showed that the combined effects of segregation and recombination strongly contributed to the evolution of sex in diploids. If deleterious mutations were only present, segregation efficiently slowed down the speed of Muller''s ratchet. As the recombination level was increased, the accumulation of deleterious mutations was totally inhibited and recombination substantially contributed to the evolution of sex. The presence of beneficial mutations evidently increased the fixation rate of a recombination modifier. We also observed that the twofold cost of sex was easily to overcome in diploids if a sex modifier caused a moderate frequency of sex.     

Genetic Variation in Reproductive Investment Across an Ephemerality Gradient in Daphnia pulex

Species across the tree of life can switch between asexual and sexual reproduction. In facultatively sexual species, the ability to switch between reproductive modes is often environmentally dependent and subject to local adaptation. However, the ecological and evolutionary factors that influence the maintenance and turnover of polymorphism associated with facultative sex remain unclear. We studied the ecological and evolutionary dynamics of reproductive investment in the facultatively sexual model species, Daphnia pulex. We found that patterns of clonal diversity, but not genetic diversity varied among ponds consistent with the predicted relationship between ephemerality and clonal structure. Reconstruction of a multi-year pedigree demonstrated the coexistence of clones that differ in their investment into male production. Mapping of quantitative variation in male production using lab-generated and field-collected individuals identified multiple putative quantitative trait loci (QTL) underlying this trait, and we identified a plausible candidate gene. The evolutionary history of these QTL suggests that they are relatively young, and male limitation in this system is a rapidly evolving trait. Our work highlights the dynamic nature of the genetic structure and composition of facultative sex across space and time and suggests that quantitative genetic variation in reproductive strategy can undergo rapid evolutionary turnover.     

Reduced recombination in gynodioecious populations of a facultative apomictic orchid

Many plants combine sexual reproduction with some form of asexual reproduction to different degrees, and lower genetic diversity is expected with asexuality. Moreover, the ratios of sexual morphs in species with gender dimorphism are expected to vary in proportion to the reproductive success of the sexual process. Hence, sex ratios can directly influence the genetic structure and diversity of a population. We investigated genotypic diversity in 23 populations of a facultative, apomictic gynodioecious orchid, Satyrium ciliatum, to examine the effect on genotypic diversity of variation in the frequency of females and in the amount of sexual reproduction. The study involved one pure female, seven gynodioecious (both females and hermaphrodites present) and 15 hermaphroditic populations. Pollinia receipt was higher in hermaphroditic than in gynodioecious populations. Analyses of variation in ISSRs demonstrated that genotypic diversity was high in all populations and was not significantly different between hermaphroditic and gynodioecious populations. We used character compatibility analysis to determine the extent to which recombination by sexual reproduction contributed to genotypic diversity. The results indicate that the contribution of recombination to genotypic diversity is higher in hermaphroditic than in gynodioecious populations, consistent with the finding that hermaphroditic populations received higher amounts of pollinia. Our finding of reduced recombination in gynodioecious populations suggests that maintenance of sex in hermaphrodites plays an important role in generating genotypic diversity in this apomictic orchid.     

Sexual reproduction and diversity: Connection between sexual selection and biological communities via population dynamics

Sexual reproduction is a mysterious phenomenon. Most animals and plants invest in sexual reproduction, even though it is more costly than asexual reproduction. Theoretical studies suggest that occasional or conditional use of sexual reproduction, involving facultative switching between sexual and asexual reproduction, is the optimal reproductive strategy. However, obligate sexual reproduction is common in nature. Recent studies suggest that the evolution of facultative sexual reproduction is prevented by males that coerce females into sexual fertilization; thus, sexual reproduction has the potential to enforce costs on a given species. Here, the effect of sex on biodiversity is explored by evaluating the reproductive costs arising from sex. Sex provides atypical selection pressure that favors traits that increase fertilization success, even at the expense of population growth rates, that is, sexual selection. The strength of sexual selection depends on the density of a given species. Sexual selection often causes strong negative effects on the population growth rates of species that occur at high density. Conversely, a species that reduces its density is released from this negative effect, and so increases its growth rate. Thus, this negative density-dependent effect on population growth that arises from sexual selection could be used to rescue endangered species from extinction, prevent the overgrowth of common species and promote the coexistence of competitive species. Recent publications on sexual reproduction provide several predictions related to the evolution of reproductive strategies, which is an important step toward integrating evolutionary dynamics, demographic dynamics and community dynamics.     

The origin and evolution of sexual reproduction up to the evolution of the male-female phenomenon

Summary Sexual reproduction is a composite, not a singular, phenomenon and as such can be subdivided into a number of componentsi.e. fusion, recombination, fission, and the male-female phenomenon. These components can evolve independently, though any evolutionary change in one component is likely to influence the future evolution of the other components. The ambiguity that surrounds the term sex due to a failure to recognise the composite nature of sexual reproduction has led to considerable confusion in past discussions of the evolution of the phenomenon. This paper considers the possible chronological interaction of the components of sexual reproduction both with each other and with the sequence of selective pressures that seem likely to have acted. This chronological approach is used to consider: the origin of sexual reproduction; the evolution of sexual reproduction in the common ancestor of the procaryotes and eucaryotes; the modification of the ancestral system in the procaryote line following the procaryote-eucaryote dichotomy; and the modification of the ancestral system in the eucaryote line up to the origin of the male-female phenomenon.It is suggested that the fusion and recombination of the first living organisms were chronological continuations of the fusion and recombination of complex organic molecules that led up to the origin of life. The evolution of the third major component of sexual reproductioni.e. fission (replication), by definition coincided with the origin of life. Initial selection on the components of sexual reproduction are likely to have been related to the optimum manifestations of size, complexity, diversity, multiplication, and distribution. Resultant early evolutionary trends are likely to have been: selective fusion between more-similar organisms; increase in number of fissions per fusion; and less recombination.The procaryote-eucaryote dichotomy is argued to have evolved in response to the increasing cellular problems of packing and replicating an increasing amount of hereditary material. The evolution of a single circular hereditary organelle in the procaryote line is argued to have led to the loss of total fusion and the specialisation of individuals into either donors or recipients. The donor-recipient phenomenon of procaryotes is directly analogous to the male-female phenomenon of eucaryotes and leads to parallel evolution due to sexual selection in both groups. In the eucaryote line the ancestral mechanism of sexual reproduction is argued to have persisted through, but to have been greatly modified by, the evolution of complex machinery (mitotic/meiotic) for the handling of multiple hereditary organelles at cell division and reduction division. The evolutionary modification of the ancestral system of sexual reproduction is suggested to have led in eucaryotes to the evolution of: the species phenomenon; allelic recombination; and the male-female phenomenon.     

The advantages of segregation and the evolution of sex

In diploids, sexual reproduction promotes both the segregation of alleles at the same locus and the recombination of alleles at different loci. This article is the first to investigate the possibility that sex might have evolved and been maintained to promote segregation, using a model that incorporates both a general selection regime and modifier alleles that alter an individual's allocation to sexual vs. asexual reproduction. The fate of different modifier alleles was found to depend strongly on the strength of selection at fitness loci and on the presence of inbreeding among individuals undergoing sexual reproduction. When selection is weak and mating occurs randomly among sexually produced gametes, reductions in the occurrence of sex are favored, but the genome-wide strength of selection is extremely small. In contrast, when selection is weak and some inbreeding occurs among gametes, increased allocation to sexual reproduction is expected as long as deleterious mutations are partially recessive and/or beneficial mutations are partially dominant. Under strong selection, the conditions under which increased allocation to sex evolves are reversed. Because deleterious mutations are typically considered to be partially recessive and weakly selected and because most populations exhibit some degree of inbreeding, this model predicts that higher frequencies of sex would evolve and be maintained as a consequence of the effects of segregation. Even with low levels of inbreeding, selection is stronger on a modifier that promotes segregation than on a modifier that promotes recombination, suggesting that the benefits of segregation are more likely than the benefits of recombination to have driven the evolution of sexual reproduction in diploids.     

Sex and recombination in the Hötzel aging model

Why sex evolved and it prevails in nature remain one of thegreat puzzles of evolution. Most biologists would explain that it promotes genetic variability, however this explanation suffers from several difficulties. What advantages might sex confer? The present communication aims at certain investigations related to this question, in this way we introduce sexual recombination on the Hötzel model (with males and females) and wecompare these results with those from asexual reproduction without recombination.