Can punishment maintain sex?

Individuals who reproduce asexually have a two-fold advantage over their sexually-reproducing counterparts as they are able to reproduce twice as fast. Explaining why sexual reproduction is favoured over asexual reproduction therefore remains an important challenge in evolutionary biology. Various mechanisms involving resistance to parasites, adaptation to novel environments and helping to purge the genome of deleterious mutations have all been proposed as potential mechanisms which could promote the evolution of sex. A recent article has suggested that spiteful males may help to reduce the two-fold advantage of asexual females. Here I discuss this idea, and further ask whether punishment of asexual females by sexual females could be one way in which sexual reproduction could be maintained in groups of animals; in light of recent research on the repression of competition, it could be possible that asexual females which reproduce faster than their sexual counterparts will be punished for using group resources. It may therefore be possible that the behaviour of sexual individuals towards asexual females could have fitness consequences which could potentially reduce the two-fold advantage they gain from reproducing parthenogenetically.     

EXPERIMENTAL STUDIES OF THE EVOLUTIONARY SIGNIFICANCE OF SEXUAL REPRODUCTION. VI. A GREENHOUSE TEST OF THE SIB-COMPETITION HYPOTHESES

This study tests the hypothesis that competition among groups of sexual and asexual siblings generates an advantage for sexual females. Individual tillers of Anthoxanthum odoratum were planted singly, among other siblings from the same family, and among groups of sexual and asexual siblings from different families in pots in an unheated greenhouse. Unlike previous field experiments, there was little difference between the performance of sexual and clonal tillers after two years, despite strong treatment effects and high mortality. The results demonstrate that sib competition does not generate an advantage for sexual reproduction in biotically simple environments.     

Soft selection reduces loss of heterozygosity in asexual reproduction

The adaptive value of sexual reproduction is still debated in evolutionary theory. It has been proposed that the advantage of sexual reproduction over asexual reproduction is to promote genetic diversity, to prevent the accumulation of harmful mutations or to preserve heterozygosity. Since these hypothetical advantages depend on the type of asexual reproduction, understanding how selection affects the taxonomic distribution of each type could help us discriminate between existing hypotheses. Here, I argue that soft selection, competition among embryos or offspring in selection arenas prior to the hard selection of the adult phase, reduces loss of heterozygosity in certain types of asexual reproduction. Since loss of heterozygosity leads to the unmasking of recessive deleterious mutations in the progeny of asexual individuals, soft selection facilitates the evolution of these types of asexual reproduction. Using a population genetics model, I calculate how loss of heterozygosity affects fitness for different types of apomixis and automixis, and I show that soft selection significantly reduces loss of heterozygosity, hence increases fitness, in apomixis with suppression of the first meiotic division and in automixis with central fusion, the most common types of asexual reproduction. Therefore, if sexual reproduction evolved to preserve heterozygosity, soft selection should be associated with these types of asexual reproduction. I discuss the evidence for this prediction and how this and other observations on the distribution of different types of asexual reproduction in nature is consistent with the heterozygosity hypothesis.     

Genetic variation in sexual and clonal lineages of a freshwater snail

Sexual reproduction within natural populations of most plants and animals continues to remain an enigma in evolutionary biology. That the enigma persists is not for lack of testable hypotheses but rather because of the lack of suitable study systems in which sexual and asexual females coexist. Here we review our studies on one such organism, the freshwater snail Potamopyrgus antipodarum (Gray). We also present new data that bear on hypotheses for the maintenance of sex and its relationship to clonal diversity. We have found that sexual populations of the snail are composed of diploid females and males, while clonal populations are composed of a high diversity of triploid apomictic females. Sexual and asexual individuals coexist in stable frequencies in many ‘mixed’ populations; genetic data indicate that clones from these mixed populations originated from the local population of sexual individuals without interspecific hybridization. Field data show that clonal and sexual snails have completely overlapping life histories, but individual clonal genotypes are less variable than individuals from the sympatric sexual population. Field data also show segregation of clones among depth‐specific habitat zones within a lake, but clonal diversity remains high even within habitats. A new laboratory experiment revealed extensive clonal variation in reproductive rate, a result which suggests that clonal diversity would be low in nature without some form of frequency‐dependent selection. New results from a long‐term field study of a natural, asexual population reveal that clonal diversity remained nearly constant over a 10‐year period. Nonetheless, clonal turnover occurs, and it occurs in a manner that is consistent with parasite‐mediated, frequency‐dependent selection. Reciprocal cross‐infection experiments have further shown that parasites are more infective to sympatric host snails than to allopatric snails, and that they are also more infective to common clones than rare clones within asexual host populations. Hence we suggest that sexual reproduction in these snails may be maintained, at least in part, by locally adapted parasites. Parasite‐mediated selection possibly also contributes to the maintenance of local clonal diversity within habitats, while clonal selection may be responsible for the distribution of clones among habitats. © 2003 The Linnean Society of London. Biological Journal of the Linnean Society 2003, 79 , 165–181.     

Genetics of decayed sexual traits in a parasitoid wasp with endosymbiont-induced asexuality

Trait decay may occur when selective pressures shift, owing to changes in environment or life style, rendering formerly adaptive traits non-functional or even maladaptive. It remains largely unknown if such decay would stem from multiple mutations with small effects or rather involve few loci with major phenotypic effects. Here, we investigate the decay of female sexual traits, and the genetic causes thereof, in a transition from haplodiploid sexual reproduction to endosymbiont-induced asexual reproduction in the parasitoid wasp Asobara japonica. We take advantage of the fact that asexual females cured of their endosymbionts produce sons instead of daughters, and that these sons can be crossed with sexual females. By combining behavioral experiments with crosses designed to introgress alleles from the asexual into the sexual genome, we found that sexual attractiveness, mating, egg fertilization and plastic adjustment of offspring sex ratio (in response to variation in local mate competition) are decayed in asexual A. japonica females. Furthermore, introgression experiments revealed that the propensity for cured asexual females to produce only sons (because of decayed sexual attractiveness, mating behavior and/or egg fertilization) is likely caused by recessive genetic effects at a single locus. Recessive effects were also found to cause decay of plastic sex-ratio adjustment under variable levels of local mate competition. Our results suggest that few recessive mutations drive decay of female sexual traits, at least in asexual species deriving from haplodiploid sexual ancestors.     

Within‐population covariation between sexual reproduction and susceptibility to local parasites

Evolutionary biology has yet to reconcile the ubiquity of sex with its costs relative to asexual reproduction. Here, we test the hypothesis that coevolving parasites maintain sex in their hosts. Specifically, we examined the distributions of sexual reproduction and susceptibility to local parasites within a single population of freshwater snails (Potamopyrgus antipodarum). Susceptibility to local trematode parasites (Microphallus sp.) is a relative measure of the strength of coevolutionary selection in this system. Thus, if coevolving parasites maintain sex, sexual snails should be common where susceptibility is high. We tested this prediction in a mixed population of sexual and asexual snails by measuring the susceptibility of snails from multiple sites in a lake. Consistent with the prediction, the frequency of sexual snails was tightly and positively correlated with susceptibility to local parasites. Strikingly, in just two years, asexual females increased in frequency at sites where susceptibility declined. We also found that the frequency of sexual females covaries more strongly with susceptibility than with the prevalence of Microphallus infection in the field. In linking susceptibility to the frequency of sexual hosts, our results directly implicate spatial variation in coevolutionary selection in driving the geographic mosaic of sex.     

Evolutionary traction: the cost of adaptation and the evolution of sex

The advantage of sexual reproduction remains a puzzle for evolutionary biologists. Everything else being equal, asexual populations are expected to have twice the number of offspring produced by similar sexual populations. Yet, asexual species are uncommon among higher eukaryotes. In models assuming small populations, high mutation rates, or frequent environmental changes, sexual reproduction seems to have at least a two-fold advantage over asexuality. But the advantage of sex for large populations, low mutation rates, and rare or mild environmental changes remains a conundrum. Here we show that without recombination, rare advantageous mutations can result in increased accumulation of deleterious mutations ('evolutionary traction'), which explains the long-term advantage of sex under a wide parameter range.     

INBREEDING DEPRESSION VARIES WITH INVESTMENT IN SEX IN A FACULTATIVE PARTHENOGEN

The reproductive mode of facultative parthenogens allows recessive mutations that accumulate during the asexual phase to be unmasked following sexual reproduction. Longer periods of asexual reproduction should increase the accumulation of deleterious mutations within individuals, reduce population-level genetic diversity via competition and increase the probability of mating among close relatives. Having documented that the investment in sexual reproduction differs among populations and clones of Daphnia pulicaria , we ask if this variation is predictive of the level of inbreeding depression across populations. In four lake populations that vary in sex investment, we raised multiple families (mother, field-produced daughter, laboratory-produced daughter) on high food and estimated the fitness reduction in both sexually produced offspring relative to the maternal genotype. Inbred individuals had lower fitness than their field-produced siblings. The magnitude of fitness reduction in inbred offspring increased as population-level investment in sex decreased. However, there was less of a fitness reduction following sex in the field-produced daughters, suggesting that many field-collected mothers were involved in outcross mating.     

Asexual reproduction and somatic growth of the fissiparous sea star Allostichaster polyplax in New Zealand

Allostichaster polyplax is a fissiparous (capable of reproducing asexually by fission) sea star found in intertidal and shallow subtidal habitats in New Zealand and Australia. A localized population of A. polyplax occurred at a density of 2.7?individuals?m^?2 in an intertidal boulder field at Otago Harbour, South Island, New Zealand. The percentage of sea stars undergoing fission, recorded from January 2010 to March 2011, peaked in January (midsummer) in both years. The frequency of fission decreased for larger sea stars (mean arm length, R?>?25?mm), suggesting an ontogenic shift from asexual to sexual reproduction. Effects of fission (i.e. arm regeneration) and food availability (small gastropods) on growth, storage and sexual reproduction were examined in a factorial laboratory experiment. There was no effect of arm regeneration or food on total arm growth. Storage capacity, measured as pyloric caeca index (PCI), was greater in full-armed than regenerating sea stars, and greater in fed than starved individuals. Fed individuals had a similar PCI as field-collected ones. Gonads were observed in two individuals (males) in the full-armed and fed treatment. Fission did not occur during the experiment. Feeding rate on snails was greater for full-armed than regenerating sea stars. Water temperature had a weak positive effect on the feeding rate of regenerating sea stars. Our findings suggest that fission and subsequent growth of ramets can sustain demographically stable and geographically isolated populations of A. polyplax. The role of sexual reproduction in population dynamics and connectivity of this species (and fissiparous sea stars in general) remains equivocal and requires further research on genetic differentiation within and among populations.     

Why reproduce sexually?

There is reason to believe that intense selection, such that only a small minority at the top of the fitness distribution has any appreciable chance of survival, can sometimes give sexual reproduction an immediate (one-life-cycle) advantage over asexual. The advantage must be great enough to balance the 50% loss of genetic material in meiosis.One model shows the advantage to be frequency-dependent in life cycles in which there are several asexual generations and one sexual. The observed frequency of sexual reproduction in such a life cycle is explained as an evolutionary equilibrium by this model. In another model the optimum frequency of asexual reproduction drops to zero as fecundity and competition increase. This explains the exclusively sexual reproduction of such fecund organism as elms and oysters. Once lost, asexual reproduction may be difficult to evolve secondarily. This explains the presence of such exclusively sexual, low-fecundity organisms as the higher vertebrates.     

Genetic signature of amphimixis allows for the detection and fine scale localization of sexual reproduction events in a mainly parthenogenetic nematode

Asexuality is an important mode of reproduction in eukaryotic taxa and has a theoretical advantage over sexual reproduction because of the increased ability to propagate genes. Despite this advantage, hidden signs of cryptic sex have been discovered in the genomes of asexual organisms. This has provided an interesting way to address the evolutionary impact of sex in plant and animal populations. However, the identification of rare sexual reproduction events in mainly asexual species has remained a challenging task. We examined the reproductive history in populations of the plant parasitic nematode Xiphinema index by genotyping individuals collected from six grapevine fields using seven microsatellite markers. A high level of linkage disequilibrium and heterozygous excess suggested a clonality rate of 95–100%. However, we also detected rare sexual reproduction events within these highly clonal populations. By combining highly polymorphic markers with an appropriate hierarchical sampling, and using both Bayesian and multivariate analysis with phylogenetic reconstructions, we were able to identify a small number of sexually produced individuals at the overlapping zones between different genetic clusters. This suggested that sexual reproduction was favoured when and where two nematode patches came into contact. Among fields, a high degree of genetic differentiation indicated a low level of gene flow between populations. Rare genotypes that were shared by several populations suggested passive dispersal by human activities, possibly through the introduction of infected plants from nurseries. We conclude that our method can be used to detect and locate sexual events in various predominantly asexual species.     

Resource competition between genetically varied and genetically uniform populations of Daphnia pulex (Leydig): does sexual reproduction confer a short‐term ecological advantage?

Small competitive advantages may suffice to compensate for a large disadvantage in intrinsic growth capacity. This well‐known principle from ecology has recently been applied to the enduring question of how sexual reproduction can persist in the face of invasion by female‐only parthenogens. Small competitive advantages resulting directly from sexual reproduction are predicted to cancel a two‐fold disadvantage in intrinsic growth capacity caused by males (which do not themselves produce offspring) comprising half the sexual population. In this paper we test the principal assumption of this theory, that the genetic variation produced by sexual reproduction confers a competitive advantage over self‐identical asexual invaders. We set up competition between a diverse clonal assembly of Daphnia pulex and genetically uniform populations from single clones. At young ages, the population comprising genetically varied Daphnia had significantly higher birth rates in competition with populations of genetically uniform Daphnia than in competition with itself, indicating competitive release and a Lotka–Volterra competition coefficient α₁₂ < 1. No such difference was apparent under conditions of greater food stress, possibly due to individuals channelling more energy into survival, or for old‐aged populations, possibly as a result of reduced selective pressures for high reproduction in old females. Mean birth rates differed between the clones at all ages in the presence of competition, providing evidence of variation in life history traits between clones. A Lotka–Volterra model predicted empirical estimates of α₁₂ = 0.896 (genetically uniform on varied) and α₂₁ = 1.010 (varied on uniform), which permits immediate coexistence of a sexual population of D. pulex even with an asexual lineage having twice the intrinsic growth capacity. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85 , 111–123.     

Radical amino acid mutations persist longer in the absence of sex

Harmful mutations are ubiquitous and inevitable, and the rate at which these mutations are removed from populations is a critical determinant of evolutionary fate. Closely related sexual and asexual taxa provide a particularly powerful setting to study deleterious mutation elimination because sexual reproduction should facilitate mutational clearance by reducing selective interference between sites and by allowing the production of offspring with different mutational complements than their parents. Here, we compared the rate of removal of conservative (i.e., similar biochemical properties) and radical (i.e., distinct biochemical properties) nonsynonymous mutations from mitochondrial genomes of sexual versus asexual Potamopyrgus antipodarum, a New Zealand freshwater snail characterized by coexisting and ecologically similar sexual and asexual lineages. Our analyses revealed that radical nonsynonymous mutations are cleared at higher rates than conservative changes and that sexual lineages eliminate radical changes more rapidly than asexual counterparts. These results are consistent with reduced efficacy of purifying selection in asexual lineages allowing harmful mutations to remain polymorphic longer than in sexual lineages. Together, these data illuminate some of the population‐level processes contributing to mitochondrial mutation accumulation and suggest that mutation accumulation could influence the outcome of competition between sexual and asexual lineages.     

The effects of deleterious mutations in cyclically parthenogenetic organisms

Cyclically parthenogenetic organisms experience benefits of both sexual and asexual reproductive modes in a constant environment. Sexual reproduction generates new genotypes and may facilitate the purging of deleterious mutations whereas asexuality has a two-fold advantage and enables maintenance of well-fitted genotypes. Asexual reproduction can have a drawback as increased linkage may lead to the accumulation of deleterious mutations. This study presents the results of Monte Carlo simulations of small and infinite diploid populations, with deleterious mutations occurring at multiple loci. The recombination rate and the length of the asexual period, interrupted by sexual reproduction, are allowed to vary. Here I show that the fitness of cyclical parthenogenetic population is dependent on the length of the asexual period. Increased length of the asexual period can lead both to increased segregational load following sexual reproduction and to a stronger effect of deleterious mutations on variation at a linked neutral marker, either by reducing or increasing the variation.     

EXPERIMENTAL STUDIES OF THE EVOLUTIONARY SIGNIFICANCE OF SEXUAL REPRODUCTION. V. A FIELD TEST OF THE SIB-COMPETITION LOTTERY HYPOTHESIS

Sexually and asexually derived tillers of Anthoxanthum odoratum were planted directly in the field to test the hypothesis that competition among groups of sexual and asexual siblings favors the maintenance of sexual reproduction in populations. The results showed a substantial fitness advantage for sexual tillers. However, in contrast with the models, the advantage of sex did not increase with increasing numbers of colonists in the patch, there were multiple survivors among colonists, and an advantage was observed even for singly planted tillers. When a truncation-selection scheme was imposed ex post facto on the data, the relative performance of sexual tillers was similar to that predicted by the Bulmer (1980) model, suggesting that sib-competition models fail due to the violation of the assumption of truncation selection. The advantage of sex was not correlated with the presence of other species, total percentage cover, or species diversity, although sites where sex was favored were physically clustered.     

Extreme genetic diversity in asexual grass thrips populations

The continuous generation of genetic variation has been proposed as one of the main factors explaining the maintenance of sexual reproduction in nature. However, populations of asexual individuals may attain high levels of genetic diversity through within‐lineage diversification, replicate transitions to asexuality from sexual ancestors and migration. How these mechanisms affect genetic variation in populations of closely related sexual and asexual taxa can therefore provide insights into the role of genetic diversity for the maintenance of sexual reproduction. Here, we evaluate patterns of intra‐ and interpopulation genetic diversity in sexual and asexual populations of Aptinothrips rufus grass thrips. Asexual A. rufus populations are found throughout the world, whereas sexual populations appear to be confined to few locations in the Mediterranean region. We found that asexual A. rufus populations are characterized by extremely high levels of genetic diversity, both in comparison with their sexual relatives and in comparison with other asexual species. Migration is extensive among asexual populations over large geographic distances, whereas close sexual populations are strongly isolated from each other. The combination of extensive migration with replicate evolution of asexual lineages, and a past demographic expansion in at least one of them, generated high local clone diversities in A. rufus. These high clone diversities in asexual populations may mimic certain benefits conferred by sex via genetic diversity and could help explain the extreme success of asexual A. rufus populations.     

Sexual and asexual reproduction of the holothurian Stichopus chloronotus (Echinodermata): a comparison between La Réunion (Indian Ocean) and east Australia (Pacific Ocean)

Summary

Stichopus chloronotus (Brandt, 1835) is one among nine aspidochirotide holothurian species known to reproduce both sexually by broadcast spawning and asexually by transverse fission. New data on the sexual cycle of this species in La Réunion are presented here and information available on sexual and asexual reproduction in this species is summarised. Sexual reproduction on La Réunion shows a distinct seasonality with a main spawning period in the warm season (November-February). The spawning period the Great Barrier Reef appears to be at the same time. Some intriguing deviations from unity in sex-ratio, usually biased towards more male individuals, have been observed in both geographic regions (sex ratio at La Reunion 31:1). New data on the asexual reproduction of this species in La Réunion confirm the high rates of fission. The peak of asexual reproduction in both the Indian and Pacific Ocean was observed in winter (June-July). Thus, asexual reproduction in this species occurs outside the season for sexual reproduction. The rate of asexual reproduction appears to vary between sample locations. However, results of population genetic studies on S. chloronotus (Uthicke et al., 1999; Uthicke et al., 2001) indicated that in most populations investigated a maximum of about 60% of all individuals may be derived from sexual recruitment. Cluster analyses on genetic distances between populations grouped populations within Oceans together, with the exception of one sample from a nearshore reef of the GBR. Although genetic differences between the two regions exist, these are relatively small regarding the large geographic distance. We conclude that asexual reproduction in S. chloronotus is important to maintain local population sizes, but that larval exchange between populations mediated by sexual reproduction is important for colonisation of new areas and to provide connectivity between populations. Here, we present the first synthesis of these phenomena for a holothurian species.     

Outcomes of reciprocal invasions between genetically diverse and genetically uniform populations of <Emphasis Type="Italic">Daphnia obtusa</Emphasis> (Kurz)

Ecological theory predicts that genetic variation produced by sexual reproduction results in niche diversification and provides a competitive advantage both to facilitate invasion into genetically uniform asexual populations and to withstand invasion by asexual competitors. We tested the hypothesis that a large group of diverse clones of Daphnia obtusa has greater competitive advantage when invading into genetically uniform populations of this species than a smaller group with inherently less genetic diversity. We compared competitive outcomes to those of genetically uniform groups of small and large size invading into genetically diverse populations. Genetically diverse invaders of initially large group size increased their representation by more than those of initially small size; in contrast, genetically uniform invaders of initially large group size diminished on average by more than those of initially small size. These results demonstrate an advantage to the genetic variation produced by sexual reproduction, both in invasion and resisting invasion, which we attribute to competitive release experienced by individuals in genetically diverse populations.     

VARIATION IN THE STRENGTH OF MALE MATE CHOICE ALLOWS LONG‐TERM COEXISTENCE OF SPERM‐DEPENDENT ASEXUALS AND THEIR SEXUAL HOSTS

In several asexual taxa, reproduction requires mating with related sexual species to stimulate egg development, even though genetic material is not incorporated from the sexuals (gynogenesis). In cases in which gynogens do not invest in male function, they can potentially have a twofold competitive advantage over sexuals because the asexuals avoid the cost of producing males. If unmitigated, however, the competitive success of the asexuals would ultimately lead to their own demise, following the extinction of the sexual species that stimulate egg development. We have studied a model of mate choice among sexual individuals and asexual gynogens, where males of the sexual species preferentially mate with sexual females over gynogenetic females, to determine if such mating preferences can stably maintain both gynogenetic and sexual individuals within a community. Our model shows that stable coexistence of gynogens and their sexual hosts can occur when there is variation among males in the degree of preference for mating with sexual females and when pickier males pay a higher cost of preference.     

Thelytokous Parthenogenesis in the Fungus-Gardening Ant Mycocepurus smithii (Hymenoptera: Formicidae)

The general prevalence of sexual reproduction over asexual reproduction among organisms testifies to the evolutionary benefits of recombination, such as accelerated adaptation to changing environments and elimination of deleterious mutations. Documented instances of asexual reproduction in groups otherwise dominated by sexual reproduction challenge evolutionary biologists to understand the special circumstances that might confer an advantage to asexual reproductive strategies. Here we report one such instance of asexual reproduction in the ants. We present evidence for obligate thelytoky in the asexual fungus-gardening ant, Mycocepurus smithii, in which queens produce female offspring from unfertilized eggs, workers are sterile, and males appear to be completely absent. Obligate thelytoky is implicated by reproductive physiology of queens, lack of males, absence of mating behavior, and natural history observations. An obligate thelytoky hypothesis is further supported by the absence of evidence indicating sexual reproduction or genetic recombination across the species'' extensive distribution range (Mexico-Argentina). Potential conflicting evidence for sexual reproduction in this species derives from three Mycocepurus males reported in the literature, previously regarded as possible males of M. smithii. However, we show here that these specimens represent males of the congeneric species M. obsoletus, and not males of M. smithii. Mycocepurus smithii is unique among ants and among eusocial Hymenoptera, in that males seem to be completely absent and only queens (and not workers) produce diploid offspring via thelytoky. Because colonies consisting only of females can be propagated consecutively in the laboratory, M. smithii could be an adequate study organism a) to test hypotheses of the population-genetic advantages and disadvantages of asexual reproduction in a social organism and b) inform kin conflict theory.For a Portuguese translation of the abstract, please see Abstract S1.