An analytical model for a short-term advantage for sex

An analytical treatment is given for a model of Maynard Smith in which a short-term advantage for sex and recombination is provided by the mechanism of sib-competition. Suppose the next generation is formed by the winners of a large number of contests. Suppose a number of parents each contribute M offspring to a given contest, but the offspring of an asexual parent are identical whereas those of a sexual parent are distributed with some variance. If M is large there is a high probability that a sexual offspring will have a high enough fitness to win the contest. Calculations show that values of M around 3 and 4 are generally enough for sexual behaviour to overcome its two-fold disadvantage.     

The role of Haldane's rule in sex allocation

Sex allocation theory predicts that parents should bias their reproductive investments toward the offspring sex generating the greatest fitness return. When females are the heterogametic sex (e.g., ZW in butterflies, some lizards, and birds), production of daughters is associated with an increased risk of offspring inviability due to the expression of paternal, detrimental recessives on the Z chromosome. Thus, daughters should primarily be produced when mating with partners of high genetic quality. When female sand lizards (Lacerta agilis) mate with genetically superior males, exhibiting high MHC Class I polymorphism, offspring sex ratios are biased towards daughters, possibly due to recruitment of more Z-carrying oocytes when females have assessed the genetic quality of their partners. If our study has general applicability across taxa, it predicts taxon-specific sex allocation effects depending on which sex is the heterogametic one.     

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.     

Lethal combat and sex ratio evolution in a parasitoid wasp

Sex allocation theory provides excellent opportunities for testinghow behavior and life histories are adjusted in response toenvironmental variation. One of the most successful areas fromthis respect is Hamilton's local mate competition theory. Aspredicted by theory, a large number of animal species have beenshown to adjust their offspring sex ratios (proportion male)conditionally, laying less female-biased sex ratios as the numberof females that lay eggs on a patch increases. However, recentstudies have shown that this predicted pattern is not followedby 2 parasitoid species in the genus Melittobia, which alwaysproduce extremely female-biased sex ratios. A possible explanationfor this is that males fight fatally and that males producedby the first female to lay eggs on a patch have a competitiveadvantage over later emerging males. This scenario would negatethe advantage of later females producing a less female-biasedsex ratio. Here we examine fatal fighting and sex ratio evolutionin another species, Melittobia acasta. We show that femalesof this species also fail to adjust their offspring sex ratioin response to the number of females laying eggs on a patch.We then show that although earlier emerging males do have anadvantage in winning fights, this advantage 1) can be reducedby an interaction with body size, with larger males more likelyto win fights and 2) only holds for a brief period around thetime at which the younger males emerge from their pupae. Thissuggests that lethal male combat cannot fully explain the lackof sex ratio shift observed in Melittobia species. We discussalternative explanations.     

Empirical evidence for son-killing X chromosomes and the operation of SA-zygotic drive

Background

Diploid organisms have two copies of all genes, but only one is carried by each haploid gamete and diploid offspring. This causes a fundamental genetic conflict over transmission rate between alternative alleles. Single genes, or gene clusters, only rarely code for the complex phenotypes needed to give them a transmission advantage (drive phenotype). However, all genes on a male''s X and Y chromosomes co-segregate, allowing different sex-linked genes to code for different parts of the drive phenotype. Correspondingly, the well-characterized phenomenon of male gametic drive, occurring during haploid gametogenesis, is especially common on sex chromosomes. The new theory of sexually antagonistic zygotic drive of the sex chromosomes (SA-zygotic drive) extends the logic of gametic drive into the diploid phase of the lifecycle, whenever there is competition among siblings or harmful sib-sib mating. The X and Y are predicted to gain a transmission advantage by harming offspring of the sex that does not carry them.

Results

Here we analyzed a mutant X-chromosome in Drosophila simulans that produced an excess of daughters when transmitted from males. We developed a series of tests to differentiate between gametic and SA-zygotic drive, and provide multiple lines of evidence that SA-zygotic drive is responsible for the sex ratio bias. Driving sires produce about 50% more surviving daughters than sons.

Conclusion

Sex-ratio distortion due to genetic conflict has evolved via gametic drive and maternally transmitted endosymbionts. Our data indicate that sex chromosomes can also drive by harming the non-carrier sex of offspring.     

Maintenance of handedness polymorphism in humans: a frequency-dependent selection model

Frequency-dependent selection is an important process in the maintenance of genetic variation in fitness. In humans, it has been proposed that the polymorphism of handedness is maintained by negative frequency-dependent selection, through a strategic advantage of left-handers in fighting interactions. Using simple mathematical models, we explore: (1) whether it is possible to predict the range of left-handedness frequencies observed in human populations by the frequency and the violence of fighting interactions; (2) the consequences of the sex differences in the probability of transmission of hand preference to offspring. We show that a wide range of values of the frequency of left-handers can be obtained with realistic changes of the parameters values. Our models reinforce the idea that negative frequency-dependence may have played a role in maintaining left-handedness in human populations, and provide further support for the importance of fighting interactions in the evolution of hand preference. Moreover, they suggest an explanation for the occurrence of left-handedness among women in this context, namely an indirect selective advantage through their male offspring.     

Sex-ratio optimization with helpers at the nest

In many cooperatively breeding animals, offspring produced earlier in life assist their parents in raising subsequent broods. Such helping behaviour is often confined to offspring of one sex. Sex-allocation theory predicts that parents overproduce offspring of the helping sex, but the expected degree of sex-ratio bias was thought to depend on specific details of female and male life histories, hampering empirical tests of the theory. Here we demonstrate the following two theories. (i) If all parents produce the same sex ratio, the evolutionarily stable sex ratio obeys a very simple rule that is valid for a general class of life histories. The rule predicts that the expected sex-ratio bias depends on the product of only two parameters which are relatively easily measured: the average number of helping offspring per nest and the relative contribution to offspring production per helper. (ii) If the benefit of helping varies between parents, and parents facultatively adjust the sex ratio accordingly, then the population sex ratio is not necessarily biased towards the helping sex. For example, in line with empirical evidence, if helpers are produced under favourable conditions and parents do not adjust their clutch size to the number of helpers, then a surplus of the non-helping sex is expected.     

Female Control of Offspring Sex Ratios Based on Male Attractiveness in the Guppy

The sex allocation hypothesis predicts that females manipulate the offspring sex ratios according to mate attractiveness. Although there is increasing evidence to support this prediction, it is possible that paternal effects may often obscure the relationship between female control of offspring sex ratios and male attractiveness. In the present study, we examined whether females played a primary role in the manipulation their offspring sex ratios based on male attractiveness, in the guppy Poecilia reticulata, a live‐bearing fish. We excluded the paternal effects by controlling the relative sexual attractiveness of the male by presenting them to the females along with a more attractive or less attractive stimulus male. The test male was perceived to be relatively more attractive by females when it was presented along with a less attractive stimulus male, or vice versa. Subsequently, test male was mated in two different roles (relatively more and less attractive) with two females. If females were responsible for offspring sex ratio manipulation, the sex ratio of the brood would be altered on the basis of the relative attractiveness of the test male. On the other hand, if males play a primary role in offspring sex ratio manipulation, the sex ratios would not differ with the relative attractiveness of the test male. We found that females gave birth to more male‐biased broods when they mated with test males in the attractive role than when they mated with males in the less attractive role. This finding suggests that females are responsible for the manipulation of offspring sex ratios based on the attractiveness of their mates.     

Persistence of females that produce only female progeny in lepidoptera

In Lepidoptera females that produce only female progeny, can be found in wild populations of at least 11 species. The genetic variation is passed on to each generation of female offspring. If genetically abnormal females produce more female offspring than normal females do and mating is random, then populations containing these abnormal females will have a biased population sex ratio. Unmated females will increase due to the scarcity of males and so the population as a unit will die out. Several possible biological explanations for the persistence of the genetic variation have been proposed. But experiments and observations have not verified those hypotheses. Simulations of Heuch's model (1978), however, have shown that the variation persists if the population is distributed, in patches and there is dispersal among patches, even when insects disperse at random. Abnormal females tend to persist at both low and high migration rates, but the probability of persistence is higher at high migration rates. It has been suggested that abnormal females in a population are an adaptation, but the results of this investigation show that this explanation, may not be plausible.     

Temporal variation in sex allocation in the mealybug Planococcus citri: adaptation, constraint, or both?

Sex ratio theory has been very successful in predicting under which circumstances parents should bias their investment towards a particular offspring sex. However, most examples of adaptive sex ratio bias come from species with well-defined mating systems and sex determining mechanisms, while in many other groups there is still an on-going debate about the adaptive nature of sex allocation. Here we study the sex allocation in the mealybug Planococcus citri, a species in which it is currently unclear how females adjust their sex ratio, even though experiments have shown support for facultative sex ratio adjustment. Previous work has shown that the sex ratio females produce changes over the oviposition period, with males being overproduced early and late in the laying sequence. Here we investigate this complex pattern further, examining both the robustness of the pattern and possible explanations for it. We first show that this sex allocation behaviour is indeed consistent across lines from three geographical regions. Second, we test whether females produce sons first in order to synchronize reproductive maturation of her offspring, although our data provide little evidence for this adaptive explanation. Finally we test the age at which females are able to mate successfully and show that females are able to mate and store sperm before adult eclosion. Whilst early-male production may still function in promoting protandry in mealybugs, we discuss whether mechanistic constraints limit how female allocate sex across their lifetime.     

Sex slows down the accumulation of deleterious mutations in the homothallic fungus Aspergillus nidulans

Coexistence of sexual and asexual reproduction within the same individual is an intriguing problem, especially when it concerns homothallic haplonts, like the fungus Aspergillus nidulans. In this fungus asexual and sexual offspring have largely identical genotypes. This genetic model organism is an ideal tool to measure possible fitness effects of sex (compared to asex) resulting from causes other than recombination. In this article we show that slightly deleterious mutations accumulate at a lower rate in the sexual pathway than in the asexual pathway. This secondary sex advantage may contribute to the persistence of sexual spores in this fungus. We propose that this advantage results from intra-organismal selection of the fittest gametes or zygotes, which is more stringent in the costly sexual pathway.     

What’s wrong with a little sex?

In many species, most (or all) offspring are produced by sexual means. However, theory suggests that selection should often favour the evolution of species in which a small fraction of offspring are produced sexually, and the rest are produced asexually. Here, we present the analysis of a model that may help to resolve this paradox. We show that, when heterozygote advantage is in force, members of species in which sex is rare will tend to produce poorly adapted offspring when they mate. This problem should be less severe in species where most offspring are produced by sexual means. As a consequence, once the rate of sexual reproduction becomes sufficiently rare, the benefits of sex may vanish, leading to the evolution of obligate asexuality. Substantial benefits of sexual reproduction may tend to accrue only if a large proportion of offspring are produced sexually. We suggest that similar findings are likely in the case of epistatic interactions between loci.     

Reproducing lizards modify sex allocation in response to operational sex ratios

Sex-allocation theory suggests that selection may favour maternal skewing of offspring sex ratios if the fitness return from producing a son differs from that for producing a daughter. The operational sex ratio (OSR) may provide information about this potential fitness differential. Previous studies have reached conflicting conclusions about whether or not OSR influences sex allocation in viviparous lizards. Our experimental trials with oviparous lizards (Amphibolurus muricatus) showed that OSR influenced offspring sex ratios, but in a direction opposite to that predicted by theory: females kept in male-biased enclosures overproduced sons rather than daughters (i.e. overproduced the more abundant sex). This response may enhance fitness if local OSRs predict survival probabilities of offspring of each sex, rather than the intensity of sexual competition.     

Sex-sorted sperm and fertility: an alternative view

Although contemporary methods of physically separating X from Y chromosome-bearing spermatozoa are now very efficient, overall fertility rates following the use of sex-sorted sperm are not as impressive, in spite of many attempts to improve them. At the same time, there are suggestions from evolutionary biology, and from sex allocation theory in particular, that there may need to be a modification to the chance theory of sex determination in mammals. This is because it now appears that the mammalian female could have some influence on the sex of her offspring, and furthermore, that this influence could be preconceptual. If so, this could go some way towards accounting for the putative inefficiencies in fertilization following insemination with sex-sorted sperm.     

Does sex-ratio selection influence nest-site choice in a reptile with temperature-dependent sex determination?

Evolutionary theory predicts that dioecious species should produce a balanced primary sex ratio maintained by frequency-dependent selection. Organisms with environmental sex determination, however, are vulnerable to maladaptive sex ratios, because environmental conditions vary spatio-temporally. For reptiles with temperature-dependent sex determination, nest-site choice is a behavioural maternal effect that could respond to sex-ratio selection, as mothers could adjust offspring sex ratios by choosing nest sites that will have particular thermal properties. This theoretical prediction has generated decades of empirical research, yet convincing evidence that sex-ratio selection is influencing nesting behaviours remains absent. Here, we provide the first experimental evidence from nature that sex-ratio selection, rather than only viability selection, is probably an important component of nest-site choice in a reptile with temperature-dependent sex determination. We compare painted turtle (Chrysemys picta) neonates from maternally selected nest sites with those from randomly selected nest sites, observing no substantive difference in hatching success or survival, but finding a profound difference in offspring sex ratio in the direction expected based on historical records. Additionally, we leverage long-term data to reconstruct our sex ratio results had the experiment been repeated in multiple years. As predicted by theory, our results suggest that sex-ratio selection has shaped nesting behaviour in ways likely to enhance maternal fitness.     

Could maternal testosterone levels govern mammalian sex ratio deviations?

Although maternal dominance and good condition are frequently associated with raised offspring sex ratios in mammals, the key factor may be female testosterone, which not only underpins the behavioural indicators but could also provide a pathway to a possible proximate mechanism for sex determination. By taking into account the fact that female testosterone levels rise in response to environmental stressors, it is possible to re-interpret the findings of atypical sex ratios in mammals in a way that reconciles seemingly conflicting results and reveals instead what could be a coherent, adaptive system of sex allocation in mammals.     

Diversity and the maintenance of sex by parasites

The Red Queen hypothesis (RQH) predicts that parasite‐mediated selection will maintain sexual individuals in the face of competition from asexual lineages. The prediction is that sexual individuals will be difficult targets for coevolving parasites if they give rise to more genetically diverse offspring than asexual lineages. However, increasing host genetic diversity is known to suppress parasite spread, which could provide a short‐term advantage to clonal lineages and lead to the extinction of sex. We test these ideas using a stochastic individual‐based model. We find that if parasites are readily transmissible, then sex is most likely to be maintained when host diversity is high, in agreement with the RQH. If transmission rates are lower, however, we find that sexual populations are most likely to persist for intermediate levels of diversity. Our findings thus highlight the importance of genetic diversity and its impact on epidemiological dynamics for the maintenance of sex by parasites.     

Transgenerational plasticity mitigates the impact of global warming to offspring sex ratios

Global warming poses a threat to organisms with temperature‐dependent sex determination because it can affect operational sex ratios. Using a multigenerational experiment with a marine fish, we provide the first evidence that parents developing from early life at elevated temperatures can adjust their offspring gender through nongenetic and nonbehavioural means. However, this adjustment was not possible when parents reproduced, but did not develop, at elevated temperatures. Complete restoration of the offspring sex ratio occurred when parents developed at 1.5 °C above the present‐day average temperature for one generation. However, only partial improvement in the sex ratio occurred at 3.0 °C above average conditions, even after two generations, suggesting a limitation to transgenerational plasticity when developmental temperature is substantially increased. This study highlights the potential for transgenerational plasticity to ameliorate some impacts of climate change and that development from early life may be essential for expression of transgenerational plasticity in some traits.     

Does time of the season influence filial cannibalism in the sand goby, <Emphasis Type="Italic">Pomatoschistus minutus</Emphasis>?

According to life-history theory, filial cannibalism by fish that breed over one season only should be more beneficial early than late in the season if they eat eggs to invest energy into later clutches. Also, filial cannibalism may be more costly late in the season if finding ripe females for replacing eaten eggs is harder then. On the other hand, offspring hatching early may have a competitive advantage over fry hatching late and hence provide higher fitness to the parent. Using data collected over three successive years, I tested if sand goby males are more prone to eat of their eggs early than late in the reproductive season. I found no difference in the amount of eggs eaten or in the frequency of males eating the whole clutch between early and late in the season. Furthermore, there was no difference in the frequency of males who ate parts of their clutches, early compared to late. This might reflect a trade-off between quality (early hatching offspring) and quantity (producing as many offspring as possible over a long reproductive season). If so, the lack of seasonal pattern of filial cannibalism found in sand gobies might be the result of opposing selection pressures.     

Parasites and mutational load: an experimental test of a pluralistic theory for the evolution of sex

Ecological and mutational explanations for the evolution of sexual reproduction have usually been considered independently. Although many of these explanations have yielded promising theoretical results,experimental support for their ability to overcome a twofold cost of sex has been limited. For this reason, it has recently been argued that a pluralistic approach, combining effects from multiple models, may be necessary to explain the apparent advantage of sex. One such pluralistic model proposes that parasite load and synergistic epistasis between deleterious mutations might interact to create an advantage for recombination.Here, we test this proposal by comparing the fitness functions of parasitized and parasite-free genotypes of Escherichia coli bearing known numbers of transposon-insertion mutations. In both classes, we failed to detect any evidence for synergistic epistasis. However, the average effect of deleterious mutations was greater in parasitized than parasite-free genotypes. This effect might broaden the conditions under which another proposed model combining parasite-host coevolutionary dynamics and mutation accumulation can explain the maintenance of sex. These results suggest that, on average, deleterious mutations act multiplicatively with each other but in synergy with infection in determining fitness.