A theory of gene-culture coevolution of parental preference and sex ratio in humans

A theory on the evolution of human primary sex ratio is proposed. Effects of parental preference for sons, reflected in birth control based on offspring sex ratio and female biased infanticide, on the evolution of primary sex ratio are analyzed. Both are shown to select for female bias in primary sex ratio. The gene-culture coevolution of female infanticide and primary sex ratio is also studied and it is shown that female infanticide develops more in societies in which the father plays a more important role in the transmission of culture than the mother does.     

Culturally transmitted paternity beliefs and the evolution of human mating behaviour

Recent anthropological findings document how certain lowland South American societies hold beliefs in 'partible paternity', which allow children to have more than one 'biological' father. This contrasts with Western beliefs in 'singular paternity', and biological reality, where children have just one father. Here, mathematical models are used to explore the coevolution of paternity beliefs and the genetic variation underlying human mating behaviour. A gene-culture coevolutionary model found that populations exposed to a range of selection regimes typically converge on one of two simultaneously stable equilibria; one where the population is monogamous and believes in singular paternity, and the other where the population is polygamous and believes in partible paternity. A second agent-based model, with alternative assumptions regarding the formation of mating consortships, broadly replicated this finding in populations with a strongly female-biased sex ratio, consistent with evidence for high adult male mortality in the region. This supports an evolutionary scenario in which ancestral South American populations with differing paternity beliefs were subject to divergent selection on genetically influenced mating behaviour, facilitated by a female-biased sex ratio, leading to the present-day associations of female control, partible paternity and polygamy in some societies, and male control, singular paternity and monogamy in others.     

ASSOCIATION BETWEEN SEX RATIO DISTORTION AND SEXUALLY ANTAGONISTIC FITNESS CONSEQUENCES OF FEMALE CHOICE

Genetic variation can be beneficial to one sex yet harmful when expressed in the other—a condition referred to as sexual antagonism. Because X chromosomes are transmitted from fathers to daughters, and sexually antagonistic fitness variation is predicted to often be X-linked, mates of relatively low-fitness males might produce high-fitness daughters whereas mates of high-fitness males produce low-fitness daughters. Such fitness consequences have been predicted to influence the evolution of female mating biases and the offspring sex ratio. Females might evolve to prefer mates that provide good genes for daughters or might adjust offspring sex ratios in favor of the sex with the highest relative fitness. We test these possibilities in a laboratory-adapted population of Drosophila melanogaster , and find that females preferentially mate with males carrying genes that are deleterious for daughters. Preferred males produce equal numbers of sons and daughters, whereas unpreferred males produce female-biased sex ratios. As a consequence, mean offspring fitness of unpreferred males is higher than offspring fitness of preferred males. This observation has several interesting implications for sexual selection and the maintenance of population genetic variation for fitness.     

Trends in Population Sex Ratios May be Explained by Changes in the Frequencies of Polymorphic Alleles of a Sex Ratio Gene

A test for heritability of the sex ratio in human genealogical data is reported here, with the finding that there is significant heritability of the parental sex ratio by male, but not female offspring. A population genetic model was used to examine the hypothesis that this is the result of an autosomal gene with polymorphic alleles, which affects the sex ratio of offspring through the male reproductive system. The model simulations show that an equilibrium sex ratio may be maintained by frequency dependent selection acting on the heritable variation provided by the gene. It is also shown that increased mortality of pre-reproductive males causes an increase in male births in following generations, which explains why increases in the sex ratio have been seen after wars, also why higher infant and juvenile mortality of males may be the cause of the male-bias typically seen in the human primary sex ratio. It is concluded that various trends seen in population sex ratios are the result of changes in the relative frequencies of the polymorphic alleles of the proposed gene. It is argued that this occurs by common inheritance and that parental resource expenditure per sex of offspring is not a factor in the heritability of sex ratio variation.     

Gene-culture coevolution and the nature of human sociality

Human characteristics are the product of gene-culture coevolution, which is an evolutionary dynamic involving the interaction of genes and culture over long time periods. Gene-culture coevolution is a special case of niche construction. Gene-culture coevolution is responsible for human other-regarding preferences, a taste for fairness, the capacity to empathize and salience of morality and character virtues.     

Sex-ratio conflict between queens and workers in eusocial Hymenoptera: mechanisms, costs, and the evolution of split colony sex ratios

Because workers in the eusocial Hymenoptera are more closely related to sisters than to brothers, theory predicts that natural selection should act on them to bias (change) sex allocation to favor reproductive females over males. However, selection should also act on queens to prevent worker bias. We use a simulation approach to analyze the coevolution of this conflict in colonies with single, once-mated queens. We assume that queens bias the primary (egg) sex ratio and workers bias the secondary (adult) sex ratio, both at some cost to colony productivity. Workers can bias either by eliminating males or by directly increasing female caste determination. Although variation among colonies in kin structure is absent, simulations often result in bimodal (split) colony sex ratios. This occurs because of the evolution of two alternative queen or two alternative worker biasing strategies, one that biases strongly and another that does not bias at all. Alternative strategies evolve because the mechanisms of biasing result in accelerating benefits per unit cost with increasing bias, resulting in greater fitness for strategies that bias more and bias less than the population equilibrium. Strategies biasing more gain from increased biasing efficiency whereas strategies biasing less gain from decreased biasing cost. Our study predicts that whether queens or workers evolve alternative strategies depends upon the mechanisms that workers use to bias the sex ratio, the relative cost of queen and worker biasing, and the rates at which queen and worker strategies evolve. Our study also predicts that population and colony level sex allocation, as well as colony productivity, will differ diagnostically according to whether queens or workers evolve alternative biasing strategies and according to what mechanism workers use to bias sex allocation.     

Sex ratio under the haystack model

This paper investigates the evolution of the sex ratio under an extension of the haystack model of Maynard Smith (1964). At the beginning of each season a stack is colonized by a number of fertilized females, and their offspring breed there for several generations until new haystacks are available for colonization. We intend this as a model for populations which undergo periodical population explosions and crashes. With mating before dispersal, the number of generations in the stack has little effect on the equilibrium sex ratio, but it has a marked effect with mating after dispersal. This model is then used to investigate the evolutionary stability of the mechanism of sex determination found in the wood lemming which leads to a population sex ratio of three females to one male.     

Variable Female Mating Positions and Offspring Sex Ratio in the Spider Pityohyphantes phrygianus (Araneae: Linyphiidae)

Chromosomal sex determination and male heterogamety have been thought to seriously impede direct sex ratio control. However, in Pityohyphantes phrygianus, a solitary sheetweb spider with a skewed sex ratio, earlier experimental studies suggested that there are options for female control of offspring sex ratio, if females change their position during the normal mating sequence. Here we show that under natural conditions there is considerable between-female variation in positions, especially after termination of mating. Computer simulations of the orientation of female inner genitalia suggest that sperm are placed in different storage sites depending on the positions adopted. This means that a specific position after mating might potentially influence offspring sex ratio. The variance in offspring sex ratio among females in earlier experiments was binomially distributed, which leads us to conclude that females control the mean sex ratio but do not exercise direct control of the sex of individual offspring.     

Alternative mating strategies,partial sibmating and split sex ratios in haplodiploid species

It is shown that when females can adjust their offspring sex ratios conditionally to the identity of their mates, i.e. sib or non-sib, split sex ratios are expected. These split sex ratios result from variation in relatedness between females and their daughters. Haplodiploid females' relatedness to their daughters increases as their relatedness to their mates increases. Therefore, sibmated females' optimal progeny sex ratio is more female biased than that of outbred females. Inbreeding depression that can result from complementary sex determination (CSD) is also considered. The genetic load caused by CSD can be so costly to sibmated females that they switch to the production of males only. The evolutionarily stable sex ratios for a sibmating model is found to be of a weak type. These weak equilibria and split sex ratios can lead to high variation about the mean and are an incentive for further studies on sex ratio variation in conjunction with mating behaviour. The occurrence of split sex ratios in haplodiploid taxa is important because it favours the evolution of eusociality. Partial local mating and alternative mating strategies can thus eventually lead to the evolution of eusociality.     

Sex ratio, mating behaviour and Wolbachia infections in a sheetweb spider

The solitary sheetweb spider Pityohyphantes phrygianus has a female-biased primary sex ratio. Earlier studies have indicated that female post-copulatory position may influence the degree of bias, but the adaptive significance of the departure from a Fisherian 1 : 1 sex ratio is not known. In this study we show that there is a significant relationship between abdominal position and offspring sex ratio in undisturbed females. Moreover, female mating behaviour (and thus sex ratio) is correlated with female size, but this relationship may shift from negative to positive depending on the presence of the maternally acquired endosymbiotic bacterium Wolbachia in both sexes. A survey of wild-caught individuals shows that the incidence of Wolbachia infection in natural populations is high. This indicates that Wolbachia may be a significant factor influencing female post-copulatory behaviour and sex ratio in natural populations. We discuss various adaptive reasons for sex-ratio bias and behavioural plasticity in females.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 181–186.     

Sex ratios and the evolution of eusociality in the hymenoptera

The potential role of sex ratio biassing in the evolution of worker behaviour in male-haploid hymenopteran insects is examined using a deterministic genetic model. The model is based on a bivoltine life cycle with annual colonies and it assumes five gene loci, each of them controlling a specific feature of the life cycle (particularly brood sex ratios). The hypothetical gene controlling worker behaviour is assumed to be expressed either in the mothers (parental manipulation models) or in the female offspring (offspring altruism models). The threshold of the worker efficiency required for the worker behaviour to evolve is 0.5 under parental manipulation and 1.0 under offspring altruism when the sex ratios are not skewed. Worker evolution by offspring altruism can evolve more easily if the first workers initially raise mainly female brood. With such a sex ratio bias, the threshold of worker efficiency allowing eusociality to evolve drops below 1.0, even close to 0.8. Worker evolution is also favoured by the elimination of males from the first of the two annually occurring offspring generations. It is concluded that the male-haploid sex determination can, through the control of sex ratios, play a significant role in the evolution of eusociality in hymenopteran insects.     

Sex ratio comparisons between nestlings and dead embryos of the Sparrowhawk Accipiter nisus

Sex ratios that differ from unity have been reported for several bird species, but are poorly understood. Skewed sex ratios may originate at ovulation (primary sex ratio) or arise through differential mortality between the sexes (secondary sex ratio). To estimate the primary sex ratio from nestlings is difficult because in some nests not all the offspring can be sexed. Both when including and excluding such nests, there is a risk of overestimating the proportion of the better-surviving sex. Here we sexed dead Sparrowhawk embryos to determine whether unhatched eggs affect primary sex ratio estimates that are based on nestling data. In nests in which embryo mortality occurred, there was up to a 9% discrepancy in the primary sex ratio estimates based on nestlings alone compared to nestlings and dead embryos together. There was no evidence that these differences were based on sex-specific causes of mortality of embryos.     

Parental investment, sexual selection and sex ratios

Conventional sex roles imply caring females and competitive males. The evolution of sex role divergence is widely attributed to anisogamy initiating a self‐reinforcing process. The initial asymmetry in pre‐mating parental investment (eggs vs. sperm) is assumed to promote even greater divergence in post‐mating parental investment (parental care). But do we really understand the process? Trivers [Sexual Selection and the Descent of Man 1871–1971 (1972), Aldine Press, Chicago] introduced two arguments with a female and male perspective on whether to care for offspring that try to link pre‐mating and post‐mating investment. Here we review their merits and subsequent theoretical developments. The first argument is that females are more committed than males to providing care because they stand to lose a greater initial investment. This, however, commits the ‘Concorde Fallacy’ as optimal decisions should depend on future pay‐offs not past costs. Although the argument can be rephrased in terms of residual reproductive value when past investment affects future pay‐offs, it remains weak. The factors likely to change future pay‐offs seem to work against females providing more care than males. The second argument takes the reasonable premise that anisogamy produces a male‐biased operational sex ratio (OSR) leading to males competing for mates. Male care is then predicted to be less likely to evolve as it consumes resources that could otherwise be used to increase competitiveness. However, given each offspring has precisely two genetic parents (the Fisher condition), a biased OSR generates frequency‐dependent selection, analogous to Fisherian sex ratio selection, that favours increased parental investment by whichever sex faces more intense competition. Sex role divergence is therefore still an evolutionary conundrum. Here we review some possible solutions. Factors that promote conventional sex roles are sexual selection on males (but non‐random variance in male mating success must be high to override the Fisher condition), loss of paternity because of female multiple mating or group spawning and patterns of mortality that generate female‐biased adult sex ratios (ASR). We present an integrative model that shows how these factors interact to generate sex roles. We emphasize the need to distinguish between the ASR and the operational sex ratio (OSR). If mortality is higher when caring than competing this diminishes the likelihood of sex role divergence because this strongly limits the mating success of the earlier deserting sex. We illustrate this in a model where a change in relative mortality rates while caring and competing generates a shift from a mammalian type breeding system (female‐only care, male‐biased OSR and female‐biased ASR) to an avian type system (biparental care and a male‐biased OSR and ASR).     

Evolution of eusocial behavior: Offspring choice or parental parasitism?

Assuming the subsocial route towards eusociality, I show that selection favors worker habits (under haplodiploidy) provided the mutant workers are able to bias the sex ratio towards sisters and/or selectively substitute their sons for brothers. If the original workers are not able to do this, selection does not favor the habit. However, under these conditions, selection is indifferent as to whether an individual rears offspring or sibs. This makes it easy for a mother to enlist her daughter's services in rearing other offspring, since the daughter cannot evolve to stop the parental parisitism. These results deal with the origin of eusocial behavior. I also look at selection acting on genes (to invest in offspring rather than sibs) in existing eusocial societies. It is shown that selection for laying workers is very strong, even if such workers give up rearing a seemingly advantageous combination of brothers and sisters. This poses distinct problems for the maintenance of eusocial societies.     

Non-pollinating wasps distort the sex ratio of pollinating fig wasps

In fig wasps, mating occurs among the offspring of one or a few foundress mothers within the fig, from which the mated females disperse to found new broods. Under these conditions, males will compete with each other for mating, and such local mate competition can result in female-biased sex ratios. In addition to pollinating wasps, non-pollinating wasp species are also associated with figs and develop in flower ovaries or parasitize the larvae of primary galling wasps. While studying the fig wasp Pegoscapus tonduzi , which pollinates Ficus citrifolia in Brazil, we examined the influence of non-pollinating fig wasps on the sex ratio of species that pollinate F. citrifolia to determine whether the presence of non-pollinating wasps resulted in a distorted sex ratio. There was a positive relationship between the sex ratio of P. tonduzi and the number of non-pollinating wasps that was independent of the number of foundresses and brood size. In addition, the number of non-pollinating wasps correlated negatively with the number of pollinating females, but was not significantly related to the number of pollinating males. This finding suggested that non-pollinating wasps had a direct effect in distorting the sex ratio of P. tonduzi broods. Our results indicate that the secondary sex ratio may not precisely reflect the primary sex ratio when there is a high infestation of non-pollinating fig wasps.     

Local Mate Competition and Sex Ratio in the Diploid Worm Dinophilus

Summary

The marine archiannelid worm Dinophilus gyrociliatus has a mating system characterized by mostly sib mating; such a system is termed “local mate competition” (LMC) by sex ratio theorists and is known to favor the evolution of highly female biased sex ratios. Dinophilus shows such sex ratios.     

Speciation and Sexual Conflict

We review mathematical models that explicitly consider the dynamics of evolutionary change driven by sexual conflict over mating rate when males are selected for increasing mating success whereas females are selected to restrict mating rate. These models focus on a pair of traits each of which is controlled by a separate set of genes expressed in one sex only. The traits control the probability of mating and/or fertilization. Overall, there are at least six different dynamic regimes observed in models of sexual conflict: (1) continuous coevolutionary chase between the sexes (which can result in allopatric speciation as a byproduct), (2) evolution towards an equilibrium, (3) cyclic evolution, (4) evolution towards a line of equilibria with subsequent random drift along this line, (5) Buridan’s Ass regime involving extensive diversification in female alleles without comparable diversification in male alleles, and (6) extensive diversification in both male and female alleles (which can result in sympatric speciation). Mathematical models also show that different dynamic regimes can be observed with the same set of parameter values but under different initial conditions. It is also possible that the same population switches from one regime to another as a result of stochastic perturbations due to, say, random genetic drift. Moreover, different sets of loci controlling mating and fertilization in the same species can follow different dynamic regimes. We attempt to make some generalizations and identify important directions for theoretical and empirical work.     

Female resistance to sexual coercion can evolve to preserve the indirect benefits of mate choice

Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization per se). Although we might hypothesize that females can evolve resistance in order to retain the indirect, genetic benefits (reflected in offspring attractiveness) of mating with attractive males, up to now it has been difficult to evaluate potential underlying mechanisms. Traditional theoretical approaches do not usually conceptually distinguish between female preference for male mating display and female resistance to forced fertilization, yet sexual conflict over indirect benefits implies the simultaneous action of all of these traits. Here, we present an integrative theoretical framework that draws together concepts from both sexual selection and sexual conflict traditions, allowing for the simultaneous coevolution of displays and preferences, and of coercion and resistance. We demonstrate that it is possible for resistance to coercion to evolve in the absence of direct costs of mating to preserve the indirect benefits of mate choice. We find that resistance traits that improve the efficacy of female mating preference can evolve as long as females are able to attain some indirect benefits of mating with attractive males, even when both attractive and unattractive males can coerce. These results reveal new evolutionary outcomes that were not predicted by prior theories of indirect benefits or sexual conflict.     

Antagonistic Coevolution and Sex

One of the leading hypotheses for the maintenance of sexual reproduction is the Red Queen hypothesis. The underlying premise of the Red Queen hypothesis is that parasites rapidly evolve to infect common host genotypes. This response by parasites could result in the long-term maintenance of genetic variation and may favor sexual reproduction over asexual reproduction. The underlying ideas present a wonderful microcosm for teaching evolution. Here I present the reasons for why sex is anomalous for evolutionary theory, the rationale underlying the Red Queen hypothesis, and some empirical studies of the Red Queen hypothesis using a freshwater snail. The empirical results are consistent with the Red Queen hypothesis. In addition, the distribution of sexual and asexual reproduction in the snail leads naturally to thinking about coevolution in a geographic mosaic of parasite-mediated natural selection.     

Sex ratio bias in the dung beetle <Emphasis Type="Italic">Onthophagus taurus</Emphasis>: adaptive allocation or sex-specific offspring mortality?

Sex allocation theory predicts that females should adjust the sex of their offspring when the fitness returns of one sex are higher than the other. However, biased sex ratios may also arise if mortality differs between the sexes. Here, we examine whether offspring sex ratio bias in the dung beetle, Onthophagus taurus, represents adaptive sex allocation by females or is due to sex-specific mortality. First, we re-analyze an existing data set to show that females produce an excess of daughters when mating to smaller, less attractive males and near equal sex ratio with large, more attractive males. We show, that this results from females adjusting larval provisions after mating to males of variable attractiveness which in turn influences the likelihood that sons die during development. Second, we conduct a manipulative experiment varying the quantity and quality of larval provisions and show that the mortality of sons increased when larval provisions were reduced. Collectively, our work demonstrates that offspring mortality is contingent on the amount of resources provisioned by females and that sons have greater nutritional demands than daughters during development, leading to higher mortality. Our results therefore demonstrate the importance of considering sex-specific offspring mortality in studies of sex ratio evolution.