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).     

Paternal Care by Genetic Fathers and Stepfathers I: Reports from Albuquerque Men

We present a biosocial model of human male parental care that allows male parental allocations to be influenced not only by changes in the fitness (welfare) of the recipient offspring, but also by their effects on the man's relationship with the child's mother. The model recognizes four classes of relationships between males and the children they parent: genetic offspring of current mates (combined relationship and parental effort), genetic offspring of previous mates (parental effort solely), step offspring of current mates (relationship effort solely), and stepchildren of previous mates (essentially no expected investment). We test the model using data on parental investments collected from adult males living in Albuquerque, New Mexico, U.S.A. Four measures of paternal investment are examined: the probability that a child attends college (2,191 offspring), the probability that a child who attends college receives money for it (N = 1,212), current financial expenditures on children (N = 635), and the amount of time per week that men spend with children ages 5 to 12 years (N = 2,589). The tests are consistent with a role for relationship effort in parental care: men invest more in the children of their current mates, even when coresidence with offspring is not a confounder.     

Sexual conflict over parental care promotes the evolution of sex differences in care and the ability to care

Strong asymmetries in parental care, with one sex providing more care than the other, are widespread across the animal kingdom. At present, two factors are thought to ultimately cause sex differences in care: certainty of parentage and sexual selection. By contrast, we here show that the coevolution of care and the ability to care can result in strong asymmetries in both the ability to care and the level of care, even in the absence of these factors. While the coevolution of care and the ability to care does not predict which sex evolves to care more than the other, once other factors give rise to even the slightest differences in the cost and benefits of care between the sexes (e.g. differences in certainty in parentage), a clear directionality emerges; the sex with the lower cost or higher benefit of care evolves both to be more able to care and to provide much higher levels of care than the other sex. Our findings suggest that the coevolution of levels of care and the ability to care may be a key factor underlying the evolution of sex differences in care.     

Fishes as models in studies of sexual selection and parental care

Fishes are by far the most diverse group of vertebrates. This fact is in no way, however, reflected in their use as model organisms for understanding sexual selection or parental care. Why is this so? Is it because fishes are actually poor models? The usefulness of fishes as models for sexual selection and parental care is discussed by emphasizing some problems inherent in fish studies, along with a number of reasons why fishes are indeed excellently suited. The pros and cons of fishes as models are discussed mainly by comparison with birds, the most popular model organisms in animal behaviour. Difficulties include a lack of background knowledge for many species, and the problems of marking and observing fishes in their natural environment. Positive attributes include the diversity of lifestyles among fishes, and the ease with which they can be studied experimentally in the laboratory. How useful fish models can be is briefly illustrated by the impressive and broadly relevant advances derived from studies of guppies Poecilia reticulata and three‐spined sticklebacks Gasterosteus aculeatus . A selection of topics is highlighted where fish studies have either advanced or could greatly enhance, the understanding of processes fundamental to animal reproductive dynamics. Such topics include sex role dynamics, the evolution of female ornamentation and mate choice copying. Finally, a number of potential pitfalls in the future use of fish as models for sexual selection and parental care are discussed. Researchers interested in these issues are recommended to make much more extensive use of fish models, but also to adopt a wider range of models among fishes.     

Predicting the direction of sexual selection

Our current understanding of the operation of sexual selection is predicated on a sex difference in parental investment, which favours one sex becoming limiting and choosy over mates, the other competitive and nonchoosy. This difference is reflected in the operational sex ratio (OSR), the ratio of sexually receptive males to females, considered to be of fundamental importance in predicting the direction of sexual selection. Difficulties in measuring OSR directly have led to the use of the potential reproductive rates (PRR) as a measure of the level of investment in offspring of males and females. Several recent studies have emphasized that other factors, such as variation in mate quality and sex differences in mortality patterns, also influence the direction of sexual selection. However, as yet there has been no attempt to form a comprehensive theory of sex roles. Here we show that neither OSR nor PRR is the most fundamentally important determinant of sex roles, and that they are not interchangeable. Instead, the cost of a single breeding attempt has a strong direct effect on competition and choosiness as well as consistent relationships to both OSR and PRR. Our life history based approach to mate choice also yields simple, testable predictions on lack of choice in either sex and on mutual mate choice.     

Paternal Care by Genetic Fathers and Stepfathers II: Reports by Xhosa High School Students

In this article we present a biosocial model of human male parental care that allows relationship (mating) effort to influence male parental allocations. The model recognizes four classes of relationships between men and the children they parent: genetic offspring of current mates (combined relationship and parental effort), genetic offspring of previous mates (parental effort solely), step offspring of current mates (relationship effort solely), and stepchildren of previous mates (essentially no expected investment). We test the model using data on parental investment collected from 340 Xhosa high school students in Cape Town, South Africa. Six measures of paternal investment are examined: the amount of money men spent on students for school, clothing, and miscellaneous expenditures, respectively, and how often men spent time with children, helped them with their homework, or spoke English with them. The tests provide support for the roles of both parental and relationship effort in influencing parental care: men invest significantly more in their genetic offspring and in the children of their current mates. We also examine several proximate influences on parental care, specifically the age and sex of the child, and the percentage of the child's life the father figure coresided with him or her.     

Persistence of an extreme male-biased adult sex ratio in a natural population of polyandrous bird

In a number of insects, fishes and birds, the conventional sex roles are reversed: males are the main care provider, whereas females focus on matings. The reversal of typical sex roles is an evolutionary puzzle, because it challenges the foundations of sex roles, sexual selection and parental investment theory. Recent theoretical models predict that biased parental care may be a response to biased adult sex ratios (ASRs). However, estimating ASR is challenging in natural populations, because males and females often have different detectabilities. Here, we use demographic modelling with field data from 2101 individuals, including 579 molecularly sexed offspring, to provide evidence that ASR is strongly male biased in a polyandrous bird with male-biased care. The model predicts 6.1 times more adult males than females (ASR=0.860, proportion of males) in the Kentish plover Charadrius alexandrinus. The extreme male bias is consistent between years and concordant with experimental results showing strongly biased mating opportunity towards females. Based on these results, we conjecture that parental sex-role reversal may occur in populations that exhibit extreme male-biased ASR.     

Male age mediates reproductive investment and response to paternity assurance

Theory predicts that male response to reduced paternity will depend on male state and interactions between the sexes. If there is little chance of reproducing again, then males should invest heavily in current offspring, regardless of their share in paternity. We tested this by manipulating male age and paternity assurance in the burying beetle Nicrophorus vespilloides. We found older males invested more in both mating effort and parental effort than younger males. Furthermore, male age, a component of male state, mediated male response to perceived paternity. Older males provided more prenatal care, whereas younger males provided less prenatal care, when perceived paternity was low. Adjustments in male care, however, did not influence selection acting indirectly on parents, through offspring performance. This is because females adjusted their care in response to the age of their partner, providing less care when paired with older males than younger males. As a result offspring, performance did not differ between treatments. Our study shows, for the first time, that a male state variable is an important modifier of paternity–parental care trade-offs and highlights the importance of social interactions between males and females during care in determining male response to perceived paternity.     

Men’s reproductive investment decisions

Using questionnaire data completed by 170 men, we examine variation in paternal investment in relation to the trade-off between mating and parenting. We found that as men’s self-perceived mate value increases, so does their mating effort, and in turn, as mating effort increases, paternal investment decreases. This study also simultaneously examined the influence on parental investment of men’s mating effort, men’s perception of their mates’ fidelity, and their perceived resemblance to their offspring. All predicted investment. The predictors of investment are also tested independently for men who are still in a relationship with the mother of their children and those that are separated from her. Finally we examine how self-perceived mate value affects how men respond to variation in paternity confidence. Men with a self-perceived low mate value were less likely to respond to lowered mate fidelity by reducing their parental investment compared with men with a self-perceived high mate value.     

Stepparental Behavior as Mating Effort in Birds and Other Animals

In many animal species, widowed or divorced parents may remate before young of the prior union are independent. In such circumstances, stepparents may kill their predecessors' offspring, may tolerate them without providing care, or may invest in them more or less as genetic parents do. Rohwer proposed that all three of these responses may be understood as mating tactics, adapted to different social and ecological circumstances. We discuss the selection pressures that would favor each of these alternatives and review relevant evidence on nonhuman stepparenting, especially in birds. Stepparental tolerance and (partial or full) care, which are the predominant human responses, are common in nonhuman animals too, and in many cases there is evidence supporting their interpretation as stepparental mating effort adaptations. In general, however, this interpretation is not as well established for tolerance and care as it is for stepparental infanticide. Because tolerance and care are not distinct modes of behavior peculiar to stepparents, the hypothesis that they are nonadaptive by-products of parental psychology often remains tenable. We discuss the kinds of evidence needed to choose between by-product and stepparental adaptation hypotheses.