Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica)

Parents should differentially invest in sons or daughters depending on the sex‐specific fitness returns from male and female offspring. In species with sexually selected heritable male characters, highly ornamented fathers should overproduce sons, which will be more sexually attractive than sons of less ornamented fathers. Because of genetic correlations between the sexes, females that express traits which are under selection in males should also overproduce sons. However, sex allocation strategies may consist in reaction norms leading to spatiotemporal variation in the association between offspring sex ratio (SR) and parental phenotype. We analysed offspring SR in barn swallows (Hirundo rustica) over 8 years in relation to two sexually dimorphic traits: tail length and melanin‐based ventral plumage coloration. The proportion of sons increased with maternal plumage darkness and paternal tail length, consistently with sexual dimorphism in these traits. The size of the effect of these parental traits on SR was large compared to other studies of offspring SR in birds. Barn swallows thus manipulate offspring SR to overproduce ‘sexy sons’ and potentially to mitigate the costs of intralocus sexually antagonistic selection. Interannual variation in the relationships between offspring SR and parental traits was observed which may suggest phenotypic plasticity in sex allocation and provides a proximate explanation for inconsistent results of studies of sex allocation in relation to sexual ornamentation in birds.     

PATERNAL CARE: DIRECT AND INDIRECT GENETIC EFFECTS OF FATHERS ON OFFSPRING PERFORMANCE

Knowledge of how genetic effects arising from parental care influence the evolution of offspring traits comes almost exclusively from studies of maternal care. However, males provide care in some taxa, and often this care differs from females in quality or quantity. If variation in paternal care is genetically based then, like maternal care and maternal effects, paternal effects may have important consequences for the evolution of offspring traits via indirect genetic effects (IGEs). IGEs and direct–indirect genetic covariances associated with parental care can contribute substantially to total heritability and influence predictions about how traits respond to selection. It is unknown, however, if the magnitude and sign of parental effects arising from fathers are the same as those arising from mothers. We used a reciprocal cross‐fostering experiment to quantify environmental and genetic effects of paternal care on offspring performance in the burying beetle, Nicrophorus vespilloides. We found that IGEs were substantial and direct–indirect genetic covariances were negative. Combined, these patterns led to low total heritabilities for offspring performance traits. Thus, under paternal care, offspring performance traits are unlikely to evolve in response to selection, and variation in these traits will be maintained in the population despite potentially strong selection on these traits. These patterns are similar to those generated by maternal care, indicating that the genetic effects of care on offspring performance are independent of the caregiver's sex.     

The role of maternal and paternal effects in the evolution of parental quality by sexual selection

Genetic models of maternal effects and models of mate choice have focused on the evolutionary effects of variation in parental quality. There have been, however, few attempts to combine these into a single model for the evolution of sexually selected traits. We present a quantitative genetic model that considers how male and female parental quality (together or separately) affect the expression of a sexually selected offspring trait. We allow female choice of males based on this parentally affected trait and examine the evolution of mate choice, parental quality and the indicator trait. Our model reveals a number of consequences of maternal and paternal effects. (1) The force of sexual selection owing to adaptive mate choice can displace parental quality from its natural selection optimum. (2) The force of sexual selection can displace female parental quality from its natural selection optimum even when nonadaptive mate choice occurs (e.g. runaway sexual selection), because females of higher parental quality produce more attractive sons and these sons counterbalance the loss in fitness owing to over-investment in each offspring. (3) Maternal and paternal effects can provide a source of genetic variation for offspring traits, allowing evolution by sexual selection even when those traits do not show direct genetic variation (i.e. are not heritable). (4) The correlation between paternal investment and the offspring trait influenced by the parental effects can result in adaptive mate choice and lead to the elaboration of both female preference and the male sexually selected trait. When parental effects exist, sexual selection can drive the evolution of parental quality when investment increases the attractiveness of offspring, leading to the elaboration of indicator traits and higher than expected levels of parental investment.     

No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in barn swallows

Sex allocation theory predicts that parents should adjust investment in sons and daughters according to relative fitness of differently sexed offspring. In species with female preference for highly ornamented males, one advantage potentially accruing to parents from investing more in sons of the most ornamented males is that male offspring will inherit characters ensuring sexual attractiveness or high-quality genes, if ornaments honestly reveal male genetic quality. Furthermore, in species where extra-pair fertilizations occur, offspring sired by an extra-pair male are expected to more frequently be male than those of the legitimate male if the latter is of lower quality than the extra-pair male. We investigated adjustment of sex ratio of offspring in relation to ornamentation of the extra-pair and the social mate of females by direct manipulation of tails of male barn swallows Hirundo rustica . Molecular sexing of the offspring was performed using the W chromosome-linked avian chromo-helicase-DNA-binding protein (CHD) gene while paternity assessment was conducted by typing of hypervariable microsatellite loci. Extra-pair offspring sex ratio was not affected by ornamentation of their biological fathers relative to the experimental ornamentation of the parental male. Experimental ornamentation of the parental males did not affect the sex ratio of nestlings in their broods. Female barn swallows might be unable to bias offspring sex ratio at hatching according to the quality of the biological father. Alternatively, fitness benefits in terms of sexual attractiveness of sons might be balanced by the cost of compensating for little parental care provided by highly ornamented parental males, if sons are more costly to rear than daughters, or the advantage of producing more daughters, if males with large ornaments contribute differentially more to the viability of daughters than sons.     

Pectoral fins and paternal quality in sticklebacks

Sexual selection through female mate choice exerts a strong selection pressure on males' sexual traits, particularly when direct benefits are involved. In species with male parental care, one would expect sexual selection to favour paternal quality, for instance through selection on morphological structures which promote quality. We experimentally studied the influence of pectoral fins on paternal quality in male three-spined sticklebacks (Gasterosteus aculeatus L.). After reductions of fin area to different degrees, similar-sized males had to perform a complete reproductive cycle in enclosures in the field. The collected data on fanning behaviour and egg development showed that a reduction in pectoral fin size affected paternal quality probably through an increased beat frequency of the pectorals. Thus, pectoral fins can potentially signal paternal quality to choosy females.     

Sex differences in parental care: Gametic investment,sexual selection,and social environment

Male and female parents often provide different type and amount of care to their offspring. Three major drivers have been proposed to explain parental sex roles: (1) differential gametic investment by males and females that precipitates into sex difference in care, (2) different intensity of sexual selection acting on males and females, and (3) biased social environment that facilitates the more common sex to provide more care. Here, we provide the most comprehensive assessment of these hypotheses using detailed parental care data from 792 bird species covering 126 families. We found no evidence for the gametic investment hypothesis: neither gamete sizes nor gamete production by males relative to females was related to sex difference in parental care. However, sexual selection correlated with parental sex roles, because the male share in care relative to female decreased with both extra‐pair paternity and frequency of male polygamy. Parental sex roles were also related to social environment, because male parental care increased with male‐biased adult sex ratios (ASRs). Taken together, our results are consistent with recent theories suggesting that gametic investment is not tied to parental sex roles, and highlight the importance of both sexual selection and ASR in influencing parental sex roles.     

Male mate choice relies on major histocompatibility complex class I in a sex‐role‐reversed pipefish

Mate choice for compatible genes is often based on genes of the major histocompatibility complex (MHC). Although MHC‐based mate choice is commonly observed in female choice, male mate choice remains elusive. In particular, if males have intense paternal care and are thus the choosing sex, male choice for females with dissimilar MHC can be expected. Here, we investigated whether male mate choice relies on MHC class I genes in the sex‐role reversed pipefish Syngnathus typhle. In a mate choice experiment, we determined the relative importance of visual and olfactory cues by manipulating visibility and olfaction. We found that pipefish males chose females that maximize sequence‐based amino acid distance between MHC class I genotypes in the offspring when olfactory cues were present. Under visual cues, large females were chosen, but in the absence of visual cues, the choice pattern was reversed. The use of sex‐role reversed species thus revealed that sexual selection can lead to the evolution of male mate choice for MHC class I genes.     

Sex differences in life history drive evolutionary transitions among maternal,paternal, and bi‐parental care

Evolutionary transitions among maternal, paternal, and bi‐parental care have been common in many animal groups. We use a mathematical model to examine the effect of male and female life‐history characteristics (stage‐specific maturation and mortality) on evolutionary transitions among maternal, paternal, and bi‐parental care. When males and females are relatively similar – that is, when females initially invest relatively little into eggs and both sexes have similar mortality and maturation – transitions among different patterns of care are unlikely to be strongly favored. As males and females become more different, transitions are more likely. If females initially invest heavily into eggs and this reduces their expected future reproductive success, transitions to increased maternal care (paternal → maternal, paternal → bi‐parental, bi‐parental → maternal) are favored. This effect of anisogamy (i.e., the fact that females initially invest more into each individual zygote than males) might help explain the predominance of maternal care in nature and differs from previous work that found no effect of anisogamy on the origin of different sex‐specific patterns of care from an ancestral state of no care. When male mortality is high or male egg maturation rate is low, males have reduced future reproductive potential and transitions to increased paternal care (maternal → paternal, bi‐parental → paternal, maternal → bi‐parental) are favored. Offspring need (i.e., low offspring survival in the absence of care) also plays a role in transitions to paternal care. In general, basic life‐history differences between the sexes can drive evolutionary transitions among different sex‐specific patterns of care. The finding that simple life‐history differences can alone lead to transitions among maternal and paternal care suggests that the effect of inter‐sexual life‐history differences should be considered as a baseline scenario when attempting to understand how other factors (mate availability, sex differences in the costs of competing for mates) influence the evolution of parental care.     

Sexual selection determines parental care patterns in cichlid fishes

Despite a massive research effort, our understanding of why, in most vertebrates, males compete for mates and females care for offspring remains incomplete. Two alternative hypotheses have been proposed to explain the direction of causality between parental care and sexual selection. Traditionally, sexual selection has been explained as a consequence of relative parental investment, where the sex investing less will compete for the sex investing more. However, a more recent model suggests that parental care patterns result from sexual selection acting on one sex favoring mating competition and lower parental investment. Using species-level comparative analyses on Tanganyikan cichlid fishes we tested these alternative hypotheses employing a proxy of sexual selection based on mating system, sexual dichromatism, and dimorphism data. First, while controlling for female reproductive investment, we found that species with intense sexual selection were associated with female-only care whereas species with moderate sexual selection were associated with biparental care. Second, using contingency analyses, we found that, contrary to the traditional view, evolutionary changes in parental care type are dependent on the intensity of sexual selection. Hence, our results support the hypothesis that sexual selection determines parental care patterns in Tanganyikan cichlid fishes.     

Offspring sexual dimorphism and sex-allocation in relation to parental age and paternal ornamentation in the barn swallow

We analysed the morphology of nestling barn swallows (Hirundo rustica) in relation to their sex, and laying and hatching order. In addition, we studied sex-allocation in relation to parentage, parental age and expression of a secondary sexual character of fathers. Molecular sexing was conducted using the sex chromosome-linked avian CHD1 gene. Sex of the offspring was not associated with laying or hatching order. None of nine morphological, serological and immunological variables varied in relation to offspring sex. Sexual dimorphism did not vary in relation to parental age and expression of a paternal secondary sexual character. The proportion of sons declined with brood size. Individual males and females had a similar proportion of sons during consecutive breeding years. The proportion of sons of individual females declined with age, but increased with the expression of a secondary sexual character of their current mate. The generalized lack of variation in sexual dimorphism among nestlings may suggest that barn swallows do not differentially invest in sons vs. daughters. Alternatively, male offspring may require different parental effort compared to their female siblings in order to attain the same morphological state. The lack of variation in offspring sexual dimorphism with paternal ornamentation suggests no adjustment of overall parental effort in relation to reproductive value of the two sexes. However, male-biased sex ratio among offspring of highly ornamented males may represent an adaptive sex-allocation strategy because the expression of male ornaments is heritable and highly ornamented males are at a sexual selection advantage.     

A model for evolution of male parental care and female multiple mating

In most animals, males gain a fitness benefit by mating with many females, whereas the number of progeny per female is unlikely to increase as a function of additional mates. Furthermore, males of internally fertilizing species run the risk of investing in offspring of other males if they provide parental care. Nevertheless, males of many avian species and a minority of mammalian species provide parental care, and females of various species mate with multiple males. I investigate a two-locus genetic model for evolution of male parental care and female multiple mating in which females gain a direct benefit by multiple mating from the paternal care they thereby elicit for their offspring. The model suggests that, first, male parental care can evolve when it strongly enhances offspring survival and the direct costs of female multiple mating (e.g., loss of energy, risk of injury, exposure to infectious diseases) are greater than its indirect benefit (e.g., acquisition of good genes, increased genetic diversity among offspring); second, female multiple mating can evolve when paternal care is important for offspring survival or the indirect benefit of multiple mating is larger than its direct cost; and, finally, male parental care and female multiple mating can co-occur.     

Evolution of male parental care and female multiple mating: game-theoretical and two-locus diploid models

Males gain a fitness benefit by mating with many females, whereas the number of progeny per female does not increase as a function of additional mates. Furthermore, males run the risk of investing in the offspring of other males if they provide parental care. Nevertheless, in various species, males provide parental care, and females mate with multiple males. We investigate a game-theoretical model in which females gain a direct benefit by multiple mating from the paternal care they elicit for their offspring. The parameters that directly favor male parental care, such as small cost of paternal care, have indirect positive effects on the evolution of female multiple mating, while they have negative effects in the opposite case. Both traits are more likely to evolve when the number of matings is smaller. The individual-based model of a diploid two-locus, two-allelic genetic model confirms the result.     

A theoretical study on the evolution of male parental care and female multiple mating: effects of female mate choice and male care bias

Male parental care and female multiple mating are seen in many species in spite of the cost they entail. Moreover, they even coexist in some species though polyandry, by reducing paternity confidence of caregiving males, seems to hinder the evolution of paternal care. Previous studies have investigated the coevolutionary process of paternal care and polyandry under various simplifying assumptions, including random mating and random provision of male care. We extend these models to examine possible effects of female mate choice and male care bias, assuming that (a) monandrous females mate preferentially with caregiving males while polyandrous females compromise their preference in order to mate with multiple males and (b) caregiving males tend to direct their care to offspring of monandrous females. Our models suggest that both the female preference and the male bias always favor caregiving males while they may not always facilitate the evolution of monandry.     

Sex roles and sex ratios in animals

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.     

Morphological and genetic predictors of parental care in the North American barn swallow Hirundo rustica erythrogaster

Sexually dimorphic traits often signal the fitness benefits an individual can provide to potential mates. In species with altricial young, these signals may also predict the level of parental care an individual is expected to provide to shared offspring. In this study, we tested three hypotheses that traditionally relate sexually dimorphic traits to parental care in two populations of North American barn swallows Hirundo rustica erythrogaster. The good parent hypothesis predicts a positive relationship between an individual's ornamentation and his or her care whereas the differential allocation (more care given by individuals when paired to high quality mates) and reproductive compensation (more care given by individuals when paired to low quality mates) hypotheses predict that an individual's level of parental investment is relative to the quality of their mate. Male and female North American barn swallows have colorful ventral feathers and elongated tail streamers, but there is evidence that ventral color, not tail streamer length, predicts measures of seasonal reproductive success. Accounting for the positive correlation between within‐pair feeding rates and other potentially confounding variables in all of our models, we found no support for the good parent hypothesis because in both males and females, traits shown to be under sexual selection did not predict feeding rates in either sex. However, our data reveal that male coloration, and not streamer length, predicted a female's provisioning rate to shared offspring (females fed more when paired with darker individuals) in two separate populations, supporting the differential allocation, but not the reproductive compensation hypothesis. Because genetic traits have also been shown to affect parental investment, we evaluated this variable as well and found that a male's paternity did not have significant effects on either male or female feeding rates. Overall, our results suggest that females do not pair with darker males in order to gain direct benefits in terms of his expected levels of parental care to shared offspring, but do themselves invest greater levels of care when paired to darker males. Further, our results are consistent with previous studies which suggest that ventral feather color, not streamer length, is a target of sexual selection in North American populations of barn swallow because females invested more in their offspring when paired to darker mates.     

Sexual selection when the female directly benefits

Why do females of many species mate with males on the basis of traits apparently detrimental to male survival? The answer may lie in the fact that these male traits are correlated with male condition. We consider the argument that high male condition directly benefits female fecundity and/or viability (e.g. through lower transmission of parasites, improved control of resources, or better paternal care). Using a quantitative genetic model we show how female preferences for male traits that indicate condition can evolve, even if the male traits themselves have deleterious effects on both the male and the female's fecundity. So-called ‘arbitrary preferences’ can spread in this way because male traits subject to sexual selection are often under additional selection to become correlated with condition. At equilibrium the positive effects of male condition on a female's fecundity and the negative effects of the male trait on her fecundity are balanced and the female preference is under stabilizing selection. The male trait will often be correlated with viability, but not with fecundity, even though the preference evolved as a result of differences in male fecundity. The mean fecundity of females is not maximized, and can steadily decline as the male trait and female preference evolve. If the male trait has no direct deleterious effects on female fecundity, as may happen in species with no paternal care, female preferences are under continuous directional selection to increase.     

Male parental care, female reproductive success, and extrapair paternity

Birds differ considerably in the degree of male parental care,and it has been suggested that interspecific variation in extrapairpaternity is determined by the relative importance of benefitsto females from male parental care and good genes from extrapairsires. I estimated the relationship between extrapair paternityand the importance of male parental care for female reproductivesuccess mainly based on male removal studies, using a comparativeapproach. The reduction in female reproductive success causedby the absence of a male mate was positively correlated withthe male contribution to feeding offspring. The frequency ofextrapair paternity was negatively related to the reductionin female reproductive success caused by the absence of a mate.This was also the case when potentially confounding variablessuch as developmental mode of offspring and sexual dichromatismwere considered. A high frequency of extrapair paternity occursparticularly in bird species in which males play a minor rolein offspring provisioning and in which attractive males providerelatively little parental care. Bird species with frequentextrapair paternity thus appear to be those in which direct fitness benefits from male care are small, females can readilycompensate for the absence of male care, and indirect fitnessbenefits from extrapair sires are important.     

Anisogamy selects for male-biased care in self-consistent games with synchronous matings

We reexamine the influential parental investment hypothesis proposed by Trivers for the causal relationship between anisogamy and widespread female-biased parental care. We build self-consistent versions of Maynard Smith's simple evolutionary game between males and females over parental care, and incorporate consequences of anisogamy for gamete production and its trade-off with parental care, and for patterns of mate limitation. As male mating opportunities are limited by females, frequency-dependent selection acts on male strategies. Assuming synchrony of matings in the population, our analytical models find either symmetric sex roles or male-biased care as an evolutionarily stable strategy (ESS), in contrast to Trivers' hypothesis. We simulate evolution in asynchronously mating populations and find that diverse parental roles, including female care, can be ESS depending on the parameters. When caring males can also remate, or when females can increase the clutch size by deserting, there is stronger selection for male-biased care. Hence, we argue that the mating-caring trade-off for males is neither a necessary consequence of anisogamy nor sufficient to select for female-biased care. Instead, the factors excluded from our models—costly competitive traits, sexual selection, and partial parentage—may be necessary for the parental investment hypothesis to work.     

The evolution of parental care in the context of sexual selection: a critical reassessment of parental investment theory

Males and females are often defined by differences in their energetic investment in gametes. In most sexual species, females produce few large ova, whereas males produce many tiny sperm. This difference in initial parental investment is presumed to exert a fundamental influence on sex differences in mating and parental behavior, resulting in a taxonomic bias toward parental care in females and away from parental care in males. In this article, we reexamine the logic of this argument as well as the evolutionarily stable strategy (ESS) theory often used to substantiate it. We show that the classic ESS model, which contrasts parental care with offspring desertion, violates the necessary relationship between mean male and female fitness. When the constraint of equal male and female mean fitness is correctly incorporated into the ESS model, its results are congruent with those of evolutionary genetic theory for the evolution of genes with direct and indirect effects. Male parental care evolves whenever half the magnitude of the indirect effect of paternal care on offspring viability exceeds the direct effect of additional mating success gained by desertion. When the converse is true, desertion invades and spreads. In the absence of a genetic correlation between the sexes, the evolution of paternal care is independent of maternal care. Theories based on sex differences in gametic investment make no such specific predictions. We discuss whether inferences about the evolution of sex differences in parental care can hold if the ESS theory on which they are based contains internal contradictions.     

Potential fitness benefits from mate selection in the Atlantic cod (Gadus morhua)

Little evidence of benefits from female mate choice has been found when males provide no parental care or resources. Yet, good genes models of sexual selection suggest that elaborated male sexual characters are reliable signals of mate quality and that the offspring of males with elaborate sexual ornaments will perform better than those of males with less elaborate ornaments. We used cod (Gadus morhua L.), an externally fertilizing species where males provide nothing but sperm, to examine the potential of optimal mate selection with respect to offspring survival. By applying in vitro fertilizations, we crossed eight females with nine males in all possible combinations and reared each of the 72 sib groups. We found that offspring survival was dependent on which female was mated with which male and that optimal mate selection has the potential to increase mean offspring survival from 31.9 to 55.6% (a 74% increase). However, the size of the male sexual ornaments and sperm quality (i.e. sperm velocity and sperm density) could not predict offspring survival. Thus, even if there may be large fitness benefits of mate selection, we might not yet have identified the male characteristics generating high offspring survival.