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.     

Paternal reproductive success drives sex allocation in a wild mammal

Parents should bias sex allocation toward offspring of the sex most likely to provide higher fitness returns. Trivers and Willard proposed that for polygynous mammals, females should adjust sex‐ratio at conception or bias allocation of resources toward the most profitable sex, according to their own body condition. However, the possibility that mammalian fathers may influence sex allocation has seldom been considered. Here, we show that the probability of having a son increased from 0.31 to 0.60 with sire reproductive success in wild bighorn sheep (Ovis canadensis). Furthermore, our results suggest that females fertilized by relatively unsuccessful sires allocated more energy during lactation to daughters than to sons, while the opposite occurred for females fertilized by successful sires. The pattern of sex‐biased offspring production appears adaptive because paternal reproductive success reduced the fitness of daughters and increased the average annual weaning success of sons, independently of maternal allocation to the offspring. Our results illustrate that sex allocation can be driven by paternal phenotype, with profound influences on the strength of sexual selection and on conflicts of interest between parents.     

Better‐surviving barn swallow mothers produce more and better‐surviving sons

Sex allocation theory predicts that parents are selected to bias their progeny sex ratio (SR) toward the sex that will benefit the most from parental quality. Because parental quality may differentially affect survival of sons and daughters, a pivotal test of the adaptive value of SR adjustment is whether parents overproduce offspring of the sex that accrues larger fitness advantages from high parental quality. However, this crucial test of the long‐term fitness consequences of sex allocation decisions has seldom been performed. In this study of the barn swallow (Hirundo rustica), we showed a positive correlation between the proportion of sons and maternal annual survival. We then experimentally demonstrated that this association did not depend on the differential costs of rearing offspring of either sex. Finally, we showed that maternal lifespan positively predicted lifespan of sons but not of daughters. Because in barn swallows lifespan is a strong determinant of lifetime reproductive success, the results suggest that mothers overproduce offspring of the sex that benefits the most from maternal quality. Hence, irrespective of mechanisms causing the SR bias and mother–son covariation in lifespan, we provide strong evidence that sex allocation decisions of mothers can highly impact on their lifetime fitness.     

PATERNAL CONDITION DRIVES PROGENY SEX‐RATIO BIAS IN A LIZARD THAT LACKS PARENTAL CARE

Sex‐allocation theory predicts that females in good condition should preferentially produce offspring of the sex that benefits the most from an increase in maternal investment. However, it is generally assumed that the condition of the sire has little effect on progeny sex ratio, particularly in species that lack parental care. We used a controlled breeding experiment and molecular paternity analyses to examine the effects of both maternal and paternal condition on progeny sex ratio and progeny fitness in the brown anole (Anolis sagrei), a polygynous lizard that lacks parental care. Contrary to the predictions of sex‐allocation theory, we found no relationship between maternal condition and progeny sex ratio. By contrast, progeny sex ratio shifted dramatically from female‐biased to male‐biased as paternal condition increased. This pattern was driven entirely by an increase in the production of sons as paternal condition improved. Despite strong natural selection favoring large size and high condition in both sons and daughters, we found no evidence that progeny survival was related to paternal condition. Our results emphasize the importance of considering the paternal phenotype in studies of sex allocation and highlight the need for further research into the pathways that link paternal condition to progeny fitness.     

Postcopulatory fertilization bias as a form of cryptic sexual selection

Males and females share most of their genetic material yet often experience very different selection pressures. Some traits that are adaptive when expressed in males may therefore be maladaptive when expressed in females. Recent studies demonstrating negative correlations in fitness between parents and their opposite-sex progeny suggest that natural selection may favor a reduction in trait correlations between the sexes to partially mitigate intralocus sexual conflict. We studied sex-specific forms of selection acting in Anolis lizards in the Greater Antilles, a group for which the importance of natural selection has been well documented in species-level diversification, but for which less is known about sexual selection. Using the brown anole (Anolis sagrei), we measured fitness-related variation in morphology (body size), and variation in two traits reflecting whole animal physiological condition: running endurance and immune function. Correlations between body size and physiological traits were opposite between males and females and the form of natural selection acting on physiological traits significantly differed between the sexes. Moreover, physiological traits in progeny were correlated with the body-size of their sires, but correlations were null or even negative between parents and their opposite-sex progeny. Although results based on phenotypic and genetic correlations, as well as the action of natural selection, suggest the potential for intralocus sexual conflict, females used sire body size as a cue to sort sperm for the production of either sons or daughters. Our results suggest that intralocus sexual conflict may be at least partly resolved through post-copulatory sperm choice in A. sagrei.     

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.     

Offspring sex ratio produced by female guppies in the wild correlates with sexual ornaments of their sons

The attractiveness hypothesis predicts that females produce broods with male-biased sex ratios when they mate with attractive males. This hypothesis presumes that sons in broods with male-biased sex ratios sired by attractive males have high reproductive success, whereas the reproductive success of daughters is relatively constant, regardless of the attractiveness of their sires. However, there is little direct evidence for this assumption. We have examined the relationships between offspring sex ratios and (1) sexual ornamentation of sons and (2) body size of daughters in broods from wild female guppies Poecilia reticulata. Wild pregnant females were collected and allowed to give birth in the laboratory. Body size and sexual ornamentation of offspring were measured at maturity. Our analysis revealed a significant positive correlation between offspring sex ratios (the proportion of sons per brood) and the total length as well as the area of orange spots of sons, two attributes that influence female mating preferences in guppies. The sex ratio was not associated with the body size of daughters. These results suggest that by performing adaptive sex allocation according to the expected reproductive success of sons and daughters, female guppies can enhance the overall fitness of their offspring.     

Parents’ genetic dissimilarity and offspring sex in a polygynous mammal

Offspring quality may benefit from genetic dissimilarity between parents. However, genetic dissimilarity may trade‐off with additive genetic benefits. We hypothesized that when sexual selection produces sex‐specific selective scenarios, the relative benefits of additive genetic vs. dissimilarity may differ for sons and daughters. Here we study a sample of 666 red deer (Cervus elaphus) microsatellite genotypes, including males, females and their foetuses, from 20 wild populations in Spain (the main analyses are based on 241 different foetuses and 190 mother‐foetus pairs). We found that parental lineages were more dissimilar in daughters than in sons. On average, every mother was less related to her mate than to the sample of fathers in the population when producing daughters not sons. Male foetuses conceived early in the rutting season were much more inbred than any other foetuses. These differences maintained through gestation length, ruling out intrauterine mortality as a cause for the results, and indicating that the potential mechanism producing the association between parents’ dissimilarity and offspring sex should operate close to mating or conception time. Our findings highlight the relevance of considering the sex of offspring when studying genetic similarity between parents.     

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.     

Within-clutch variation in offspring sex determined by differences in sire body size: cryptic mate choice in the wild

Sexual selection theory predicts that paternal quality should drive female investment in progeny. We tested whether polyandrous female side-blotched lizards, Uta stansburiana, would adjust within-clutch progeny investment according to sire phenotypes. In two different years, polyandrous females selectively used sperm from larger sires to produce sons and used sperm from smaller sires to produce daughters. This cryptic sperm choice had significant effects on progeny survival to maturity that were consistent with sexually antagonistic effects associated with sire body size. Large sires produced sons with high viability and small sires produced daughters with high viability. These results are consistent with our previous findings that alleles for male body size have different fitness effects in male and female progeny. Breeding experiments in the laboratory indicate that results from the wild are more likely due to female choice than biased sperm production by males. Our results demonstrate highly refined gender-specific female choice for sperm and indicate that sire body size may signal the quality of sons or daughters that a sire will produce.     

Intralocus sexual conflict for fitness: sexually antagonistic alleles for testosterone

Intralocus sexual conflict occurs when a trait encoded by the same genetic locus in the two sexes has different optima in males and females. Such conflict is widespread across taxa, however, the shared phenotypic traits that mediate the conflict are largely unknown. We examined whether the sex hormone, testosterone (T), that controls sexual differentiation, contributes to sexually antagonistic fitness variation in the bank vole, Myodes glareolus. We compared (opposite-sex) sibling reproductive fitness in the bank vole after creating divergent selection lines for T. This study shows that selection for T was differentially associated with son versus daughter reproductive success, causing a negative correlation in fitness between full siblings. Our results demonstrate the presence of intralocus sexual conflict for fitness in this small mammal and that sexually antagonistic selection is acting on T. We also found a negative correlation in fitness between parents and their opposite-sex progeny (e.g. father-daughter), highlighting a dilemma for females, as the indirect genetic benefits of selecting reproductively successful males (high T) are lost with daughters. We discuss mechanisms that may mitigate this disparity between progeny quality.     

Attractive males do not sire superior daughters

Much of the recent work on the evolution of female choice has focused on the relative influence of direct and indirect benefits, and particularly whether direct costs can be offset by indirect benefits. Studies investigating whether attractive males benefit females by increasing the viability of their offspring often report mating advantages to sons consistent with the Fisher process, while detecting no or weak viability benefits. One potential reason for this is that sons may trade-off viability benefits with investment in costly traits that enhance mating success, leading to the suggestion that viability benefits may be better detected by examining daughters’ fitness. Here we investigate the relationship between male attractiveness and daughters’ fitness in Drosophila simulans. We measured daughter (and dam) lifetime reproductive success and longevity. We found no evidence that attractive males sire high fitness daughters. Additionally, neither daughters nor dams gained direct benefits from mating with attractive males. However, aspects of daughters’ fitness were related to dam characters.     

Sex differences in begging vocalizations of nestling barn swallows, Hirundo rustica

Parents of sexually reproducing species should adjust their investment in production of sons and daughters in relation to the relative costs and reproductive value of offspring of either sex. Sex allocation mediated by differential allocation of care such as food provisioning, however, requires that parents can identify offspring sex. We analysed sex differences in offspring begging calls that may serve as a cue for parents to discriminate between sons and daughters. A combination of three sonagraphic variables of begging calls of nestling barn swallows allowed us to classify them according to sex at day 16, but not at day 12 after hatching, suggesting that sex differences in begging calls arise during the nestling period as the time of fledging approaches. Hence, parents may be able to discriminate between sons and daughters by auditory cues, which would enable differential allocation of food between offspring during the late nestling and early fledging stages. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Within‐female plasticity in sex allocation is associated with a behavioural polyphenism in house wrens

Sex allocation theory assumes individual plasticity in maternal strategies, but few studies have investigated within‐individual changes across environments. In house wrens, differences between nests in the degree of hatching synchrony of eggs represent a behavioural polyphenism in females, and its expression varies with seasonal changes in the environment. Between‐nest differences in hatching asynchrony also create different environments for offspring, and sons are more strongly affected than daughters by sibling competition when hatching occurs asynchronously over several days. Here, we examined variation in hatching asynchrony and sex allocation, and its consequences for offspring fitness. The number and condition of fledglings declined seasonally, and the frequency of asynchronous hatching increased. In broods hatched asynchronously, sons, which are over‐represented in the earlier‐laid eggs, were in better condition than daughters, which are over‐represented in the later‐laid eggs. Nonetheless, asynchronous broods were more productive later within seasons. The proportion of sons in asynchronous broods increased seasonally, whereas there was a seasonal increase in the production of daughters by mothers hatching their eggs synchronously, which was characterized by within‐female changes in offspring sex and not by sex‐biased mortality. As adults, sons from asynchronous broods were in better condition and produced more broods of their own than males from synchronous broods, and both males and females from asynchronous broods had higher lifetime reproductive success than those from synchronous broods. In conclusion, hatching patterns are under maternal control, representing distinct strategies for allocating offspring within broods, and are associated with offspring sex ratios and differences in offspring reproductive success.     

Direct benefits of choosing a high‐fitness mate can offset the indirect costs associated with intralocus sexual conflict

Intralocus sexual conflict generates a cost to mate choice: high‐fitness partners transmit genetic variation that confers lower fitness to offspring of the opposite sex. Our earlier work in the fruit fly, Drosophila melanogaster, revealed that these indirect genetic costs were sufficient to reverse potential “good genes” benefits of sexual selection. However, mate choice can also confer direct fitness benefits by inducing larger numbers of progeny. Here, we consider whether direct benefits through enhanced fertility could offset the costs associated with intralocus sexual conflict in D. melanogaster. Using hemiclonal analysis, we found that females mated to high‐fitness males produced 11% more offspring compared to those mated to low‐fitness males, and high‐fitness females produced 34% more offspring than low‐fitness females. These direct benefits more than offset the reduction in offspring fitness caused by intralocus sexual conflict, creating a net fitness benefit for each sex to pairing with a high‐fitness partner. Our findings highlight the need to consider both direct and indirect effects when investigating the fitness impacts of mate choice. Direct fitness benefits may shelter sexually antagonistic alleles from selection, suggesting a novel mechanism for the maintenance of fitness variation.     

Sex ratio variation in mammals

Parents will increase their fitness by varying the sex ratio of their progeny in response to differences in the costs and benefits of producing sons and daughters. Sex differences in energy requirements or viability during early growth, differences in the relative fitness of male and female offspring, and competition or cooperation between siblings or between siblings and parents might all be expected to affect the sex ratio. Although few trends have yet been shown to be consistent, growing numbers of studies have demonstrated significant variation in birth sex ratios in non-human mammals. These are commonly cited as evidence of adaptive manipulation of the sex ratio. However, several different mechanisms may affect the birth sex ratio, and not all of them are likely to be adaptive. Valid evidence that sex ratio trends are adaptive must be based either on the overall distribution of those trends or on cases in which the sex ratio can be shown to vary with the relative fitness of producing sons and daughters. The distribution of observed sex ratio trends does not conform closely to the predictions of any single adaptive theory. Some recent studies, however, indicate that, within species, the sex ratio varies with the costs or benefits of producing male or female offspring.     

Does the differential cost of sons and daughters lead to sex ratio adjustment in great frigatebirds Fregataminor?

Sex allocation theory predicts that if benefits of producing sons and daughters differ and outweigh the costs of sex ratio adjustment, parents should produce more of the offspring that provide them with greater fitness. Potential benefits may be more likely to outweigh costs where sexual size dimorphism and, in birds, single‐egg clutches exist. Great frigatebirds Fregataminor are seabirds in which females are larger than males and clutch size is one egg. In our study population, sexual size dimorphism develops primarily during the period of complete juvenile dependence on parental care, consistent with a higher cost of producing daughters than sons. Over the course of the 1998 breeding season there was a shift from early season prevalence of daughters to late‐season prevalence of sons. Variation in food availability at time of egg laying, as indexed by sea surface temperature (SST), was a strong predictor of offspring sex in 1998. In contrast, SST in 2003 was not a predictor of offspring sex, nor was there a seasonal shift in the hatching sex ratio, despite a seasonal shift in SST. Besides food availability, we tested two additional factors in 2003 that could explain sex ratio adjustment in relation to the cost of reproduction. Offspring sex in 2003 was not related to natural or experimentally induced variation in maternal body condition; pre‐laying food supplements raised the body condition of females at the time of egg laying but did not affect offspring sex or egg mass. In addition, offspring sex was not predicted by the length of maternal telomere restriction fragments (TRFs), an index of age and possibly of reproductive experience. Broad confidence intervals on effect size suggest that undetected effects of maternal condition on offspring sex ratio could easily exist, but confidence intervals were narrower on the non‐significant effects of SST and TRF length on offspring sex ratio. The cause of different seasonal patterns of hatching sex ratio and different SST effects in 1998 and 2003 is unclear.     

Long-term fitness benefits of egg sex modification by the Seychelles warbler

Sex-ratio theory states that if the fitness costs to the parents of producing one offspring's sex relative to the other are higher, parents should discount these costs by producing fewer individuals of the more costly sex. In the co-operatively breeding Seychelles warbler (Acrocephalus sechellensis) mothers adaptively modify the sex of their single egg toward daughters, the helping sex, when living on territories with rich resources where helpers increase parental reproductive success, but toward sons, the dispersing sex, when living on territories where resources are scarce and/or no helping benefits accrue. By modifying offspring sex ratio, parents maximize their inclusive fitness benefits. Pairs in high-quality territories gained significantly more inclusive fitness benefits (through helping and reproducing offspring) from the production of daughters than from sons, and vice versa in low-quality territories (through reproducing offspring). Experimental manipulation of the offspring's sex shows that the consequences of sex allocation are adaptive for parents on high-quality territories. On high-quality territories with female production, breeding pairs raising step-daughters gained significantly higher inclusive benefits (through indirect and direct fitness gains) than by raising step-sons.     

Different optimal offspring sizes for sons versus daughters may favor the evolution of temperature-dependent sex determination in viviparous lizards

Temperature-dependent sex determination (TSD) has evolved independently in at least two lineages of viviparous Australian scincid lizards, but its adaptive significance remains unclear. We studied a montane lizard species (Eulamprus heatwolei) with TSD. Our data suggest that mothers can modify the body sizes of their offspring by selecting specific thermal regimes during pregnancy (mothers with higher and more stable temperatures produced smaller offspring), but cannot influence sons versus daughters differentially in this way. A field mark-recapture study shows that optimal offspring size differs between the sexes: larger body size at birth enhanced the survival of sons but reduced the survival of daughters. Thus, a pregnant female can optimize the fitness of either her sons or her daughters (via yolk allocation and thermoregulation), but cannot simultaneously optimize both. One evolutionary solution to reduce this fitness cost is to modify the sex-determining mechanism so that a single litter consists entirely of either sons or daughters; TSD provides such a mechanism. Previous work has implicated a sex difference in optimal offspring size as a selective force for TSD in turtles. Hence, opposing fitness determinants of sons and daughters may have favored evolutionary transitions from genetic sex determination to TSD in both oviparous turtles and viviparous lizards.     

Facultative sex allocation in snow skink lizards (Niveoscincus microlepidotus)

Mathematical models suggest that reproducing females may benefit by facultatively adjusting their relative investment into sons vs. daughters, in response to population‐wide shifts in operational sex ratio (OSR). Our field studies on viviparous alpine skinks (Niveoscincus microlepidotus) document such a case, whereby among‐ and within‐year shifts in OSR were followed by shifts in sex allocation. When adult males were relatively scarce, females produced male‐biased litters and larger sons than daughters. The reverse was true when adult males were relatively more common. That is, females that were courted and mated by few males produced mainly sons (and these were larger than daughters), whereas females that were courted and mated by many males produced mainly daughters (and these were larger than sons). Maternal body size and condition also covaried with sex allocation, and the shifting pattern of sexual size dimorphism at birth may reflect these correlated effects rather than a discrete component of an evolved sex‐allocation strategy.