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.     

Intralocus sexual conflict,adaptive sex allocation,and the heritability of fitness

Intralocus sexual conflict arises when selection favours alternative fitness optima in males and females. Unresolved conflict can create negative between‐sex genetic correlations for fitness, such that high‐fitness parents produce high‐fitness progeny of their same sex, but low‐fitness progeny of the opposite sex. This cost of sexual conflict could be mitigated if high‐fitness parents bias sex allocation to produce more offspring of their same sex. Previous studies of the brown anole lizard (Anolis sagrei) show that viability selection on body size is sexually antagonistic, favouring large males and smaller females. However, sexual conflict over body size may be partially mitigated by adaptive sex allocation: large males sire more sons than daughters, whereas small males sire more daughters than sons. We explored the evolutionary implications of these phenomena by assessing the additive genetic (co)variance of fitness within and between sexes in a wild population. We measured two components of fitness: viability of adults over the breeding season, and the number of their progeny that survived to sexual maturity, which includes components of parental reproductive success and offspring viability (RS^V). Viability of parents was not correlated with adult viability of their sons or daughters. RS^V was positively correlated between sires and their offspring, but not between dams and their offspring. Neither component of fitness was significantly heritable, and neither exhibited negative between‐sex genetic correlations that would indicate unresolved sexual conflict. Rather, our results are more consistent with predictions regarding adaptive sex allocation in that, as the number of sons produced by a sire increased, the adult viability of his male progeny increased.     

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.     

Effect of paternal age on the birth sex ratio in captive populations of aye‐aye (Daubentonia madagascariensis (Gmelin))

For the management of captive populations of zoo animals, it is important to elucidate factors that affect the offspring birth sex ratio. On the basis of the sex allocation theory, the Trivers–Willard and mate attractive/quality hypotheses predict that maternal and paternal conditions affect offspring birth sex ratios. We examined these predictions for the birth sex ratio of aye‐aye Daubentonia madagascariensis (Gmelin) by analyzing the pedigree information in the International Studbook. We found that the birth sex ratio of the aye‐aye was affected by the paternal age, but not maternal age and other environmental factors (birth year, season, and institution). The younger the sire, the more the offspring sex ratio was biased toward males. These results are useful for the effective population management of captive aye‐aye and illustrated the usefulness of the sex allocation theory in the sex ratio management of zoo animals.     

Sex-specific fitness returns are too weak to select for non-random patterns of sex allocation in a viviparous snake

When environmental conditions exert sex-specific selection on offspring, mothers should benefit from biasing their sex allocation towards the sex with the highest fitness in a given environment. Yet, studies show mixed support for such adaptive strategies in vertebrates, which may be due to mechanistic constraints and/or weak selection on facultative sex allocation. In an attempt to disentangle these alternatives, we quantified sex-specific fitness returns and sex allocation (sex ratio and sex-specific mass at birth) according to maternal factors (body size, age, birth date, and litter size), habitat, and year in a viviparous snake with genotypic sex determination. We used data on 106 litters from 19 years of field survey in two nearby habitats occupied by the meadow viper Vipera ursinii ursinii in south-eastern France. Maternal reproductive investment and habitat quality had no differential effects on the growth and survival of sons and daughters. Sex ratio at birth was balanced despite a slight female-biased mortality before birth. No sexual mass dimorphism between offspring was evident. Sex allocation was almost random apart for a trend towards more male-biased litters as females grew older, which could be explained by an inbreeding avoidance strategy. Thus, a weak selection for facultative sex allocation seems sufficient to explain the almost equal sex allocation in the meadow viper.     

No seasonal sex-ratio shift despite sex-specific fitness returns of hatching date in a lizard with genotypic sex determination

Sex allocation theory predicts that mothers should adjust their sex-specific reproductive investment in relation to the predicted fitness returns from sons versus daughters. Sex allocation theory has proved to be successful in some invertebrate taxa but data on vertebrates often fail to show the predicted shift in sex ratio or sex-specific resource investment. This is likely to be partly explained by simplistic assumptions of vertebrate life-history and mechanistic constraints, but also because the fundamental assumption of sex-specific fitness return on investment is rarely supported by empirical data. In short-lived species, the time of hatching or parturition can have a strong impact on the age and size at maturity. Thus, if selection favors adult sexual-size dimorphism, females can maximize their fitness by adjusting offspring sex over the reproductive season. We show that in mallee dragons, Ctenophorus fordi, date of hatching is positively related to female reproductive output but has little, if any, effect on male reproductive success, suggesting selection for a seasonal shift in offspring sex ratio. We used a combination of field and laboratory data collected over two years to test if female dragons adjust their sex allocation over the season to ensure an adaptive match between time of hatching and offspring sex. Contrary to our predictions, we found no effect of laying date on sex ratio, nor did we find any evidence for within-female between-clutch sex-ratio adjustment. Furthermore, there was no differential resource investment into male and female offspring within or between clutches and sex ratios did not correlate with female condition or any partner traits. Consequently, despite evidence for selection for a seasonal sex-ratio shift, female mallee dragons do not seem to exercise any control over sex determination. The results are discussed in relation to potential constraints on sex-ratio adjustment, alternative selection pressures, and the evolution of temperature-dependent sex determination.     

Spatial dynamics of adaptive sex ratios

According to Fisherian sex allocation theory, parents that can adjust their offspring sex ratio in response to skews in population sex ratio will maximize their fitness over parents lacking this ability. There is good evidence that adaptive sex ratio adjustment occurs in many natural populations, but deviations from theoretical predictions have also been observed. These anomalies may be more apparent than real. When the spatial dimension of sex ratio variation is ignored, then a mismatch between empirical data and theoretical predictions based on panmictic mating is to be expected. We illustrate this with data on human sex ratio variation in 21 preindustrial populations, and with a cellular automaton model built to obey Fisherian sex allocation rules. The results from the model generally match with the data. When information about the ambient sex ratio is limited, then the sex allocation decisions may appear locally maladaptive. In general, the results indicate that Fisher's sex-ratio theory may have greater explanatory power than previously thought.     

Conflict over condition‐dependent sex allocation can lead to mixed sex‐determination systems

Theory suggests that genetic conflicts drive turnovers between sex‐determining mechanisms, yet these studies only apply to cases where sex allocation is independent of environment or condition. Here, we model parent–offspring conflict in the presence of condition‐dependent sex allocation, where the environment has sex‐specific fitness consequences. Additionally, one sex is assumed to be more costly to produce than the other, which leads offspring to favor a sex ratio less biased toward the cheaper sex in comparison to the sex ratio favored by mothers. The scope for parent–offspring conflict depends on the relative frequency of both environments: when one environment is less common than the other, parent–offspring conflict can be reduced or even entirely absent, despite a biased population sex ratio. The model shows that conflict‐driven invasions of condition‐independent sex factors (e.g., sex chromosomes) result either in the loss of condition‐dependent sex allocation, or, interestingly, lead to stable mixtures of condition‐dependent and condition‐independent sex factors. The latter outcome corresponds to empirical observations in which sex chromosomes are present in organisms with environment‐dependent sex determination. Finally, conflict can also favor errors in environmental perception, potentially resulting in the loss of condition‐dependent sex allocation without genetic changes to sex‐determining loci.     

Disentangling the effect of genes, the environment and chance on sex ratio variation in a wild bird population

Sex ratio theory proposes that the equal sex ratio typically observed in birds and mammals is the result of natural selection. However, in species with chromosomal sex determination, the same 1 : 1 sex ratio is expected under random Mendelian segregation. Here, we present an analysis of 14 years of sex ratio data for a population of song sparrows (Melospiza melodia) on Mandarte Island, at the nestling stage and at independence from parental care. We test for the presence of variance in sex ratio over and above the binomial variance expected under Mendelian segregation, and thereby quantify the potential for selection to shape sex ratio. Furthermore, if sex ratio variation is to be shaped by selection, we expect some of this extra-binomial variation to have a genetic basis. Despite ample statistical power, we find no evidence for the existence of either genetic or environmentally induced variation in sex ratio, in the nest or at independence. Instead, the sex ratio variation observed matches that expected under random Mendelian segregation. Using one of the best datasets of its kind, we conclude that female song sparrows do not, and perhaps cannot, adjust the sex of their offspring. We discuss the implications of this finding and make suggestions for future research.     

Lewontin and Kojima Meet Fisher: Linkage in a Symmetric Model of Sex Determination

The effect of linkage and epistasis on the evolution of the sex-ratio is studied in a symmetric two-locus model of autosomal sex determination closely related to the symmetric viability model of R. C. Lewontin and K. Kojima. R. A. Fisher's expectation of an even sex ratio for autosomal sex determination by a single gene governs the dynamics when the loci are tightly linked. However, recombination may preclude optimization of the sex ratio just as occurs in viability selection models. Many of the evolutionary phenomena known for the symmetric viability model also occur here. In addition, we exhibit a series of new phenomena related to the presence of surfaces of even sex ratio.     

Sex ratios in geographically structured populations

In his book on sexual selection (1), Darwin documented evidence that the primary sex ratio (the proportion of males at conception) is about 1/2 in a wide variety of species. Otherwise, he explained, a newly conceived member of the rare sex will, on average, have more offspring than one of the common sex, since each offspring has one mother and one father; thus there is frequency-dependent selection in favour of parents producing the rare sex. Darwin formulated this explanation in the first edition (1871) for monogamous species, but he failed to extend it to polygamous species, and in the second edition (1874) he retracted it completely. It was left to Fisher (2) to develop the theory in the more general form that there should be equal parental expenditure on the two sexes, allowing for the possibility that one sex may cost more to produce than the other. Despite the wide applicability of Fisher's principle, recent work on sex ratio evolution has focused on situations where it breaks down (3). Hamilton (4) first pointed out that Fisher's argument assumes population-wide competition for mates, whereas most natural populations have a geographical population structure in which limited dispersal imposes constraints on mating patterns. What are the consequences for the sex ratio?     

How rapidly can maternal behavior affecting primary sex ratio evolve in a reptile with environmental sex determination?

Theoretical models identify maternal behavior as critical for the maintenance and evolution of sex ratios in organisms with environmental sex determination (ESD). Maternal choice of nest site is generally thought to respond more rapidly to sex ratio selection than environmental sensitivity of offspring sex (threshold temperatures) in reptiles with temperature-dependent sex determination (TSD, a form of ESD). However, knowledge of the evolutionary potential for either of these traits in a field setting is limited. I developed a simulation model using local climate data and observed levels of phenotypic variation for nest-site choice and threshold temperatures in painted turtles (Chrysemys picta) with TSD. Both nest-site choice and threshold temperatures, and hence sex ratios, evolved slowly to simulated climate change scenarios. In contrast to expectations from previous models, nest-site choice evolved more slowly than threshold temperatures because of large climatic effects on nest temperatures and indirect selection on maternally expressed traits. A variant of the model, assuming inheritance of nest-site choice through natal imprinting, demonstrated that natal imprinting inhibited adaptive responses in female nest-site choice to climate change. These results predict that females have relatively low potential to adaptively adjust sex ratios through nest-site choice.     

Males influence maternal effects that promote sexual selection: a quantitative genetic experiment with dung beetles Onthophagus taurus

Recently, doubt has been cast on studies supporting good genes sexual selection by the suggestion that observed genetic benefits for offspring may be confounded by differential maternal allocation. In traditional analyses, observed genetic sire effects on offspring phenotype may result from females allocating more resources to the offspring of attractive males. However, maternal effects such as differential allocation may represent a mechanism promoting genetic sire effects, rather than an alternative to them. Here we report results from an experiment on the horned dung beetle Onthophagus taurus, in which we directly compare genetic sire effects with maternal effects that are dependent on sire phenotype. We found strong evidence that mothers provide more resources to offspring when mated with large-horned males. There were significant heritabilities for both horn length and body size, but when differential maternal effects were controlled, the observed estimates of genetic variance were greatly reduced. Our experiment provides evidence that differential maternal effects may amplify genetic effects on offspring traits that are closely related to fitness. Thus, our results may partly explain the relatively high coefficients of additive genetic variation observed in fitness-related traits and provide empirical support for the theoretical argument that maternal effects can play an important role in evolution.     

No effect of parental quality or extrapair paternity on brood sex ratio in the blue tit (Parus caeruleus)

Sex allocation theory predicts that parents should manipulatebrood sex ratio in order to maximise the combined reproductivevalue of their progeny. Females mating with high quality malesshould, therefore, be expected to produce brood sex ratiosbiased towards sons, as male offspring would receive a relativelygreater advantage from inheritance of their father's characteristicsthan would their female siblings. Furthermore, it has been suggested that sex allocation in chicks fathered through extrapair fertilizations should also be biased towards sons. Contraryto these predictions, we found no evidence that the distributionof sex ratios in a sample of 1483 chicks from 154 broods ofblue tits (Parus caeruleus) deviated significantly from thatof a binomial distribution around an even sex ratio. In addition,we found no significant effect on brood sex ratio of the individualquality of either parent as indicated by their biometrics, feather mite loads, time of breeding, or parental survival. This suggeststhat females in our population were either unable to manipulateoffspring sex allocation or did not do so because selectionpressures were not strong enough to produce a significant shiftaway from random sex allocation. The paternity of 986 chicks from 103 broods was determined using DNA microsatellite typing.Extrapair males sired 115 chicks (11.7%) from 41 broods (39.8%).There was no significant effect of paternity (within-pair versusextrapair) on the sex of individual offspring. We suggest that,in addition to the weakness of selection pressures, the possiblemechanisms responsible for the allocation of sex may not besufficiently accurate to control offspring sex at the levelof the individual egg.     

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

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

The evolution of sex ratios and sex-determining systems

Sex determination is a fundamental process governed by diverse mechanisms. Sex ratio selection is commonly implicated in the evolution of sex-determining systems, although formal models are rare. Here, we argue that, although sex ratio selection can induce shifts in sex determination, genomic conflicts between parents and offspring can explain why single-factor systems (e.g. XY/XX or ZW/ZZ) are common even in species that experience selection for biased sex ratios. Importantly, evolutionary shifts in sex determination do not always result in the biased production of sons and daughters sensu sex ratio theory. Thus, equal sex ratios might be an emergent character of sex-determining systems even when biased sex ratios are favored by selection.     

Evolutionary stable sex ratios with non‐facultative male‐eggs first sex allocation in fig wasps

Sex allocation theory has long generated insights into the nature of natural selection. Classical models have elucidated causal phenomena such as local mate competition and inbreeding on the degree of female bias exhibited by various invertebrates. Typically, these models assume mothers facultatively adjust sex allocation using predictive cues of future offspring mating conditions. Here we relax this assumption by developing a sex allocation model for haplodiploid mothers experiencing local mate competition that lay a fixed number of male eggs first. Female egg number is determined by remaining oviposition sites or remaining eggs of the mother, depending on which is exhausted first. Our model includes parameters for variation in foundress number, patch size, fecundity and offspring mortality that allow us to generate secondary sex ratio predictions based on specific parameterizations for natural populations. Simulations show that: 1) in line with classical models, factors that increase sib‐mating result in mothers laying relatively more female eggs; 2) high offspring mortality leads to relatively more males as fertilization insurance; 3) unlike classical model predictions, sub‐optimal predictions, such as more males than females are possible. In addition, our model provides the first quantitative predictions for the expected number of males and females in a patch where typically only one mother utilizes a given patch. We parameterized the model with data obtained from seven species of southern African fig wasps to predict expected means and variances for numbers of male and female offspring for typical numbers of mothers utilizing a patch. These predictions were compared to secondary sex ratio data from single foundress patches, the most commonly encountered situation for these species. Our predictions matched both the observed number and variance of male and female offspring with a high degree of accuracy suggesting that facultative adjustment is not required to produce evolutionary stable sex ratios.     

Genetic variation of sex allocation in the parasitoid wasp Heterospilus prosopidis

The genetic variation of sex ratio and sex allocation were examined in a series of half-sib analyses on the sex ratio of braconid parasitoid wasp Heterospilus prosopidis populations collected in Hawaii and Arizona. The mean threshold value and the range of the threshold for change in the sex of offspring in response to resource quality (host size) were determined. Estimates of the narrow-sense heritability (h2) of sex ratio at a specific host size ranged from 0.185 to 0.315, and those of the sex changing point (threshold value) ranged from 0.220 to 0.342. The coefficient of variation (CV(A)) of sex ratio was significantly larger than CV(A) of body weight. We discuss factors that maintained the significant additive genetic variation of sex ratio.     

Parental care and adaptive brood sex ratio manipulation in birds

Under many circumstances, it might be adaptive for parents to bias the investment in offspring in relation to sex. Recently developed molecular techniques that allow sex determination of newly hatched offspring have caused a surge in studies of avian sex allocation. Whether females bias the primary brood sex ratio in relation to factors such as environmental and parental quality is debated. Progress is hampered because the mechanisms for primary sex ratio manipulation are unknown. Moreover, publication bias against non-significant results may distort our view of adaptive sex ratio manipulation. Despite this, there is recent experimental evidence for adaptive brood sex ratio manipulation in birds. Parental care is a particularly likely candidate to affect the brood sex ratio because it can have strong direct effects on the fitness of both parents and their offspring. We investigate and make predictions of factors that can be important for adaptive brood sex ratio manipulation under different patterns of parental care. We encourage correlational studies based on sufficiently large datasets to ensure high statistical power, studies identifying and experimentally altering factors with sex-differential fitness effects that may cause brood sex ratio skew, and studies that experimentally manipulate brood sex ratio and investigate fitness effects.     

Maternal nutrition affects reproductive output and sex allocation in a lizard with environmental sex determination

Life-history traits such as offspring size, number and sex ratio are affected by maternal feeding rates in many kinds of animals, but the consequences of variation in maternal diet quality (rather than quantity) are poorly understood. We manipulated dietary quality of reproducing female lizards (Amphibolurus muricatus; Agamidae), a species with temperature-dependent sex determination, to examine strategies of reproductive allocation. Females maintained on a poor-quality diet produced fewer clutches but massively (twofold) larger eggs with lower concentrations of yolk testosterone than did conspecific females given a high-quality diet. Although all eggs were incubated at the same temperature, and yolk steroid hormone levels were not correlated with offspring sex, the nutrient-deprived females produced highly male-biased sex ratios among their offspring. These responses to maternal nutrition generate a link between sex and offspring size, in a direction likely to enhance maternal fitness if large body size enhances reproductive success more in sons than in daughters (as seems plausible, given the mating system of this species). Overall, our results show that sex determination in these animals is more complex, and responsive to a wider range of environmental cues, than that suggested by the classification of 'environmental sex determination'.