Local resource competition and local resource enhancement shape primate birth sex ratios

Sex ratio theory provides a powerful source of testable predictions about sex allocation strategies. Although studies of invertebrates generally support predictions derived from the sex ratio theory, evidence for adaptive sex ratio biasing in vertebrates remains contentious. This may be due to the fact that most studies of vertebrates have focused on facultative adjustment in relation to maternal condition, rather than processes that might produce uniform sex biases across individuals. Here, we examine the effects of local resource enhancement (LRE) and local resource competition (LRC) on birth sex ratios (BSRs). We also examine the effects of sex differences in the costs of rearing male and female offspring on BSRs. We present data from 102 primate species and show that BSRs are skewed in favour of the dispersing sex in species that do not breed cooperatively, as predicted by the LRC model. In accordance with the LRE model, BSRs are generally skewed in favour of the more beneficial sex in cooperatively breeding primate species. There is no evidence that BSRs reflect the extent of sexual size dimorphism, an indirect measure of the costs of rearing male and female offspring. These analyses suggest that adaptive processes may play an important role in the evolution of BSRs in vertebrates.     

Sex choice in plants: facultative adjustment of the sex ratio in the perennial herb Begonia gracilis

Sex allocation theory predicts that reproducing individuals will increase their fitness by facultatively adjusting their relative investment towards the rarer sex in response to population shifts in operational sex ratio (OSR). The evolution of facultative manipulation of sex ratio depends on the ability of the parents to track the conditions favouring skewed sex allocation and on the mechanism controlling sex allocation. In animals, which have well-developed sensorial mechanisms, facultative adjustment of sex ratios has been demonstrated on many occasions. In this paper, we show that plants have mechanisms that allow them to evaluate the population OSR. We simulated three different conditions of population OSR by manipulating the amount of pollen received by the female flowers of a monoecious herb, and examined the effect of this treatment on the allocation to male vs. female flowers. A shortage of pollen on the stigmas resulted in a more male-skewed sex allocation, whereas plants that experienced a relatively pollen rich environment tended to produce a more female-skewed sex allocation pattern. Our results for Begonia gracilis demonstrate that the individuals of this species are able to respond to the levels of pollination intensity experienced by their female flowers and adjust their patterns of sex allocation in accordance to the expectations of sex allocation theory.     

Long-lasting fitness consequences of prenatal sex ratio in a viviparous lizard

Maternal effects and early environmental conditions are important in shaping offspring developmental trajectories. For example, in laboratory mammals, the sex ratio during gestation has been shown to influence fitness-related traits via hormonal interaction between fetuses. Such effects have the potential to shape, or constrain, many important aspects of the organism's life, but their generality and importance in natural populations remain unknown. Using long-term data in a viviparous lizard, Lacerta vivipara, we investigated the relationship between prenatal sex ratio and offspring growth, survival, and reproductive traits as adults. Our results show that females from male-biased clutches grow faster, mature earlier, but have lower fecundity than females from female-biased clutches. Furthermore, male reproduction was also affected by the sex ratio during embryonic development, with males from male-biased clutches being more likely to successfully reproduce at age one than males from female-biased clutches. Thus, the sex ratio experienced during gestation can have profound and long-lasting effects on fitness in natural populations of viviparous animals, with important implications for life-history evolution and sex allocation.     

Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird

When fitness benefits of investment in sons and daughters differ,animals are predicted to manipulate the sex ratio of their offspring.Sex ratio manipulation occurs in many taxa, but the mechanismsunderlying the phenomenon in vertebrates remain largely unknown.Factors favoring skewed sex ratios, such as reduced maternalcondition or food availability, also induce elevated corticosteroids.Recent experimental studies support a causal relationship betweencorticosteroids and sex ratio. Evidence of a natural correlationbetween maternal corticosteroids and offspring sex ratio hasbeen lacking, however. Without such evidence, the importanceof corticosteroids in influencing sex ratios in natural populationswas unknown. We measured baseline corticosteroids in 19 free-rangingfemale white-crowned sparrows (Zonotrichia leucophrys) and thesex ratios of their offspring. Females with high corticosteroidsproduced more daughters than females with low hormone levels.We then conducted a controlled, field-based experiment investigatingthe effects of moderately increased maternal corticosteroidson offspring sex ratios to determine if the observed correlationreflects a causal relationship between maternal corticosteroidsand offspring sex ratio. Hormone-implanted females producedmore female embryos than control females. These findings providethe first evidence of a natural correlation between maternalcorticosteroids and offspring sex ratios in free-ranging birds,and the first experimental evidence of a causal link betweenmoderate increases in corticosteroids and biased primary sexratios.     

Sources of stochasticity in models of sex allocation in spatially structured populations

There are many ways to include stochastic effects in models of sex allocation evolution. These include variability in the number of mating partners and fecundity in a rich literature that goes back 20 years. The effects of variance in the fecundity and number of mating partners have typically been considered separately from the stochastic effects of mortality. However, I show that these processes produce mathematically equivalent models with subtly different biological details. These scenarios differ in the way that information becomes available to individuals because the parents often have information on mating partners while they are making sex allocation decisions, but must make these decisions before brood mortality takes place. This makes it possible to test which mechanism, stochastic mortality or variation in mating partners, is responsible for observed sex ratios. Alternatively, asymmetric variance between sexual functions can cause skewed sex allocation, even in the absence of local mate competition. This allows the evolution of either female- or male-biased sex ratios depending on which sexual function is more variable.     

Sex ratio evolution under probabilistic sex determination

Sex allocation theory has been remarkably successful at explaining the prevalence of even sex ratios in natural populations and at identifying specific conditions that can result in biased sex ratios. Much of this theory focuses on parental sex determination (SD) strategies. Here, we consider instead the evolutionary causes and consequences of mixed offspring SD strategies, in which the genotype of an individual determines not its sex, but the probability of developing one of multiple sexes. We find that alleles specifying mixed offspring SD strategies can generally outcompete alleles that specify pure strategies, but generate constraints that may prevent a population from reaching an even sex ratio. We use our model to analyze sex ratios in natural populations of Tetrahymena thermophila, a ciliate with seven sexes determined by mixed SD alleles. We show that probabilistic SD is sufficient to account for the occurrence of skewed sex ratios in natural populations of T. thermophila, provided that their effective population sizes are small. Our results highlight the importance of genetic drift in sex ratio evolution and suggest that mixed offspring SD strategies should be more common than currently thought.     

Reproducing lizards modify sex allocation in response to operational sex ratios

Sex-allocation theory suggests that selection may favour maternal skewing of offspring sex ratios if the fitness return from producing a son differs from that for producing a daughter. The operational sex ratio (OSR) may provide information about this potential fitness differential. Previous studies have reached conflicting conclusions about whether or not OSR influences sex allocation in viviparous lizards. Our experimental trials with oviparous lizards (Amphibolurus muricatus) showed that OSR influenced offspring sex ratios, but in a direction opposite to that predicted by theory: females kept in male-biased enclosures overproduced sons rather than daughters (i.e. overproduced the more abundant sex). This response may enhance fitness if local OSRs predict survival probabilities of offspring of each sex, rather than the intensity of sexual competition.     

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.     

Sex-ratio distortion driven by migration loads

The significance of migration load in driving the evolution of recipient populations has long been documented in population genetics, but its effects have not been linked to the formation of biased sex ratios in natural populations. In this study, we develop a single-locus model to demonstrate how the migration load can shape the primary and secondary sex ratios in dioecious plants where sexual dimorphism is determined by the sex chromosomes (the XX-XY or similar systems). Our results show that migration load can generate an array of sex ratios (from the female- to male-biased primary/secondary sex ratios), depending on the selection systems at the gametophyte and sporophyte stages and on the sex ratio in the migrating seeds. Ovule abortion and the purging of maladaptive genes from the immigrating pollen at the gametophyte stage can alter the primary sex ratio and indirectly alter the secondary sex ratio. The presence of maladaptive sex-linked genes from the migrating pollen and seeds of males facilitates the outcome of the female-biased secondary sex ratios, while the presence of maladaptive sex-linked genes from the migrating seeds of females can lead to the male-biased secondary sex ratios. The detrimental effects of the Y-chromosome from the migrating pollen and seeds can enhance the formation of female-biased primary and secondary sex ratios. These theoretical predictions highlight an alternative approach to the existing sex-ratio theories for interpreting the formation of biased sex ratios in the populations that are subject to the impacts of maladaptive genes from immigrants.     

Influence of male mating history on female reproductive success among monandrous Naryciinae (Lepidoptera: Psychidae)

1. Multiple male copulations can have detrimental effects on female fitness due to sperm limitation. 2. Monandrous Naryciinae females are immobile while the males are short‐lived and do not feed. Multiple male mating is therefore expected to lead to sperm limitation in females. Sperm limitation and male limitation are hypothesised as causes of the repeated evolution of parthenogenetic reproduction in the Psychidae. 3. In this study, the effects of multiple male mating on female reproduction are investigated in several species of Naryciinae by allowing males multiple copulations. The results for two species, Siederia listerella and Dahlica lichenella, are compared. The sex ratios of 53 natural populations are examined for indications of male limitation. 4. Previous copulations by the male increased the female's risk of remaining unfertilised. However, contrary to expectations, those unfertilised females were capable of successful re‐mating. 5. In S. listerella, the number of previous copulations of males negatively influenced female fitness. Females produced 30% fewer offspring if they mated with a previously mated male. In D. lichenella, the older the male and the lower its number of total lifetime copulations, the higher the female's reproductive success. 6. Only a fraction of the investigated populations had a female‐skewed sex ratio, but differences in development time between males and females could lead to reproductive asynchrony. 7. In conclusion, male mating history did not lead to strong sperm limitation in Naryciinae as had been suggested by their life history.     

Population properties affect inbreeding avoidance in moose

Mechanisms reducing inbreeding are thought to have evolved owing to fitness costs of breeding with close relatives. In small and isolated populations, or populations with skewed age- or sex distributions, mate choice becomes limited, and inbreeding avoidance mechanisms ineffective. We used a unique individual-based dataset on moose from a small island in Norway to assess whether inbreeding avoidance was related to population structure and size, expecting inbreeding avoidance to be greater in years with larger populations and even adult sex ratios. The probability that a potential mating event was realized was negatively related to the inbreeding coefficient of the potential offspring, with a stronger relationship in years with a higher proportion or number of males in the population. Thus, adult sex ratio and population size affect the degree of inbreeding avoidance. Consequently, conservation managers should aim for sex ratios that facilitate inbreeding avoidance, especially in small and isolated populations.     

Review. Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds

Differences in relative fitness of male and female offspring across ecological and social environments should favour the evolution of sex-determining mechanisms that enable adjustment of brood sex ratio to the context of breeding. Despite the expectation that genetic sex determination should not produce consistent bias in primary sex ratios, extensive and adaptive modifications of offspring sex ratio in relation to social and physiological conditions during reproduction are often documented. Such discordance emphasizes the need for empirical investigation of the proximate mechanisms for modifying primary sex ratios, and suggests epigenetic effects on sex-determining mechanisms as the most likely candidates. Birds, in particular, are thought to have an unusually direct opportunity to modify offspring sex ratio because avian females are heterogametic and because the sex-determining division in avian meiosis occurs prior to ovulation and fertilization. However, despite evidence of strong epigenetic effects on sex determination in pre-ovulatory avian oocytes, the mechanisms behind such effects remain elusive. Our review of molecular and cytological mechanisms of avian meiosis uncovers a multitude of potential targets for selection on biased segregation of sex chromosomes, which may reflect the diversity of mechanisms and levels on which such selection operates in birds. Our findings indicate that pronounced differences between sex chromosomes in size, shape, size of protein bodies, alignment at the meiotic plate, microtubule attachment and epigenetic markings should commonly produce biased segregation of sex chromosomes as the default state, with secondary evolution of compensatory mechanisms necessary to maintain unbiased meiosis. We suggest that it is the epigenetic effects that modify such compensatory mechanisms that enable context-dependent and precise adjustment of primary sex ratio in birds. Furthermore, we highlight the features of avian meiosis that can be influenced by maternal hormones in response to environmental stimuli and may account for the precise and adaptive patterns of offspring sex ratio adjustment observed in some species.     

Sex investment ratios in eusocial Hymenoptera support inclusive fitness theory

Inclusive fitness theory predicts that sex investment ratios in eusocial Hymenoptera are a function of the relatedness asymmetry (relative relatedness to females and males) of the individuals controlling sex allocation. In monogynous ants (with one queen per colony), assuming worker control, the theory therefore predicts female‐biased sex investment ratios, as found in natural populations. Recently, E.O. Wilson and M.A. Nowak criticized this explanation and presented an alternative hypothesis. The Wilson–Nowak sex ratio hypothesis proposes that, in monogynous ants, there is selection for a 1 : 1 numerical sex ratio to avoid males remaining unmated, which, given queens exceed males in size, results in a female‐biased sex investment ratio. The hypothesis also asserts that, contrary to inclusive fitness theory, queens not workers control sex allocation and queen–worker conflict over sex allocation is absent. Here, I argue that the Wilson–Nowak sex ratio hypothesis is flawed because it contradicts Fisher's sex ratio theory, which shows that selection on sex ratio does not maximize the number of mated offspring and that the sex ratio proposed by the hypothesis is not an equilibrium for the queen. In addition, the hypothesis is not supported by empirical evidence, as it fails to explain ‘split’ (bimodal) sex ratios or data showing queen and worker control and ongoing queen–worker conflict. By contrast, these phenomena match predictions of inclusive fitness theory. Hence, the Wilson–Nowak sex ratio hypothesis fails both as an alternative hypothesis for sex investment ratios in eusocial Hymenoptera and as a critique of inclusive fitness theory.     

Sex ratio evolution when fitness and dispersal vary

In a heterogeneous environment, when the fitness of males and females are differently influenced by habitat quality, habitat-dependent sex ratios may evolve to favor the production of the sex that benefits more (or loses less) from the local habitat. Similarly, sex-biased dispersal favors the evolution of habitat-dependent sex ratios. The present study documents the convergence stable sex ratios expected in the presence of sex-specific fitness gains when dispersal is partial, sex-biased or costly, using a simple model with patches of two qualities. Results show that partial dispersal reduces the sex ratio bias expected with sex-specific fitness gains. The direction of the sex ratio bias can be reversed by sex-biased dispersal or the existence of sex-specific dispersal costs, provided that fitness gains for the two sexes are not too different. The reversal of the sex ratio bias is more readily observed when sex-specific dispersal rates are opposite and extreme. Both dispersal and fitness gains, especially when they are sex-specific, should thus be considered when making predictions about sex ratio evolution in a heterogeneous environment.     

Effects of spontaneous mutation accumulation on sex ratio traits in a parasitoid wasp

Sex allocation theory has proved extremely successful at predicting when individuals should adjust the sex of their offspring in response to environmental conditions. However, we know rather little about the underlying genetics of sex ratio or how genetic architecture might constrain adaptive sex-ratio behavior. We examined how mutation influenced genetic variation in the sex ratios produced by the parasitoid wasp Nasonia vitripennis. In a mutation accumulation experiment, we determined the mutability of sex ratio, and compared this with the amount of genetic variation observed in natural populations. We found that the mutability (h(2)(m)) ranges from 0.001 to 0.002, similar to estimates for life-history traits in other organisms. These estimates suggest one mutation every 5-60 generations, which shift the sex ratio by approximately 0.01 (proportion males). In this and other studies, the genetic variation in N. vitripennis sex ratio ranged from 0.02 to 0.17 (broad-sense heritability, H(2)). If sex ratio is maintained by mutation-selection balance, a higher genetic variance would be expected given our mutational parameters. Instead, the observed genetic variance perhaps suggests additional selection against sex-ratio mutations with deleterious effects on other fitness traits as well as sex ratio (i.e., pleiotropy), as has been argued to be the case more generally.     

Evolution of gametocyte sex ratios in malaria and related apicomplexan (protozoan) parasites

'Survival of the fittest' is usually interpreted to mean that natural selection favours genes that maximize their transmission to the next generation. Here, we discuss recent applications of this principle to the study of gametocyte sex ratios in malaria and other apicomplexan parasites. Sex ratios matter because they are an important determinant of fitness and transmission success -- and hence of disease epidemiology and evolution. Moreover, inbreeding rates can be estimated from gametocyte sex ratios. The sex ratio is also an excellent model trait for testing the validity of important components of what is being marketed as 'Darwinian medicine'.     

Turtle mating patterns buffer against disruptive effects of climate change

For organisms with temperature-dependent sex determination (TSD), skewed offspring sex ratios are common. However, climate warming poses the unique threat of producing extreme sex ratio biases that could ultimately lead to population extinctions. In marine turtles, highly female-skewed hatchling sex ratios already occur and predicted increases in global temperatures are expected to exacerbate this trend, unless species can adapt. However, it is not known whether offspring sex ratios persist into adulthood, or whether variation in male mating success intensifies the impact of a shortage of males on effective population size. Here, we use parentage analysis to show that in a rookery of the endangered green turtle (Chelonia mydas), despite an offspring sex ratio of 95 per cent females, there were at least 1.4 reproductive males to every breeding female. Our results suggest that male reproductive intervals may be shorter than the 2-4 years typical for females, and/or that males move between aggregations of receptive females, an inference supported by our satellite tracking, which shows that male turtles may visit multiple rookeries. We suggest that male mating patterns have the potential to buffer the disruptive effects of climate change on marine turtle populations, many of which are already seriously threatened.     

Climate effects on offspring sex ratio in a viviparous lizard

1. Understanding individual and population responses to climate change is emerging as an important challenge. Because many phenotypic traits are sensitive to environmental conditions, directional climate change could significantly alter trait distribution within populations and may generate an evolutionary response. 2. In species with environment-dependent sex determination, climate change may lead to skewed sex ratios at hatching or birth. However, there are virtually no empirical data on the putative link between climatic parameters and sex ratios from natural populations. 3. We monitored a natural population of viviparous lizards with temperature-dependent sex determination (Niveoscincus ocellatus) over seven field seasons. Sex ratios at birth fluctuated significantly among years and closely tracked thermal conditions in the field, with the proportion of male offspring increasing in colder years. 4. This is the first study to demonstrate the effect of local climatic conditions (e.g. temperature) on offspring sex ratio fluctuations in a free-living population of a viviparous ectotherm. A succession of warmer-than-usual years (as predicted under many climate-change scenarios) likely would generate female-biased sex ratios at birth, while an increase in interannual variation (as also predicted under climate change scenarios) could lead to significant fluctuations in cohort sex ratios. If cohort sex ratio bias at birth leads to adult sex ratio bias, long-term directional changes in thermal conditions may have important effects on population dynamics in this species.     

Biased sex ratios in the dioecious annual Croton texensis (Euphorbiaceae) are not due to environmental sex determination

At Arapaho Prairie, in the sandhills of western Nebraska, the dioecious annual Croton texensis (Euphorbiaceae) exhibits biased sex ratios. Moreover, the direction of bias changes from year to year: in 1994 the study population was significantly female biased, in 1995 and 1996 it was significantly male biased, and in 1997 and 1998 the sex ratio did not differ from 1 : 1. Such variation in the observed sex ratio in plants is frequently attributed to environmental sex determination (ESD), which is favored by natural selection if the rate of fitness gain across an environmental gradient is greater for one sex than the other. We performed experiments to determine: (1) whether variation in the sex ratio is correlated with environmental conditions, as would be expected if ESD is operating, and (2) whether ESD, if present, would be favored by natural selection. In a common garden experiment in which water and fertilizer were manipulated the sex ratio was marginally male biased in treatments in which water was added, but not different from 1 : 1 in other treatments. In field plots into which seeds were planted none of several soil characteristics, nor overall plot quality for C. texensis (measured as average plant biomass) were correlated with plot sex ratio. However, plots in which a large number of planted seeds emerged tended to be female biased. These results provide very weak evidence for sex ratio bias across an environmental gradient, and thus provide little evidence for ESD. Moreover, sex-by-environment interactions for fitness, which are required for the evolution of ESD, were absent for all measured variables. Thus, ESD does not appear to be favored by natural selection in this population. Instead, these biases may have been caused by differences between the sexes in germination and/or early mortality.     

INEXPLICABLY FEMALE‐BIASED SEX RATIOS IN MELITTOBIA WASPS

The sex ratio behavior of parasitoid wasps in the genus Melittobia is scandalous. In contrast to the prediction of Hamilton's local mate competition theory, and the behavior of numerous other species, their extremely female‐biased sex ratios (1–5% males) change little in response to the number of females that lay eggs on a patch. We examined the mating structure and fitness consequences of adjusting the sex ratio in M. australica and found that (1) the rate of inbreeding did not differ from that expected with random mating within each patch; (2) the fitness of females that produced less female‐biased sex ratios (10 or 20% males) was greater than that of females who produced the sex ratio normally observed in M. australica. These results suggest that neither assortative mating nor asymmetrical competition between males can explain the extreme sex ratios. More generally, the finding that the sex ratios produced by females led to a decrease in their fitness suggests that the existing theory fails to capture a key aspect of the natural history of Melittobia, and emphasizes the importance of examining the fitness consequences of different sex ratio strategies, not only whether observed sex ratios correlate with theoretical predictions.