Adult sex ratios in wild bird populations

Offspring sex ratios in wild bird populations, and the extent to which they vary from the equality expected by random genotypic sex determination, have received much recent attention. Adult sex ratios (ASRs) in wild birds, on the other hand, remain very poorly described, and many of the questions about them posed by Ernst Mayr in 1939 remain unanswered. This review assesses population-level sex ratio patterns in wild bird populations, with an emphasis on the ASR. A quantitative assessment of over 200 published estimates of ASR, covering species from a wide range of taxa, regions and habitats, supported Mayr's assertion that skewed ASRs are common in wild bird populations. On average, males outnumbered females by around 33%, and 65% of published estimates differed significantly from equality. In contrast, population-level estimates of offspring sex ratio in birds did not generally differ from equality, and mean ASR across a range of wild mammal species was strongly female-skewed. ASR distortion in birds was significantly more severe in populations of globally threatened species than in non-threatened species, a previously undescribed pattern that has profound implications for their monitoring and conservation. Higher female mortality, rather than skewed offspring sex ratio, is the main driver of male-skewed ASRs in birds, and the causes and implications of this are reviewed. While estimates of ASR in wild bird populations may be subject to a number of biases, which are discussed, there is currently no quantitative evidence that an ASR of one male to one female represents the norm in birds. A better understanding and reporting of ASRs in wild bird populations could contribute greatly to our understanding of population processes and could contribute much to theoretical and applied research and conservation.     

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

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

Adult sex ratio variation: implications for breeding system evolution

Adult sex ratio (ASR) exhibits immense variation in nature, although neither the causes nor the implications of this variation are fully understood. According to theory, the ASR is expected to influence sex roles and breeding systems, as the rarer sex in the population has more potential partners to mate with than the more common sex. Changes in mate choice, mating systems and parental care suggest that the ASR does influence breeding behaviour, although there is a need for more tests, especially experimental ones. In the context of breeding system evolution, the focus is currently on operational sex ratios (OSRs). We argue that the ASR plays a role of similar importance and urge researchers to study the ASR and the OSR side by side. Finally, we plead for a dynamic view of breeding system evolution with feedbacks between mating, parenting, OSR and ASR on both ecological and evolutionary time scales.     

Sex‐biased breeding dispersal is predicted by social environment in birds

Sex‐biased dispersal is common in vertebrates, although the ecological and evolutionary causes of sex differences in dispersal are debated. Here, we investigate sex differences in both natal and breeding dispersal distances using a large dataset on birds including 86 species from 41 families. Using phylogenetic comparative analyses, we investigate whether sex‐biased natal and breeding dispersal are associated with sexual selection, parental sex roles, adult sex ratio (ASR), or adult mortality. We show that neither the intensity of sexual selection, nor the extent of sex bias in parental care was associated with sex‐biased natal or breeding dispersal. However, breeding dispersal was related to the social environment since male‐biased ASRs were associated with female‐biased breeding dispersal. Male‐biased ASRs were associated with female‐biased breeding dispersal. Sex bias in adult mortality was not consistently related to sex‐biased breeding dispersal. These results may indicate that the rare sex has a stronger tendency to disperse in order to find new mating opportunities. Alternatively, higher mortality of the more dispersive sex could account for biased ASRs, although our results do not give a strong support to this explanation. Whichever is the case, our findings improve our understanding of the causes and consequences of sex‐biased dispersal. Since the direction of causality is not yet known, we call for future studies to identify the causal relationships linking mortality, dispersal, and ASR.     

Female common lizards (Lacerta vivipara) do not adjust their sex-biased investment in relation to the adult sex ratio

Sex allocation theory predicts that facultative maternal investment in the rare sex should be favoured by natural selection when breeders experience predictable variation in adult sex ratios (ASRs). We found significant spatial and predictable interannual changes in local ASRs within a natural population of the common lizard where the mean ASR is female-biased, thus validating the key assumptions of adaptive sex ratio models. We tested for facultative maternal investment in the rare sex during and after an experimental perturbation of the ASR by creating populations with female-biased or male-biased ASR. Mothers did not adjust their clutch sex ratio during or after the ASR perturbation, but produced sons with a higher body condition in male-biased populations. However, this differential sex allocation did not result in growth or survival differences in offspring. Our results thus contradict the predictions of adaptive models and challenge the idea that facultative investment in the rare sex might be a mechanism regulating the population sex ratio.     

Patterns of variation in female-biased colony sex ratios in a social spider

Colonies of a social spider Achaearanea wau (Theridiidae) from Papua, New Guinea have adult and juvenile sex ratios that are biased towards females, and this probably represents a primary bias at the egg stage. Adult sex ratios are less female-biased than are juvenile sex ratios, and both vary significantly among colonies. Adult sex ratios covary with colony size: small colonies have a larger proportion of males than large ones. The pattern of variation in adult sex ratio may be due to greater mortality of females than of males during maturation. Juvenile sex ratios do not covary with colony size, nor do they differ among populations. Colony size, however, does have a significant effect on survival and dispersal in colonies. I conclude, therefore, that a conditional sex ratio strategy, in which the primary sex ratio of the colony is adjusted to changing demographic patterns, does not occur in A. wau. I suggest that environmental heterogeneity acting on individual reproductive output may be responsible for the observed variation among colonies in juvenile sex ratios.     

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.     

Developmental mortality increases sex‐ratio bias of a size‐dimorphic bark beetle

1. Given sexual size dimorphism, differential mortality owing to body size can lead to sex‐biased mortality, proximately biasing sex ratios. This mechanism may apply to mountain pine beetles, Dendroctonus ponderosae Hopkins, which typically have female‐biased adult populations (2 : 1) with females larger than males. Smaller males could be more susceptible to stresses than larger females as developing beetles overwinter and populations experience high mortality. 2. Survival of naturally‐established mountain pine beetles during the juvenile stage and the resulting adult sex ratios and body sizes (volume) were studied. Three treatments were applied to vary survival in logs cut from trees containing broods of mountain pine beetles. Logs were removed from the forest either in early winter, or in spring after overwintering below snow or after overwintering above snow. Upon removal, logs were placed at room temperature to allow beetles to complete development under similar conditions. 3. Compared with beetles from logs removed in early winter, mortality was higher and the sex ratio was more female‐biased in overwintering logs. The bias increased with overwinter mortality. However, sex ratios were female‐biased even in early winter, so additional mechanisms, other than overwintering mortality, contributed to the sex‐ratio bias. Body volume varied little relative to sex‐biased mortality, suggesting other size‐independent causes of male‐biased mortality. 4. Overwintering mortality is considered a major determinant of mountain pine beetle population dynamics. The disproportionate survival of females, who initiate colonisation of live pine trees, may affect population dynamics in ways that have not been previously considered.     

Climate fluctuations interact with local demography and resources to predict spatially dynamic adult sex ratios in a megaherbivore

Adult sex ratio (ASR) is a fundamental concept in population and evolutionary biology, with implications for management and conservation. Although ASR is typically measured at the population‐level, local mate competition points toward spatial variation in ASR within populations, the causes of which remain unclear. Over five breeding seasons (2008–2012), we tracked the life histories and movements of all male and female feral horses known to be alive (n = 721) on Sable Island, Canada, to investigate determinants of spatially explicit ASRs. We show that local demographic traits (density, adult female abundance, and abundance of unpaired males (e.g. floaters, adult bachelors)) operate together with inter‐annual changes in weather to determine asymmetrical ASRs across time and space that deviate from the population‐level mean. While accounting for possible confounding effects of unpaired male movements and weather, we also show that local demographics are best explained by different responses to an environmental gradient (distance to surface water). Our results demonstrate that local demographic traits operate as mechanisms by which environmental gradients and weather can shape spatial variation in ASR within wild populations, which has important implications for predicting how opportunities for sexual selection may follow from changes in resource availability and climate.     

Sex allocation and sex‐specific parental investment in an endangered seabird

Biased offspring sex ratio is relatively rare in birds and sex allocation can vary with environmental conditions, with the larger and more costly sex, which can be either the male or female depending on species, favoured during high food availability. Sex‐specific parental investment may lead to biased mortality and, coupled with unequal production of one sex, may result in biased adult sex ratio, with potential grave consequences on population stability. The African Penguin Spheniscus demersus, endemic to southern Africa, is an endangered monogamous seabird with bi‐parental care. Female adult African Penguins are smaller, have a higher foraging effort when breeding and higher mortality compared with adult males. In 2015, a year in which environmental conditions were favourable for breeding, African Penguin chick production on Bird Island, Algoa Bay, South Africa, was skewed towards males (1.5 males to 1 female). Males also had higher growth rates and fledging mass than females, with potentially higher post‐fledging survival. Female, but not male, parents had higher foraging effort and lower body condition with increasing number of male chicks in their brood, thereby revealing flexibility in their parental strategy, but also the costs of their investment in their current brood. The combination of male‐biased chick production and higher female mortality, possibly at the juvenile stage as a result of lower parental investment in female chicks, and/or at the adult stage as a result of higher parental investment, may contribute to a biased adult sex ratio (ASR) in this species. While further research during years of contrasting food availability is needed to confirm this trend, populations with male‐skewed ASRs have higher extinction risks and conservation strategies aiming to benefit female African Penguin might need to be developed.     

Does breeding population trajectory and age of nesting females influence disparate nestling sex ratios in two populations of Cooper's hawks?

Offspring sex ratios at the termination of parental care should theoretically be skewed toward the less expensive sex, which in most avian species would be females, the smaller gender. Among birds, however, raptors offer an unusual dynamic because they exhibit reversed size dimorphism with females being larger than males. And thus theory would predict a preponderance of male offspring. Results for raptors and birds in general have been varied although population‐level estimates of sex ratios in avian offspring are generally at unity. Adaptive adjustment of sex ratios in avian offspring is difficult to predict perhaps in part due to a lack of life‐history details and short‐term investigations that cannot account for precision or repeatability of sex ratios across time. We conducted a novel comparative study of sex ratios in nestling Cooper's hawks (Accipiter cooperii) in two study populations across breeding generations during 11 years in Wisconsin, 2001–2011. One breeding population recently colonized metropolitan Milwaukee and exhibited rapidly increasing population growth, while the ex‐Milwaukee breeding population was stable. Following life‐history trade‐off theory and our prediction regarding this socially monogamous species in which reversed sexual size dimorphism is extreme, first‐time breeding one‐year‐old, second‐year females in both study populations produced a preponderance of the smaller and cheaper sex, males, whereas ASY (after‐second‐year), ≥2‐year‐old females in Milwaukee produced a nestling sex ratio near unity and predictably therefore a greater proportion of females compared to ASY females in ex‐Milwaukee who produced a preponderance of males. Adjustment of sex ratios in both study populations occurred at conception. Life histories and selective pressures related to breeding population trajectory in two age cohorts of nesting female Cooper's hawk likely vary, and it is possible that these differences influenced the sex ratios we documented for two age cohorts of female Cooper's hawks in Wisconsin.     

Skewed adult sex ratios in Columbina ground doves from Venezuela

Although sex ratios at conception are close to 1:1 in most species of birds, skewed adult sex ratios (ASRs) are not uncommon in populations of birds, and occur frequently at local and temporal scales. ASRs are a key variable influencing population demography, breeding systems, and many aspects of the behavior of birds. However, factors contributing to variation in ASRs, particularly for tropical species of birds, remain poorly understood. By compiling information from field sites and records from bird collections, we found that the ASRs of four species of Columbina ground doves from Venezuela deviated significantly from parity. Males of all species outnumbered females at all field sites and in all museum samples. ASR, expressed as the proportion of males, ranged from 0.59 for Common Ground Doves (Columbina passerina) to 0.65 for Plain‐breasted Ground Doves (Columbina minuta) in the overall samples. Males outnumbered females by ~ 44% in Common Ground Doves and by 85% in Plain‐breasted Ground Doves. Our samples included birds collected as specimens over many decades and across broad geographic areas, suggesting that skewed ASRs are characteristic of Venezuelan ground doves. Because these ground doves do not exhibit pronounced sexual size dimorphism and have socially monogamous breeding systems, selection would be expected to favor equal investment in males and females at hatching. As such, we argue that greater post‐hatching mortality of females, rather than deviations in the sex ratio of embryos, is the main cause of the biased ASRs of Venezuelan ground doves.     

Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara . This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.     

Size‐selective fishing affects sex ratios and the opportunity for sexual selection in Alaskan sockeye salmon Oncorhynchus nerka

Selective exploitation can cause adverse ecological and evolutionary changes in wild populations and also affect sex ratios but few studies have empirically documented skewed sex ratios in exploited fishes (other than species with extreme sexual size dimorphism, SSD). To investigate the possibility of sex‐selective fishing on Alaskan sockeye salmon Oncorhynchus nerka, we assessed sex ratios in fish at two spatial scales: within each of five fishing districts and among 13 breeding populations in one of these districts. We predicted that populations’ sex ratios would vary based on the average size of fish and SSD because size affects vulnerability to fishing. At the larger scale, we found a small but significant bias in fish returning to four of the five fishing districts (average = 52% females), and in four of the five districts males were caught at significantly higher rates than females. At the finer scale there was marked variation in sex ratio on the breeding grounds, ranging from 36% to 47% males. Populations with fish of intermediate sizes experienced the greatest sex ratio biases; the greater vulnerability of males than females to fishing resulted from a combination of larger SSD and different harvest rates between the sexes associated with the fishery size‐selectivity curve shape. Skewed sex ratios may change competition and behavior on the breeding grounds, relaxing selection on male traits associated with mate choice by females or intra‐sexual competition and altering demographic and evolutionary pressures on the fish. Assessment of the size selectivity of fishing gear and the population's SSD can help to illuminate if and how exploitation can affect sex ratios. Future studies examining size‐selective fishing should also evaluate the consequences for sex ratios, as this might help explain changes in harvested population structure and sustainability.     

Parental investment, sexual selection and sex ratios

Conventional sex roles imply caring females and competitive males. The evolution of sex role divergence is widely attributed to anisogamy initiating a self‐reinforcing process. The initial asymmetry in pre‐mating parental investment (eggs vs. sperm) is assumed to promote even greater divergence in post‐mating parental investment (parental care). But do we really understand the process? Trivers [Sexual Selection and the Descent of Man 1871–1971 (1972), Aldine Press, Chicago] introduced two arguments with a female and male perspective on whether to care for offspring that try to link pre‐mating and post‐mating investment. Here we review their merits and subsequent theoretical developments. The first argument is that females are more committed than males to providing care because they stand to lose a greater initial investment. This, however, commits the ‘Concorde Fallacy’ as optimal decisions should depend on future pay‐offs not past costs. Although the argument can be rephrased in terms of residual reproductive value when past investment affects future pay‐offs, it remains weak. The factors likely to change future pay‐offs seem to work against females providing more care than males. The second argument takes the reasonable premise that anisogamy produces a male‐biased operational sex ratio (OSR) leading to males competing for mates. Male care is then predicted to be less likely to evolve as it consumes resources that could otherwise be used to increase competitiveness. However, given each offspring has precisely two genetic parents (the Fisher condition), a biased OSR generates frequency‐dependent selection, analogous to Fisherian sex ratio selection, that favours increased parental investment by whichever sex faces more intense competition. Sex role divergence is therefore still an evolutionary conundrum. Here we review some possible solutions. Factors that promote conventional sex roles are sexual selection on males (but non‐random variance in male mating success must be high to override the Fisher condition), loss of paternity because of female multiple mating or group spawning and patterns of mortality that generate female‐biased adult sex ratios (ASR). We present an integrative model that shows how these factors interact to generate sex roles. We emphasize the need to distinguish between the ASR and the operational sex ratio (OSR). If mortality is higher when caring than competing this diminishes the likelihood of sex role divergence because this strongly limits the mating success of the earlier deserting sex. We illustrate this in a model where a change in relative mortality rates while caring and competing generates a shift from a mammalian type breeding system (female‐only care, male‐biased OSR and female‐biased ASR) to an avian type system (biparental care and a male‐biased OSR and ASR).     

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.     

Demographic origins of skewed operational and adult sex ratios: perturbation analyses of two-sex models

Skewed sex ratios – operational (OSR) and Adult (ASR) - arise from sexual differences in reproductive behaviours and adult survival rates due to the cost of reproduction. However, skewed sex-ratio at birth, sex-biased dispersal and immigration, and sexual differences in juvenile mortality may also contribute. We present a framework to decompose the roles of demographic traits on sex ratios using perturbation analyses of two-sex matrix population models. Metrics of sensitivity are derived from analyses of sensitivity, elasticity, life-table response experiments and life stage simulation analyses, and applied to the stable stage distribution instead of lambda. We use these approaches to examine causes of male-biased sex ratios in two populations of green-rumped parrotlets ( Forpus passerinus ) in Venezuela. Female local juvenile survival contributed the most to the unbalanced OSR and ASR due to a female-biased dispersal rate, suggesting sexual differences in philopatry can influence sex ratios more strongly than the cost of reproduction.     

The effect of temperature on sex ratio in the isopod Porcellionides pruinosus: Environmental sex determination or a by-product of cytoplasmic sex determination?

The sex ratios of the progenies of woodlice Porcellionides pruinosus (Crustacea, Isopoda) raised at different temperatures were studied. Females from three French populations sampled in the wild produced highly female-biased broods at 20°C and male-biased broods above 30°C. The effect of high temperature was not due to selective mortality of females. Sex determination was thus sensitive to temperature in P. pruinosus. We also found an interpopulation variability of sex ratio thermosensitivity and a weak inheritance of male-biased sex ratios at high temperatures. Samples taken from a wild population throughout the year showed that while the thermal conditions required for changes in the sex ratio occurred, there was no significant variation in the sex ratio. On the other hand, almost all the females and many males in the four populations studied harboured intracytoplasmic bacteria. These maternally inherited symbionts belong to the genus Wolbachia and are known to possess a feminizing effect. While in other arthropods Wolbachia are destroyed at high temperatures, the symbionts of P. pruinosus were detected by a PCR procedure whatever the rearing temperatures. In light of these results, we propose that the thermosensitivity of sex determination in P. pruinosus could reflect the removal of the cytoplasmic effect on sex determination rather than environmental sex determination sensu stricto. The reduction in the amount of bacteria (but not their entire elimination), or the inhibition of bacterial metabolism, may be responsible for sex ratio variations relating to temperature. The incomplete inheritance of male-biased sex ratios at high temperatures might reflect a selection of thermo-tolerant bacterial strains.     

Male‐skewed adult sex ratio,survival, mating opportunity and annual productivity in the Snowy Plover Charadrius alexandrinus

Sex differences in adult mortality may be responsible for male‐skewed adult sex ratios and male‐skewed parental care in some birds. Because a surplus of breeding males has been reported in serially polyandrous populations of Snowy Plover Charadrius alexandrinus, we examined sex ratio, early‐season nesting opportunities, adult survival and annual reproductive success of a Snowy Plover population at Monterey Bay, California. We tested the hypotheses that male adult survival was greater than female survival and that a sex difference in adult survival led to a skewed adult sex ratio, different mating opportunities and different annual productivity between the sexes. Virtually all females left chicks from their first broods to the care of the male and re‐nested with a new mate. As a result, females had time to parent three successful nesting attempts during the lengthy breeding season, whereas males had time for only two successful attempts. Among years, the median population of nesting Plovers was 96 males and 84 females (median difference = 9), resulting in one extra male per eight pairs. The number of potential breeders without mates during the early nesting period each year was higher in males than in females. Adult male survival (0.734 ± 0.028 se) was higher than female survival (0.693 ± 0.030 se) in top‐ranked models. Annually, females parented more successful clutches and fledged more chicks than their first mates of the season. Our results suggest that in C. alexandrinus a sex difference in adult survival results in a male‐skewed sex ratio, which creates more nesting opportunities and greater annual productivity for females than for males.     

Correlations between ultraviolet coloration, overwinter survival and offspring sex ratio in the blue tit

We studied the correlations between offspring sex ratio, UV coloration and overwinter survival in a population of blue tits, breeding in Gotland, Sweden, over three consecutive breeding seasons. In 2 of 3 years, we found that females paired to males with relatively brighter UV-coloration produced a greater proportion of sons in their broods, and that this effect was significant with all 3 years combined, despite a significant year by male UV interaction. In addition, we found other correlates of sex ratio (breeding time, female age and clutch size) in some, but not all years, and some of these showed significantly different relationships with sex ratio between years. In both years for which data were available, there were indications that males with relatively brighter UV coloration, and that paired with females that produced male-biased clutches, were more likely to survive to the next year. In addition, we also found that in both males and females, individuals produced similar sex ratios in consecutive years. Because correlations with the sex ratio may be expected to be weak, variation in results between years within the same population may be explained by low statistical power or genuine biological differences. Our results suggest that conclusions about sex ratio variation in birds should be based on multiple years. The correlations that we found in some years of this study are consistent with models of adaptive sex ratio adjustment in response to mate quality. However, careful experimental work is required to provide tests of the assumptions of these models, and should be a priority for future work.