Sexual conflict in action: An antagonistic relationship between maternal and paternal sex allocation in the tammar wallaby,Notamacropus eugenii

Sex ratio biases are often inconsistent, both among and within species and populations. While some of these inconsistencies may be due to experimental design, much of the variation remains inexplicable. Recent research suggests that an exclusive focus on mothers may account for some of the inconsistency, with an increasing number of studies showing variation in sperm sex ratios and seminal fluids. Using fluorescent in‐situ hybridization, we show a significant population‐level Y‐chromosome bias in the spermatozoa of wild tammar wallabies, but with significant intraindividual variation between males. We also show a population‐level birth sex ratio trend in the same direction toward male offspring, but a weaning sex ratio that is significantly female‐biased, indicating that males are disproportionately lost during lactation. We hypothesize that sexual conflict between parents may cause mothers to adjust offspring sex ratios after birth, through abandonment of male pouch young and reactivation of diapaused embryos. Further research is required in a captive, controlled setting to understand what is driving and mechanistically controlling sperm sex ratio and offspring sex ratio biases and to understand the sexually antagonistic relationship between mothers and fathers over offspring sex. These results extend beyond sex allocation, as they question studies of population processes that assume equal input of sex chromosomes from fathers, and will also assist with future reproduction studies for management and conservation of marsupials.     

Birth sex ratio in captive mammals: Patterns,biases, and the implications for management and conservation

Sex allocation theory predicts that a female should produce the offspring of the sex that most increases her own fitness. For polygynous species, this means that females in superior condition should bias offspring production toward the sex with greater variation in lifetime reproductive success, which is typically males. Captive mammal populations are generally kept in good nutritional condition with low levels of stress, and thus populations of polygynous species might be expected to have birth sex ratios biased toward males. Sex allocation theory also predicts that when competition reduces reproductive success of the mother, she should bias offspring toward whichever sex disperses. These predicted biases would have a large impact on captive breeding programs because unbalanced sex ratios may compromise use of limited space in zoos. We examined 66 species of mammals from three taxonomic orders (primates, ungulates, and carnivores) maintained in North American zoos for evidence of birth sex ratio bias. Contrary to our expectations, we found no evidence of bias toward male births in polygynous populations. We did find evidence that birth sex ratios of primates are male biased and that, within primates, offspring sex was biased toward the naturally dispersing sex. We also found that most species experienced long contiguous periods of at least 7 years with either male‐ or female‐biased sex ratios, owing in part to patterns of dispersal (for primates) and/or to stochastic causes. Population managers must be ready to compensate for significant biases in birth sex ratio based on dispersal and stochasticity. Zoo Biol 19:11–25, 2000. © 2000 Wiley‐Liss, Inc.     

Population structure leads to male‐biased population sex ratios under environmental sex determination

Spatial structure has been shown to favor female‐biased sex allocation, but current theory fails to explain male biases seen in many taxa, particularly those with environmental sex determination (ESD). We present a theory and accompanying individual‐based simulation model that demonstrates how population structure leads to male‐biased population sex ratios under ESD. Our simulations agree with earlier work showing that the high productivity of female‐producing habitats creates a net influx of sex‐determining alleles into male‐producing habitats, causing larger sex ratio biases, and lower productivity in male‐producing environments (Harts et al. 2014). In contrast to previous findings, we show that male‐biasing habitats disproportionately impact the global sex ratio, resulting in stable male‐biased population sex ratios under ESD. The failure to detect a male bias in earlier work can be attributed to small subpopulation sizes leading to local mate competition, a condition unlikely to be met in most ESD systems. Simulations revealed that consistent male biases are expected over a wide range of population structures, environmental conditions, and genetic architectures of sex determination, with male excesses as large as 30 percent under some conditions. Given the ubiquity of genetic structure in natural populations, we predict that modest, enduring male biased allocation should be common in ESD species, a pattern consistent with reviews of ESD sex ratios.     

Temperature-Dependent Sex Determination in Sea Turtles in the Context of Climate Change: Uncovering the Adaptive Significance

The adaptive significance of temperature-dependent sex determination (TSD) in reptiles remains unknown decades after TSD was first identified in this group. Concurrently, there is growing concern about the effect that rising temperatures may have on species with TSD, potentially producing extremely biased sex ratios or offspring of only one sex. The current state-of the-art in TSD research on sea turtles is reviewed here and, against current paradigm, it is proposed that TSD provides an advantage under warming climates. By means of coadaptation between early survival and sex ratios, sea turtles are able to maintain populations. When offspring survival declines at high temperatures, the sex that increases future fecundity (females) is produced, increasing resilience to climate warming. TSD could have helped reptiles to survive mass extinctions in the past via this model. Flaws in research on sex determination in sea turtles are also identified and it is suggested that the development of new techniques will revolutionize the field.     

Effects of global warming on sex ratios in fishes

In fishes, sex is determined by genetics, the environment or an interaction of both. Temperature is among the most important environmental factors that can affect sex determination. As a consequence, changes in temperature at critical developmental stages can induce biases in primary sex ratios in some species. However, early sex ratios can also be biased by sex-specific tolerances to environmental stresses that may, in some cases, be amplified by changes in water temperature. Sex-specific reactions to environmental stress have been observed at early larval stages before gonad formation starts. It is therefore necessary to distinguish between temperature effects on sex determination, generally acting through the stress axis or epigenetic mechanisms, and temperature effects on sex-specific mortality. Both are likely to affect sex ratios and hence population dynamics. Moreover, in cases where temperature effects on sex determination lead to genotype–phenotype mismatches, long-term effects on population dynamics are possible, for example temperature-induced masculinization potentially leading to the loss of Y chromosomes or feminization to male-biased operational sex ratios in future generations. To date, most studies under controlled conditions conclude that if temperature affects sex ratios, elevated temperatures mostly lead to a male bias. The few studies that have been performed on wild populations seem to confirm this general trend. Recent findings suggest that transgenerational plasticity could mitigate the effects of warming on sex ratios in some populations.     

The influence of demography and local mating environment on sex ratios in a wind‐pollinated dioecious plant

Negative frequency‐dependent selection should result in equal sex ratios in large populations of dioecious flowering plants, but deviations from equality are commonly reported. A variety of ecological and genetic factors can explain biased sex ratios, although the mechanisms involved are not well understood. Most dioecious species are long‐lived and/or clonal complicating efforts to identify stages during the life cycle when biases develop. We investigated the demographic correlates of sex‐ratio variation in two chromosome races of Rumex hastatulus, an annual, wind‐pollinated colonizer of open habitats from the southern USA. We examined sex ratios in 46 populations and evaluated the hypothesis that the proximity of males in the local mating environment, through its influence on gametophytic selection, is the primary cause of female‐biased sex ratios. Female‐biased sex ratios characterized most populations of R.  hastatulus (mean sex ratio = 0.62), with significant female bias in 89% of populations. Large, high‐density populations had the highest proportion of females, whereas smaller, low‐density populations had sex ratios closer to equality. Progeny sex ratios were more female biased when males were in closer proximity to females, a result consistent with the gametophytic selection hypothesis. Our results suggest that interactions between demographic and genetic factors are probably the main cause of female‐biased sex ratios in R. hastatulus. The annual life cycle of this species may limit the scope for selection against males and may account for the weaker degree of bias in comparison with perennial Rumex species.     

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.     

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.     

Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio

1. Parasitic Hymenoptera reproduce by arrhenotokous parthenogenesis, and females of these species are able to control their progeny sex ratios. In structured populations of parasitic Hymenoptera, primary sex ratios are often highly biased toward females. However, sex ratio can be adjusted to the quality of encountered patches or hosts or be modified by differential developmental mortality.
2. In this paper, the effects were evaluated of the quality of encountered hosts and developmental mortality on the sex ratio in Anaphes victus , a solitary egg parasitoid whose first instar larvae present a sexual dimorphism and where superparasitism is regulated by larval fights between first instar larvae.
3. The results showed that a female-biased sex ratio is allocated to unparasitized hosts. In the presence of parasitized hosts, the second (superparasitizing) female produced a significantly higher sex ratio than the first female but the tertiary sex ratio (sex ratio at emergence) was not significantly different from the sex ratio produced with unparasitized hosts. The increase in the primary sex ratio produced by the second female was mostly compensated by the higher mortality of male larvae.     

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.     

Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

Precision in sex allocation is influenced by mate choice in Drosophila melanogaster

Theory predicts that a 1 : 1 sex ratio is favoured in the absence of countervailing selection pressures. In an experiment with Drosophila melanogaster, we found significantly greater variation in the offspring sex ratios of freely mated flies than would be expected by the binomial distribution. In a surprise result, control flies given no mate choice exhibited significant under-dispersal in their sex ratio variation, possibly from sperm limitation. Both treatments, however, produced populations with a 1 : 1 sex ratio. This supports the hypothesis that sexually antagonistic selection for reproductive success in sons, and fecundity in daughters, may overcome selection for an equal sex ratio. Such precision in sex allocation may allow for the maintenance of genetic variation underlying trade-offs between male and female reproductive success.     

Statewide and local recruitment of mourning doves in Missouri

Intensive harvests have the potential to greatly affect local mourning dove (Zenaida macroura) populations, a popular gamebird and songbird. To evaluate if recruitment was commensurate with harvest, we applied a ratio-based method to estimate local and statewide mourning dove recruitment across 7 public hunting areas in Missouri from 2005 to 2011. We estimated recruitment from preharvest adult sex ratios and harvest age ratios that incorporated various methods to address potential inherent biases (e.g., bias in the adults of unknown sex in preharvest samples, bias in unknown age wings, and local differential vulnerability; DV). Data from 356 radio-marked doves revealed a DV rate, where hatch year doves were, on average 2.7× more likely to be harvested than adult doves. Recruitment estimates for local areas were highly variable and in some cases, biologically unrealistic (e.g., >10 offspring/female), because of small preharvest sample sizes. However, data pooled statewide provided recruitment estimates of 3.1 offspring/female (±0.3 SE) or 4.1 offspring/female (±0.3 SE), assuming samples of unknown sex doves were female biased or male biased, respectively. Although statewide estimates agree with directly observed rates, the sex ratios and differential vulnerability comprising them vary considerably from what has been previously assumed. Whether preharvest sex ratios are biased from trapping methods has 2 important implications; either regional approaches have overestimated recruitment or the number of females in Missouri's population is much less than originally thought. Because each of these scenarios are important to understanding the effects of regional harvest management on Missouri's dove population, they highlight the importance of a better understanding of biases involved in estimating recruitment. © 2012 The Wildlife Society.     

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.     

Reproductive biology of captive and free-ranging spider monkeys

Records from 42 zoos and from long-term studies of wild populations were analysed to describe the reproductive biology of spider monkeys (Ateles spp.). Both data sets suggested that spider monkey females typically have their first infant between 7 and 8 years of age with an interbirth interval of approximately 32–36 months. Infant sex ratio for zoo populations was approximately 1 male to 1 female; infant sex ratios from wild populations were variable. Zoo records provided adequate sample size to suggest that interbirth interval was not influenced by the sex of the infant produced, and that the sex ratio and the probability of infant survival did not change with the number of infants the mother had produced. The findings of this study have implications with respect to the conservation of New World primate species. Since spider monkeys take a long time to reach sexual maturity and their interbirth interval is longer than that expected based on their body size, their populations may be slow to recover following disturbances. Thus, particular care should be taken for the protection of these species.     

Humans at tropical latitudes produce more females

Skews in the human sex ratio at birth have captivated scientists for over a century. The accepted average human natal sex ratio is slightly male biased, at 106 males per 100 females or 51.5 per cent males. Studies conducted on a localized scale show that sex ratios deviate from this average in response to a staggering number of social, economical and physiological variables. However, these patterns often prove inconsistent when expanded to other human populations, perhaps because the nature of the influences themselves exhibit substantial cultural variation. Here, data collected from 202 countries over a decade show that latitude is a primary factor influencing the ratio of males and females produced at birth; countries at tropical latitudes produced significantly fewer boys (51.1% males) annually than those at temperate and subarctic latitudes (51.3%). This pattern remained strong despite enormous continental variation in lifestyle and socio-economic status, suggesting that latitudinal variables may act as overarching cues on which sex ratio variation in humans is based.     

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.     

Intralocus sexual conflict and offspring sex ratio

Males and females frequently have different fitness optima for shared traits, and as a result, genotypes that are high fitness as males are low fitness as females, and vice versa. When this occurs, biasing of offspring sex-ratio to reduce the production of the lower-fitness sex would be advantageous, so that for example, broods produced by high-fitness females should contain fewer sons. We tested for offspring sex-ratio biasing consistent with these predictions in broad-horned flour beetles. We found that in both wild-type beetles and populations subject to artificial selection for high- and low-fitness males, offspring sex ratios were biased in the predicted direction: low-fitness females produced an excess of sons, whereas high-fitness females produced an excess of daughters. Thus, these beetles are able to adaptively bias sex ratio and recoup indirect fitness benefits of mate choice.     

Offspring sex ratios correlate with pair-male condition in a cooperatively breeding fairy-wren

We examined sex allocation patterns in island and mainland populationsof cooperatively breeding white-winged fairy-wrens. The markeddifferences in social structure between island and mainlandpopulations, in addition to dramatic plumage variation amongmales both within and between populations, provided a uniquesituation in which we could investigate different predictionsfrom sex allocation theory in a single species. First, we testthe repayment (local resource enhancement) hypothesis by askingwhether females biased offspring sex ratios in relation to theassistance they derived from helpers. Second, we test the malequality (attractiveness) hypothesis, which suggests that femalesmated to attractive high-quality males should bias offspringsex ratios in favor of males. Finally, we test the idea thatfemales in good condition should bias offspring sex ratios towardmales because they are able to allocate more resources to offspring,whereas females in poor condition should have increased benefitsfrom producing more female offspring (Trivers-Willard hypothesis).We used molecular sexing techniques to assess total offspringsex ratios of 86 breeding pairs over 2 years. Both offspringand first brood sex ratios were correlated with the pair-male'sbody condition such that females increased the proportion ofmales in their brood in relation to the body condition (masscorrected for body size) of their social partner. This relationwas both significant and remarkably similar in both years ofour study and in both island and mainland populations. Althoughconfidence of paternity can be low in this and other fairy-wrenspecies, we show how this finding might be consistent with themale quality (attractiveness) hypothesis with respect to malecondition. There was no support for the repayment hypothesis;the presence of helpers had no effect on offspring sex ratios.There was weak support for both the male quality (attractiveness)hypothesis with respect to plumage color and the maternal conditionhypothesis, but their influence on offspring sex ratios wasnegligible after controlling for the effects of pair-male condition.     

Demographic effects of temperature‐dependent sex determination: will tuatara survive global warming?

Global climate change is of particular concern for small and isolated populations of reptiles with temperature-dependent sex determination because low genetic variation can limit adaptive response in pivotal temperatures, leading to skewed sex ratios. We explore the demographic consequences of skewed sex ratios on the viability of a tuatara population characterized by low genetic diversity. We studied the rare species of tuatara ( Sphenodon guntheri ) on the 4 ha North Brother Island in New Zealand over two nesting seasons and captured 477 individuals, with a 60% male bias in the adult population. Females first breed at 15 years and have extremely low rates of gravidity, producing clutches of three to eight eggs every 9 years. Simulations of the population using population viability analysis showed that the current population is expected to persist for at least 2000 years at hatchling sex ratios of up to 75% male, but populations with 85% male hatchlings are expected to become extinct within approximately 300 years (some eight generations). Incorporation of inbreeding depression increased the probability of extinction under male biased sex ratios, with no simulated populations surviving at hatchling sex ratios >75% male. Because recent models have predicted that climate change could lead to the production of all male S. guntheri hatchlings by 2085, we examined whether periodic intervention to produce mixed or female biased sex ratios would allow the population to survive if only males were produced in natural nests. We show that intervention every 2–3 years could buffer the effects of climate change on population sex ratios, but translocation to cooler environs might be more cost-effective. Climate change threatens tuatara populations because neither modified nesting behaviour nor adaptive response of the pivotal temperature can modify hatchling sex ratios fast enough in species with long generation intervals.