Skewed Offspring Sex Ratios Research Articles

Parental effects on offspring sex ratio in the Numbat (Myrmecobius fasciatus): does captivity influence paternal sex allocation?

Sex allocation theories predict that under different ecological conditions the production of sons and daughters will affect parental fitness differently. Skewed offspring sex ratios often occur under captive conditions where individuals are exposed to nutritional and social conditions that differ from nature. Here, we analyzed 29 years of offspring sex ratio data from a captive population of an endangered marsupial, the Numbat (Myrmecobius fasciatus). We partitioned variation in offspring sex ratio based on parental origin (captive- vs. wild-bred), parental weight, maternal age, and maternal reproductive history. Our analyses revealed no effect of parental weight or maternal origin on offspring sex ratio-however, there was a significant effect of paternal origin. Data visualization indicated that captive-bred males tended to produce male-biased litters. We discuss the result in relation to recent studies that have shown that male mammals have the capacity to be arbiters of sex allocation and highlight candidate mechanisms, but consider it with caution due to the small sample size from which the result was derived. We performed a population viability analysis (PVA) to explore the potential impact of a sex ratio skew on the sustainability of the captive Numbat population under hypothetical scenarios. Our PVA revealed that supplementation with wild individuals is critical to the persistence of the captive Numbat population and that a biased sex ratio will lead to extinction of the captive colony under certain conditions. Overall, our study demonstrates that covert sex ratio skews can persist undetected in captive populations, which have the potential to become impactful and compromise population sustainability under changed management processes.

Genome-wide DNA methylation patterns harbour signatures of hatchling sex and past incubation temperature in a species with environmental sex determination.

Conservation of thermally sensitive species depends on monitoring organismal and population-level responses to environmental change in real time. Epigenetic processes are increasingly recognized as key integrators of environmental conditions into developmentally plastic responses, and attendant epigenomic data sets hold potential for revealing cryptic phenotypes relevant to conservation efforts. Here, we demonstrate the utility of genome-wide DNA methylation (DNAm) patterns in the face of climate change for a group of especially vulnerable species, those with temperature-dependent sex determination (TSD). Due to their reliance on thermal cues during development to determine sexual fate, contemporary shifts in temperature are predicted to skew offspring sex ratios and ultimately destabilize sensitive populations. Using reduced-representation bisulphite sequencing, we profiled the DNA methylome in blood cells of hatchling American alligators (Alligator mississippiensis), a TSD species lacking reliable markers of sexual dimorphism in early life stages. We identified 120 sex-associated differentially methylated cytosines (DMCs; FDR < 0.1) in hatchlings incubated under a range of temperatures, as well as 707 unique temperature-associated DMCs. We further developed DNAm-based models capable of predicting hatchling sex with 100% accuracy (in 20 training samples and four test samples) and past incubation temperature with a mean absolute error of 1.2°C (in four test samples) based on the methylation status of 20 and 24 loci, respectively. Though largely independent of epigenomic patterning occurring in the embryonic gonad during TSD, DNAm patterns in blood cells may serve as nonlethal markers of hatchling sex and past incubation conditions in conservation applications. These findings also raise intriguing questions regarding tissue-specific epigenomic patterning in the context of developmental plasticity.

Facultative and persistent offspring sex-ratio bias in relation to the social environment in cooperatively breeding red-winged fairy-wrens (Malurus elegans)

Females should facultatively bias offspring sex ratio when fitness returns vary among sexes. In cooperative breeders, where individuals help raise others’ young, overproducing the philopatric sex will be adaptive when helpers are absent, whereas overproducing the dispersive sex may be adaptive to reduce intrasexual competition. Thus, fitness returns are expected to vary with the social environment. However, any offspring sex-ratio biases may also result from consistent among-female differences (e.g. quality) and/or environmental variables (e.g. food availability). Yet, few studies have disentangled facultative from persistent biases. We investigated offspring sex-ratio biases in relation to the social environment in cooperatively breeding red-winged fairy-wrens (Malurus elegans). Repeated observations of the same females over nine years allowed for disentanglement of facultative from persistent biases. Females without help did not overproduce daughters, despite female helpers being associated with higher fledgling survival (resource enhancement hypothesis). Instead, females without helpers facultatively overproduced sons —the slower dispersing sex— thereby ensuring long-term helper availability. Furthermore, offspring sex ratio was not biased towards the rarer sex of helpers present in the group or population (resource competition hypothesis). However, females with sex-biased helping produced similarly skewed offspring sex ratios. This among-female association may not be surprising, because helpers are previous seasons’ offspring. Thus, in addition to facultative responses to prevailing social conditions, we found evidence for persistent biases among females. This could potentially explain previous evidence for resource competition/enhancement that have typically been interpreted as facultative responses, highlighting the need for a within-female approach to better understand the adaptiveness of sex-ratio biases.Significance statementUnder certain conditions, females may benefit from producing a biased offspring sex ratio, but evidence for such effects in vertebrates is weak and inconsistent. Here, using observations of the same females under different social conditions, we show that cooperatively breeding red-winged fairy-wrens facultatively biased offspring sex ratio towards sons when living in pairs, thereby ensuring the availability of a workforce to assist in raising future offspring. However, biased offspring sex ratio patterns may also be the result of consistent differences among females. Indeed, we also found evidence for such patterns and suggest that this could be an explanation for previous findings which are often interpreted as facultative responses.

Offspring sex ratios are stable across the life course in Drosophila simulans.

Within populations, adult sex ratios influence population growth and extinction risk, mating behaviours and parental care. Sex ratio adjustment can also have pronounced effects on individual fitness. Accordingly, it is important that we understand how often, and why, offspring sex ratios deviate from parity. In Drosophila melanogaster, females appear to improve their fitness by producing fewer sons when paired with older males. However, facultative sex ratio adjustment in D.melanogaster is controversial, and our understanding of how sex ratio skew affects fitness is hampered by pronounced sexual conflict in this species. Additionally, it is unclear whether maternal age or quality interacts with paternal age to influence offspring sex ratios. Here, we test whether offspring sex ratios vary as a function of maternal quality, and maternal and paternal age in Drosophila simulans, a sister species of D.melanogaster that lacks overt sexual conflict. We find that offspring sex ratios are slightly male-biased overall, but constant across the female life course, and independent of female quality, or paternal age. To really understand if, how and when females skew offspring sex ratios, we need studies linking offspring sex ratios to paternal and maternal phenotypes that are predicted to shift optimal investment in sons and daughters.

Spatial and temporal variation in nest temperatures forecasts sex ratio skews in a crocodilian with environmental sex determination.

Species displaying temperature-dependent sex determination (TSD) are especially vulnerable to the effects of a rapidly changing global climate due to their profound sensitivity to thermal cues during development. Predicting the consequences of climate change for these species, including skewed offspring sex ratios, depends on understanding how climatic factors interface with features of maternal nesting behaviour to shape the developmental environment. Here, we measure thermal profiles in 86 nests at two geographically distinct sites in the northern and southern regions of the American alligator's (Alligator mississippiensis) geographical range, and examine the influence of both climatic factors and maternally driven nest characteristics on nest temperature variation. Changes in daily maximum air temperatures drive annual trends in nest temperatures, while variation in individual nest temperatures is also related to local habitat factors and microclimate characteristics. Without any compensatory nesting behaviours, nest temperatures are projected to increase by 1.6-3.7°C by the year 2100, and these changes are predicted to have dramatic consequences for offspring sex ratios. Exact sex ratio outcomes vary widely depending on site and emission scenario as a function of the unique temperature-by-sex reaction norm exhibited by all crocodilians. By revealing the ecological drivers of nest temperature variation in the American alligator, this study provides important insights into the potential consequences of climate change for crocodilian species, many of which are already threatened by extinction.

Androgen and mineralocorticoid receptors are present on the germinal disc region in laying hens: Potential mediators of sex ratio adjustment in birds?

Female birds skew offspring sex ratios based on environmental and social stimuli; however, the mechanism mediating this phenomenon remains unknown. Growing evidence suggests that testosterone and corticosterone may influence meiosis, as they skew sex ratios when given immediately before chromosomal segregation. It is unclear if these hormones act on the germinal disc (GD) or through a downstream mediator. It is also unknown whether the GD contains receptors for these hormones. If testosterone and/or corticosterone act on the GD to skew sex ratios, then the GD should have receptors for them and that receptor levels should be higher in the GD regions compared to other follicular regions. Furthermore, fluctuations of receptor levels should occur near meiotic segregation. We collected ovarian follicles at 5 h pre-ovulation (just before meiotic segregation) and 20 h pre-ovulation (when sex chromosomes are arrested), and measured androgen receptor (AR) and mineralocorticoid receptor (MR) protein levels via Western blot. ARs and MRs were on the follicle in the GD and non-GD regions, and at 5 h and 20 h pre-ovulation. Both AR and MR protein levels were higher in the GD region than the non-GD region at both time points, but did not differ between time points. These results suggest that hen ovarian follicles have receptors for testosterone and corticosterone, and that the ability for testosterone to respond may be specifically higher in the GD-region, providing further support for the role of testosterone in the alteration of meiotic segregation.

Dispersal and climate warming determine range shift in model reptile populations

Average air temperature is predicted to rise by at least 3°C across the 21st century. As individual sex (male or female) is determined by temperature in many reptiles, there are concerns that climate warming will skew offspring sex ratios and local species extinctions will follow. Range shift away from hotter areas through dispersal may prevent species extinctions in many reptiles with temperature-dependent sex determination (TSD), and could be facilitated or impeded by sex-biased populations at the expanding edge. We used a simulation model to examine the role of sex-determining mechanism [TSD and genotypic sex determination (GSD)], climate warming and dispersal in determining range shift and population growth in reptiles. Dispersal influenced range shift (after climate warming) in TSD species to a greater extent than in GSD species. Our novel finding is that biased sex ratios may influence range shift, through the mixing of the rare sex (females) with males located at the colder range edges, as both sexes disperse. However, if faced with climate warming of 3°C over the next 100 years many TSD reptiles will show limited capacity for range shift.

Sons do not take advantage of a head start: parity in herring gull offspring sex ratios despite greater initial investment in males

Skewed adult sex ratios sometimes occur in populations of free‐living animals yet the proximate mechanisms, timing of sex‐biases, and the selective agents contributing to skew remain a source of debate with contradictory evidence from different systems. We investigated potential mechanisms contributing to sex biases in a population of herring gulls with an apparent female skew in the adult population. Theory predicts that skewed adult sex ratios will adaptively lead to skewed offspring sex ratios to restore balance in the effective breeding population. Parents may also adaptively bias offspring sex ratios to increase their own fitness in response to environmental factors. Therefore, we expected to detect skewed sex ratios either at hatching or at fledging as parents invest differentially in offspring of different sexes. We sampled complete clutches (n = 336 chicks) at hatching to quantify potential skews in sex ratios by position in the hatch order, time of season, year, and nesting context (nest density), finding no departure from equal sex ratios at hatching related to any of these factors. Further, we sampled 258 chicks at near‐fledging to investigate potential sex biases in survival at the chick stage. Again, no biases in sex ratios were recorded. Male offspring were favored in this population via greater maternal investment in eggs carrying male embryos and greater parental provisioning of male offspring which reached greater sizes by fledging. Despite the advantages realized by male offspring, females were equally as likely to fledge as males. Thus, biased adult sex ratios apparently arise in the post‐fledging and pre‐recruitment stage in our population.

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.

Acute Corticosterone Administration during Meiotic Segregation Stimulates Females to Produce More Male Offspring

Birds have demonstrated a remarkable ability to manipulate offspring sex. Previous studies suggest that treatment with hormones can stimulate females to manipulate offspring sex before ovulation. For example, chronic treatments with corticosterone, the primary stress hormone produced by birds, stimulated significant skews toward female offspring. It has been suggested that corticosterone acts by influencing which sex chromosome is donated by the heterogametic female bird into the ovulated ovarian follicle. However, it is difficult to pinpoint when in developmental time corticosterone affects offspring sex, because in previous studies corticosterone treatment was given over a long period of time. We treated laying hens with acute high-dose corticosterone injections 5 h before the predicted time of ovulation and quantified the sexes of the subsequently ovulated eggs to determine whether mechanisms exist by which corticosterone can skew offspring sex ratios just before ovulation. We hypothesized that an injection of corticosterone coincident with segregation of the sex chromosomes would stimulate hens to produce more female than male offspring. Contrary to our predictions, hens injected with corticosterone produced a significant bias toward male offspring, nearly 83%. These results suggest that acute corticosterone treatment during meiosis I can influence primary sex ratios in birds, potentially through nonrandom chromosome segregation. Furthermore, acute corticosterone exposure, compared with chronic exposure, may act through different mechanisms to skew offspring sex.

Breeding Periodicity for Male Sea Turtles, Operational Sex Ratios, and Implications in the Face of Climate Change

Species that have temperature-dependent sex determination (TSD) often produce highly skewed offspring sex ratios contrary to long-standing theoretical predictions. This ecological enigma has provoked concern that climate change may induce the production of single-sex generations and hence lead to population extirpation. All species of sea turtles exhibit TSD, many are already endangered, and most already produce sex ratios skewed to the sex produced at warmer temperatures (females). We tracked male loggerhead turtles (Caretta caretta) from Zakynthos, Greece, throughout the entire interval between successive breeding seasons and identified individuals on their breeding grounds, using photoidentification, to determine breeding periodicity and operational sex ratios. Males returned to breed at least twice as frequently as females. We estimated that the hatchling sex ratio of 70:30 female to male for this rookery will translate into an overall operational sex ratio (OSR) (i.e., ratio of total number of males vs females breeding each year) of close to 50:50 female to male. We followed three male turtles for between 10 and 12 months during which time they all traveled back to the breeding grounds. Flipper tagging revealed the proportion of females returning to nest after intervals of 1, 2, 3, and 4 years were 0.21, 0.38, 0.29, and 0.12, respectively (mean interval 2.3 years). A further nine male turtles were tracked for short periods to determine their departure date from the breeding grounds. These departure dates were combined with a photoidentification data set of 165 individuals identified on in-water transect surveys at the start of the breeding season to develop a statistical model of the population dynamics. This model produced a maximum likelihood estimate that males visit the breeding site 2.6 times more often than females (95%CI 2.1, 3.1), which was consistent with the data from satellite tracking and flipper tagging. Increased frequency of male breeding will help ameliorate female-biased hatchling sex ratios. Combined with the ability of males to fertilize the eggs of many females and for females to store sperm to fertilize many clutches, our results imply that effects of climate change on the viability of sea turtle populations are likely to be less acute than previously suspected.

Predicting the fate of a living fossil: how will global warming affect sex determination and hatching phenology in tuatara?

How will climate change affect species' reproduction and subsequent survival? In many egg-laying reptiles, the sex of offspring is determined by the temperature experienced during a critical period of embryonic development (temperature-dependent sex determination, TSD). Increasing air temperatures are likely to skew offspring sex ratios in the absence of evolutionary or plastic adaptation, hence we urgently require means for predicting the future distributions of species with TSD. Here we develop a mechanistic model that demonstrates how climate, soil and topography interact with physiology and nesting behaviour to determine sex ratios of tuatara, cold-climate reptiles from New Zealand with an unusual developmental biology. Under extreme regional climate change, all-male clutches would hatch at 100% of current nest sites of the rarest species, Sphenodon guntheri, by the mid-2080s. We show that tuatara could behaviourally compensate for the male-biasing effects of warmer air temperatures by nesting later in the season or selecting shaded nest sites. Later nesting is, however, an unlikely response to global warming, as many oviparous species are nesting earlier as the climate warms. Our approach allows the assessment of the thermal suitability of current reserves and future translocation sites for tuatara, and can be readily modified to predict climatic impacts on any species with TSD.

Is variation in brood sex ratios adaptive in the great tit (Parus major)?

Life-history theory predicts skewed offspring sex ratios in a range of situations in which the costs and benefits of producing the two sexes differ. In recent years, many studies have demonstrated biased sex ratios in a variety of bird species. However, many of these investigations have been based on small sample sizes, on data from a single year, or both. Using a recently developed polymerase chain reaction-based molecular DNA technique, 912 great tit (Parus major) nestlings from 118 broods in 5 different years were sexed. As found in a number of previous studies on the same species, there were significant predictors of offspring sex ratio in individual years. However, there were no consistent trends across years, and none of the measured variables significantly predicted sex ratio over all years combined. Furthermore, brood sex ratio of the population did not depart from the expected binomial distribution. Although there are theoretical advantages to manipulating the sex ratio in this and other species, the physiological mechanism by which it is achieved in birds remains obscure. We argue that data from several years are needed to confirm whether facultative sex ratio manipulation is a consistent breeding strategy used by birds.

Molecular Determination of Sex-Ratio in Yellowhammer Emberiza citrinella Offspring

Theory predicts skewed offspring sex-ratios in a range of situations in which the economics of producing the two sexes differ. Offspring sex-ratio skews in birds are relatively scarcely observed compared to other taxa. This could be because avian molecular sexing techniques, which allow young birds to be sexed, have only recently become available. Alternatively, birds may be largely constrained from adaptively manipulating the sex-ratio of their offspring. We used a recently-developed molecular sexing technique for birds to sex 420 Yellowhammer Emberiza citrinella offspring from 168 clutches found in Oxfordshire. Clutch sex-ratio of the population did not depart from the expected binomial distribution, and there was no variation in clutch sex-ratio with laying date, breeding attempt, or a variety of habitat variables which were predicted to differentially affect the survival and future reproductive success of offspring of the two sexes. There was no difference in size or growth rate of the sexes and nestling mortality was not sex-biased. Hence, although we can identify possible advantages of manipulating the sex-ratio in this species, it seems not to be used as a breeding strategy. Given the lack of consistent evidence for skewed avian offspring sex-ratios, more experimental work is required to determine whether, and how, birds may adaptively manipulate their offspring sex-ratio.

Skewed offspring sex ratios and sex composition of twin litters in Serengeti spotted hyaenas ( Crocuta crocuta) are a consequence of siblicide

Long-term data on the sex ratio among offspring and sex composition of litters in a population of several hundred individually known spotted hyaenas in the Serengeti National Park, Tanzania are presented. Females produced singleton or twin litters. The overall sex ratio (proportion of males) was unbiased at 0.52 ( n = 318) but masked significant deviations in opposite directions in litters of different size. Sex ratio in singleton litters was female biased at 0.43 ( n = 91 individuals, p = 0.07). The sex ratio in twin litters was significantly ( P < 0.05) male-biased at 0.56 ( n = 228 individuals); there were significantly too many mixed-sex and too few all-female twin litters. Three hypotheses are considered that may explain these sex ratio biases: (i) the primary sex ratio may be skewed, (ii) cub mortality may be female-biased, leading to the loss of more females than males, or (iii) the biases are due to siblicide. The first two hypotheses predicted the same sex ratio biases for both singleton and twin litters, while the third hypothesis predicted opposite trends for singleton and twin litters. The results are inconsistent with the two first hypotheses but support the third. The study suggests that the lack of all-female twin litters and the female bias amongst singletons is due to a higher incidence of siblicide in all-female twin litters than among mixed-sex or all-male twin litters. Siblicide is the major source of post-natal sex ratio biases to the age of independence in this population.

Mechanisms of Facultative Sex-Ratio Variation in Zebra Finches (Taeniopygia guttata)

The offspring sex ratio at independence in a colony of Zebra Finches (Tae- niopygia guttata) was significantly male biased. Three possible proximate causes of this bias were examined. (1) The first was that there is a sex-biased laying sequence followed by brood reduction. Males were significantly more likely to hatch from earlier-laid eggs than females, but there was no evidence of increased mortality among late-laid nestlings. (2) The second was that there is sex-biased mortality due to sex-specific growth rates. Male and female offspring had similar rates of mass increase, tarsus growth, and wing-chord growth. (3) The third was that there is sex-biased provisioning by one or both parents, increasing survival probabilities of preferred sex. There was evidence that males fed male-biased broods more frequently than female-biased broods. Fledging age, fledging mass, and the number of days to independence were similar for male and female offspring, suggesting that sex-biased provisioning had no significant biological effect. Although none of the hypotheses adequately explained the observed sex-ratio bias, results from this and other studies suggest that sex- biased laying sequences followed by brood reduction are most likely to cause skewed offspring sex ratios in nature. The implications of a sex-biased laying sequence and of sex-biased provisioning by the male are discussed in reference to the potential evolutionary conflict between males and females over control of offspring sex ratios. Received 5 October 1994, accepted 21 June 1995.

Adult male house mice born to undernourished mothers are unattractive to oestrous females

In some mammal species, females in poor condition (e.g. poor nutritional state) give birth to a lower proportion of sons than do females in good condition. These skewed offspring sex ratios may be adaptive, because poor maternal condition can have a strong negative impact on the success of sons at intra-sexual competition. However, there is little information about the impact of maternal condition on the success of sons at being chosen as mates. Female house mice, Mus musculus, that are undernourished during gestation give birth to a lower proportion of sons, and those sons are smaller as adults than of well-nourished females. The preferences of oestrous females for the odours of adult sons of females that were well nourished and of those that were undernourished during gestation were tested, as well as the preferences of females for the odours of heavy and light males. Oestrous females preferred the odours of sons of well-nourished females and of heavier males. Hence, the sons of undernourished females may not be chosen as mates as often and may have lower reproductive potential than the sons of well-nourished females. These results and other evidence suggest that the skewed secondary sex ratios of undernourished female mice are adaptive.

Effects of age and parity on litter size and offspring sex ratio in golden hamsters (Mesocricetus auratus).

Golden hamsters that were mated repeatedly from 55 days of age produced 6-12 litters. Litter size at birth rose between the 1st and 2nd litters, peaked on the 3rd, and declined steadily after the 5th litter. Offspring sex ratio (% male) at birth followed a similar pattern: increasing between the 1st and 2nd litters, remaining high through the 3rd, and becoming increasingly female-biased thereafter. Weaning success decreased sharply after the 6th litter and most dams failed to raise any young to weaning after the 9th litter. These sequential effects on litter size, offspring sex ratio and weaning success were also observed in females mated once at different ages, but they occurred considerably later in life, i.e. increasing parity hastened the effects of advanced age. These age- and parity-related changes in litter composition are consistent with the Trivers-Willard hypothesis that physiologically-stressed females would skew offspring sex ratios to favour daughters. However, since the observed changes in sex ratio were probably due to differential prenatal mortality, their adaptive significance is unclear.