Primary sex ratio bias in an endangered cooperatively breeding bird, the Black-eared Miner, and its implications for conservation

The aim of our study was to investigate primary and adult sex ratios in the cooperatively breeding black-eared miner, Manorina melanotis. We used genetic methods to determine the sex of all birds. Observations were made to quantify differences in helping behaviour between the sexes. As in other miners, Manorina spp., non-breeding males provided most of the help in raising young. Male and female nestlings did not differ significantly in weight, suggesting that both sexes are equally costly to produce. Like other miners, the adult sex ratio in black-eared miners is male-biased (64.4%). However, unlike its congeners, the black-eared miner’s primary sex ratio was strongly biased toward females (62.5%). This suggests that females suffer higher juvenile mortality than males. Our study illustrates how understanding sex ratios is both of theoretical interest and relevant to biological conservation.

Breeding ecology and bias in offspring sex ratio in little grassbirds (Megalurus gramineus)

Little grassbirds (Megalurus gramineus) are small, sexually monomorphic passerines that live in reed beds, lignum swamps and salt marshes in southern Australia. The breeding biology and patterns of sex allocation of the little grassbird were investigated over a single breeding season. Our observations of this species in the Edithvale Wetland Reserve revealed a highly male-biased population sex ratio, with some breeding territories containing several additional males. Nevertheless, there was little compelling evidence that little grassbirds breed cooperatively. The growth rates of male and female nestlings were similar and, as predicted by theory, there was no overall primary sex ratio bias. However, the primary sex ratio was female-biased early in the breeding season and became increasingly male-biased later in the breeding season.

Maternal stress to partner quality is linked to adaptive offspring sex ratio adjustment

Female birds have been shown to have a remarkable degree of control over the sex ratio of the offspring they produce. However, it remains poorly understood how these skews are achieved. Female condition, and consequent variation in circulating hormones, provides a plausible mechanistic link between offspring sex biases and the environmental and social stresses commonly invoked to explain adaptive sex allocation, such as diet, territory quality, and body condition. However, although experimental studies have shown that female perception of male phenotype alone can lead to sex ratio biases, it is unknown how partner quality influences female physiological state. Using a controlled within-female experimental design where female Gouldian finches (Erythrura gouldiae) bred with both high- and low-quality males, we found that partner quality directly affects female hormonal status and subsequent fitness. When constrained to breeding with low-quality males, females had highly elevated stress responses (corticosterone levels) and produced adaptive male-biased sex ratios, whereas when they bred with high-quality males, females had low corticosterone levels and produced an equal offspring sex ratio. There was no effect of other maternal hormones (e.g., testosterone) or body condition on offspring sex ratios. Female physiological condition during egg production, and variation in circulating hormones in particular, may provide a general mechanistic route for strategic sex allocation in birds.

Little evidence that condition, stress indicators, sex ratio, or homozygosity are related to landscape or habitat attributes in declining woodland birds

Habitat loss, fragmentation and degradation are drivers of major declines in biodiversity and species extinctions. The actual causes of species population declines following habitat change are more difficult to discern and there is typically high covariation among the measures used to infer the causes of decline. The causes of decline may act directly on individual fitness and survival, or through disruption of population processes. We examined the relationships among configuration, extent and status of native vegetation and three commonly used indicators of individual body condition and chronic stress (haemoglobin level, haematocrit, residual body mass condition index) in 13 species of woodland-dependent birds in south-eastern Australia. We also examined two measures of changes to population processes (sex ratio and individual homozygosity) in ten species and alleic richness in five species. We found little support for relationships between site or landscape characteristics and individual or population response variables, notwithstanding that our simulations showed we had sufficient power to detect relatively small effects. We discuss possible causes of the absence of detectable habitat effects in this system and the implications for the usefulness of individual body condition and easily measured haematological indices as indicators of the response of avian populations to habitat change. © 2012 The Authors.

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.

Different male vs. female breeding periodicity helps mitigate offspring sex ratio skews in sea turtles

 The implications of climate change for global biodiversity may be profound with those species with little capacity for adaptation being thought to be particularly vulnerable to warming. A classic case of groups for concern are those animals exhibiting temperature-dependent sex-determination (TSD), such as sea turtles, where climate warming may produce single sex populations and hence extinction. We show that, globally, female biased hatchling sex ratios dominate sea turtle populations (exceeding 3:1 in >50% records), which, at-a-glance, reiterates concerns for extinction. However, we also demonstrate that more frequent breeding by males, empirically shown by satellite tracking 23 individuals and supported by a generalized bio-energetic life history model, generates more balanced operational sex ratios (OSRs). Hence, concerns of increasingly skewed hatchling sex ratios and reduced population viability are less acute than previously thought for sea turtles. In fact, in some scenarios skewed hatchling sex ratios in groups with TSD may be adaptive to ensure optimum OSRs.

Inheritance of molecular markers and sex in the Australian freshwater crayfish, Cherax destructor Clark

Inheritance of three kinds of molecular genetic markers (mtDNA, random-amplified polymorphic DNAs (RAPDs) and allozymes) and sex were investigated in crossbreeding experiments between three populations of the Australian freshwater crayfish Cherax destructor. Crossbreeding did not disrupt the ively maternally inherited, and allozyme and RAPD markers were transmitted following expected Mendelian principles for co-dominant and dominant traits respectively. Unlike these three markers, sex ratios were found to be distorted by crossbreeding in some families. Two crossbred families produced only females. The implications of these findings for freshwater crayfish population genetics, taxonomy and aquaculture are discussed.

Sex-specific developmental plasticity in response to yolk corticosterone in an oviparous lizard

Corticosterone exposure during prenatal development as a result of maternal upregulation of circulating hormone levels has been shown to have effects on offspring development in mammals. Corticosterone has also been documented in egg yolk in oviparous vertebrates, but the extent to which this influences phenotypic development is less studied. We show that maternal corticosterone is transferred to egg yolk in an oviparous lizard (the mallee dragon, Ctenophorus fordi Storr), with significant variation among clutches in hormone levels. Experimental elevation of yolk corticosterone did not affect hatching success, incubation period or offspring sex ratio. However, corticosterone did have a sex-specific effect on skeletal growth during embryonic development. Male embryos exposed to relatively high levels of corticosterone were smaller on average than control males at hatching whereas females from hormone-treated eggs were larger on average than control females. The data thus suggest that males are not just more sensitive to the detrimental effects of corticosterone but rather that the sexes may have opposite responses to corticosterone during development. Positive selection on body size at hatching for both sexes in this species further suggests that increased corticosterone in egg yolk may have sex-specific fitness consequences, with potential implications for sex allocation and the evolution of hormone-mediated maternal effects.

Mothers adjust offspring sex to match the quality of the rearing environment

Theory predicts that mothers should adjust offspring sex ratios when the expected fitness gains or rearing costs differ between sons and daughters. Recent empirical work has linked biased offspring sex ratios to environmental quality via changes in relative maternal condition. It is unclear, however, whether females can manipulate offspring sex ratios in response to environmental quality alone (i.e. independent of maternal condition). We used a balanced within-female experimental design (i.e. females bred on both low- and high-quality diets) to show that female parrot finches (Erythrura trichroa) manipulate primary offspring sex ratios to the quality of the rearing environment, and not to their own body condition and health. Individual females produced an unbiased sex ratio on high-quality diets, but over-produced sons in poor dietary conditions, even though they maintained similar condition between diet treatments. Despite the lack of sexual size dimorphism, such sex ratio adjustment is in line with predictions from sex allocation theory because nutritionally stressed foster sons were healthier, grew faster and were more likely to survive than daughters. These findings suggest that mothers may adaptively adjust offspring sex ratios to optimally match their offspring to the expected quality of the rearing environment.

Sex reversal in Nile tilapia (Oreochromis niloticus Linnaeus) by androgen immersion

Two experiments were conducted to investigate the efficacy of three androgens applied through immersion treatments on the sex ratio of Nile tilapia (Oreochromis niloticus L.) fry. In experiment 1, 14 days post-hatching (DPH) larvae were exposed to a single immersion treatment in 17α-methyltestosterone (MT), 17α-methyldihydrotestosterone (MDHT) or 17α-ethynyltestosterone (ET) at 200, 600 and 1800 μg L⁻¹ over 4 h (130 larvae per treatment). In experiment 2, Nile tilapia larvae were exposed to the higher androgen concentration (1800 μg L⁻¹) applied as either a single immersion (14 DPH) or double immersion (10 and 14 DPH) over 4 h (125 larvae per treatment). Change in sex proportion within each experiment as well as between experiments was analysed by the chi-square test. In experiment 1, MT, MDHT and ET were equally effective in significantly increasing the proportion of males when applied at 1800 μg L⁻¹ (86.0%, 90.0% and 86.7% respectively). At 200 μg L⁻¹ none of the androgens altered sex ratio. At 600 μg L⁻¹, only MDHT slightly, but significantly skewed the sex ratio towards males (73.0%). In experiment 2, a single immersion treatment at 14 DPH (1800 μg L⁻¹) significantly increased the proportion of males, but at this time the response was significantly hormone dependent (MDHT, 100.0%; MT, 91.6%; ET, 76.9%). When compared with a single immersion, two-immersion treatments significantly increased the proportion of males in the MT-treated group (from 91.6% to 98.3%), decreased the proportion of males in the MDHT group (from 100.0% to 93.4%) and had no significant effect the ET-treated group (change from 76.9% to 82.5%). The overall comparison of the sex ratio among same treatments from different experiments (a single immersion in 1800 μg L⁻¹) was not significantly different.

Temperature-dependent sex determination of Ascension Island green turtles

We examined the role played by temperature in the duration of incubation and sex ratio of green turtle hatchlings at Ascension Island, one of the most important green turtle rookeries in the Atlantic. Temperature at control sites at nest depth and in 39 green turtle nests was measured using small temperature recording devices. The sex ratio of hatchlings was ascertained in a sub-sample of monitored nests allowing the description of the relationship between intranest temperature and hatchling sex ratio, demonstrating a pivotal incubation temperature of 28.8°C. The seasonal profile in sex ratio of hatchlings produced on all nesting beaches at Ascension Island was estimated, showing that a female-biased sex ratio would be expected with a female:male ratio of the order of 3:1. The use of nest temperature, air temperature, sand temperature at control sites, and incubation duration as proxies to estimate hatchling sex ratio are discussed.

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.

Retracted: Experimental evidence that maternal corticosterone controls adaptive offspring sex ratios

1. Sex allocation theory has received considerable attention, yet the mechanism(s) by which mothers skew offspring sex ratios remain unknown. In birds, females are the heterogametic sex, which potentially gives them control of whether gametes will be male or female. How females might control the sex of the gamete is unclear, but one possibility is that variation in steroid hormones may mediate this process. 2. We experimentally altered circulating levels of corticosterone in female Gouldian finches (Erythrura gouldiae), a species that demonstrates both extreme stress responses and extreme offspring sex ratio biases when breeding with a low-quality (genetically incompatible) partner. 3. During egg production, individual females received both corticosterone and metyrapone (a corticosterone-synthesis inhibitor) implants, in random order, to induce both high and low levels of circulating stress hormones (within physiological limits). 4. We found that females with elevated corticosterone levels produced male-biased sex ratios, but when the same females were treated with metyrapone they produced female-biased offspring sex ratios. 5. These stress responses are adaptive because females constrained to breeding with low-quality males can substantially increase their fitness by overproducing sons. Changes in maternal corticosterone levels during stressful situations, such as the quality of a breeding partner, may provide an endocrine mechanism that can be exploited for strategic sex allocation.

Sex as a determinant of relapse incidence and progressive course of multiple sclerosis

The aim of this work was to evaluate sex differences in the incidence of multiple sclerosis relapses; assess the relationship between sex and primary progressive disease course; and compare effects of age and disease duration on relapse incidence. Annualized relapse rates were calculated using the MSBase registry. Patients with incomplete data or <1 year of follow-up were excluded. Patients with primary progressive multiple sclerosis were only included in the sex ratio analysis. Relapse incidences over 40 years of multiple sclerosis or 70 years of age were compared between females and males with Andersen-Gill and Tweedie models. Female-to-male ratios stratified by annual relapse count were evaluated across disease duration and patient age and compared between relapse-onset and primary progressive multiple sclerosis. The study cohort consisted of 11 570 eligible patients with relapse-onset and 881 patients with primary progressive multiple sclerosis. Among the relapse-onset patients (82 552 patient-years), 48 362 relapses were recorded. Relapse frequency was 17.7% higher in females compared with males. Within the initial 5 years, the female-to-male ratio increased from 2.3:1 to 3.3:1 in patients with 0 versus ≥4 relapses per year, respectively. The magnitude of this sex effect increased at longer disease duration and older age (P < 10−12). However, the female-to-male ratio in patients with relapse-onset multiple sclerosis and zero relapses in any given year was double that of the patients with primary progressive multiple sclerosis. Patient age was a more important determinant of decline in relapse incidence than disease duration (P < 10−12). Females are predisposed to higher relapse activity than males. However, this difference does not explain the markedly lower female-to-male sex ratio in primary progressive multiple sclerosis. Decline in relapse activity over time is more closely related to patient age than disease duration.