Climate effects on offspring sex ratio in a viviparous lizard

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

Influence of time of insemination relative to ovulation and frequency of insemination on gilt fertility

The objectives of this study were to determine the optimal time of insemination in the pre-ovulatory period (from 32 to 0 h before ovulation) and to evaluate once-daily versus twice-daily inseminations in gilts. In Experiment 1, pre-puberal gilts (n=102) were observed for estrus every 8h and ultrasonography was performed every 8h from the onset of estrus to confirmation of ovulation. The gilts were inseminated once with 4 x 10(9) spermatozoa at various intervals prior to ovulation. Pregnancy detection was conducted 24 days after AI and gilts were slaughtered 4-6 days later. Corpora lutea and the number of viable embryos were counted and the embryo recovery rate was calculated (based on the percentage of corpora lutea). Inseminations performed <24h before ovulation resulted in a higher embryo recovery rate (P=0.02) and produced 2.1 more embryos (P=0.01) than inseminations >or=24h before ovulation. However, the pregnancy rate was reduced when inseminations were performed >16 h before ovulation (P=0.08). In Experiment 2, pre-puberal gilts (n=105) were observed for estrus every 12h and ultrasonography was performed every 12h from the onset of estrus to confirmation of ovulation. Gilts were inseminated (with 4 x 10(9) spermatozoa) 12h after the onset of estrus, with inseminations repeated either every 12h (twice-daily) or 24h (once-daily) during estrus. The gilts were allowed to farrow. There were no differences (between gilts bred twice-daily versus once-daily) for return to estrus rate (P=0.36) and adjusted farrowing rate (P=0.19). However, gilts inseminated once-daily had 1.2 piglets less than those inseminated twice-daily (P=0.09). In conclusion, gilts should be inseminated up to 16 h before ovulation, as intervals >16 h reduced pregnancy rate and litter size.     

Relationship between sex ratio and time of insemination according to both time of ovulation and maturational state of oocyte

The aim of this study was to explore how some reproductive methodologies may affect the sex ratio. We first confirmed the association between the maturation stage of bovine oocytes at the time of in vitro fertilisation (IVF) and the sex ratio of in vitro-derived embryos. Secondly, we studied whether the time of insemination, prior to or after ovulation, could alter the sex ratio in sheep. In the first experiment, bovine oocytes were matured in vitro for 16 h; then oocytes were either fertilised in vitro immediately after extrusion of the first polar body or IVF was delayed for 8 h. The proportion of cleaving embryos and their development to the 8-cell stage was enhanced with delayed insemination. Moreover, delaying IVF produced a male-to-female sex ratio of 1.67:1.00, which was significantly different from the expected 1:1 ratio (p < 0.05), whereas more female embryos were produced when oocytes were fertilised in vitro immediately after polar body extrusion (sex ratio of 1.00:0.67; p < 0.05). In the second experiment, 380 ewes were inseminated at different times before or after ovulation, producing 537 lambs. Significant differences in the sex ratio were obtained when we compared the sex of the offspring of ewes inseminated during the 5 h preceding ovulation (more females) with those inseminated during the 5 h after ovulation (more males). Our results suggest that the differential ability of X- or Y-bearing spermatozoa to fertilise oocytes depending either on time of insemination or oocyte maturation state, may be due, at least partially, to 'intrinsic' differences in the physiological activity of X- or Y-bearing spermatozoa before fertilisation.     

2nd to 4th digit ratio and offspring sex ratio

There is evidence that the ratio of the length of the 2nd and 4th digit (2D:4D) is negatively related to prenatal and adult concentrations of testosterone. It has also been reported that high levels of testosterone at conception in both fathers and mothers are associated with an increased sex ratio (proportion of males at birth). It follows from these observations that low values of 2D:4D may be related to high sex ratio. We present evidence from three populations (English, Spanish and Jamaican) that 2D:4D is negatively related to sex ratio, independent of the sex and ethnicity of the parents.     

Effect of timing of artificial insemination on sex ratio

For a number of years, the time of insemination or mating during estrus has been believed to influence the sex ratio of offspring, with early insemination resulting in more females and late insemination, more males. Possible mechanisms of altering the sex ratio include facilitating or inhibiting the transport of either X- or Y-chromosome-bearing sperm through the reproductive tract, preferential selection of sperm at fertilization, or sex-specific death of embryos after fertilization. In livestock species, there is evidence for preferential selection of X- or Y-bearing sperm, based on the maturational state of the oocyte at fertilization. In deer and sheep, early and late insemination appears to skew the sex ratio toward females and males, respectively. In cattle, conflicting reports on the effect of time of insemination on sex ratio make the premise less clear. Many of the published studies lack adequate observations for definitive conclusions and/or are based on infrequent observations of estrus, making it difficult to assess the effect of time of insemination on sex ratio. It is likely that any effect of time of insemination on sex ratio in cattle is relatively small. Evidence is accumulating that treatments used for synchronization of estrus or ovulation in cattle may influence the sex ratio.     

Effect of sperm numbers and time of insemination relative to ovulation on sow fertility

We examined the effect of inseminating mixed parity sows (n = 231) once with fewer sperm at different times relative to ovulation. Lactation length was 19 days and sows received an IM injection of 600 IU equine chorionic gonadotrophin (eCG) 12 h before weaning. At 80 h after eCG injection, sows received an IM injection of 5 mg porcine luteinizing hormone (pLH). Predicted time of ovulation (PTO) was 38 h after pLH injection. Sows were assigned by parity to receive a single transcervical artificial insemination (AI) at either 6 or 24 h before PTO with semen doses containing either 2.5 or 1.25 × 10⁹ sperm. A positive control group of sows (n = 49) was subject to conventional AI 24 and 6 h before PTO. Detection of estrus was performed in the presence of a boar and only sows exhibiting estrous behavior at the assigned time of AI were included in the study. Farrowing rate for sows receiving 2.5 × 10⁹ sperm at 6 h before PTO was greater than that for sows receiving 1.25 × 10⁹ sperm at 24 h before PTO (85% versus 61%, P < 0.05). All other groups were intermediate. There was no effect of time of AI or sperm numbers on subsequent litter size. These data indicate that single insemination of fewer sperm may compromise sow fertility, even when performed transcervically, if not appropriately timed relative to ovulation.     

Birds bias offspring sex ratio in response to livestock grazing

Livestock grazing, which has a large influence on habitat structure, is associated with the widespread decline of various bird species across the world, yet there are few experimental studies that investigate how grazing pressure influences avian reproduction. We manipulated grazing pressure using a replicated field experiment, and found that the offspring sex ratio of a common upland passerine, the meadow pipit Anthus pratensis, varied significantly between grazing treatments. The proportion of sons was lowest in the ungrazed and intensively grazed treatments and highest in treatments grazed at low intensity (by sheep, or a mixture of sheep and cattle). This response was not related to maternal body condition. These results demonstrate the sensitivity of avian reproductive biology to variation in local conditions, and support growing evidence that too much grazing, or the complete removal of livestock from upland areas, is detrimental for common breeding birds.     

Effect of time of insemination relative to ovulation on fertility with liquid and frozen boar semen

Precise data on fertility results following peri- and postovulatory insemination in spontaneously ovulating gilts is lacking. Using transcutaneous sonography every 4 h during estrus as a tool for diagnosis of ovulation, the effects of different time intervals of insemination relative to ovulation were investigated with liquid semen (Experiment 1, n=76 gilts) and frozen semen (Experiment 2, n=80 gilts). In Experiment 3 (n=24 gilts) the number of Day-28 embryos related to the various intervals between insemination and ovulation was determined after the use of liquid semen. Using liquid semen the fertilization rates based on Day-2 to Day-5 embryos and the number of accessory spermatozoa decreased significantly in gilts inseminated with 2 x 10(9) spermatozoa per dosage in intervals of more than 12 h before or more than 4 h after ovulation. In the time interval 4 to 0 h before ovulation, comparable fertilization rates were obtained using frozen semen (88.1%) and liquid semen (92.5%). Fertilization rates and numbers of accessory spermatozoa decreased significantly when gilts were inseminated with frozen semen more than 4 h before or 0 to 4 h after the detection of ovulation. The percentage of Day-28 embryos was significantly higher following preovulatory insemination compared to inseminations 0 to 4 h and 4 to 8 h after ovulation. It is concluded that the optimal time of insemination using liquid semen is 12 to 0 h before ovulation, and 4 to 0 h before ovulation using frozen semen. The results stress the importance of further research on sperm transport and ovulation stimulating mechanisms, as well as studies on the time of ovulation relative to estrus-weaning intervals and estrus duration.     

Do females adjust the sex of their offspring in relation to the breeding sex ratio?

When the adult sex ratio differs between years in local populations, but still is predictable between adjacent years, it has been proposed that the best strategy would be to bias the offspring sex ratio in favour of the rare sex. We tested this hypothesis using a data set of great reed warbler offspring, sexed by molecular techniques, that were collected over 11 breeding seasons at two adjacent reed marshes. Three important assumptions for this hypothesis are fulfilled in the studied great reed warbler population. First, a substantial proportion of great reed warblers are living in small local populations where sex ratio distortions would be sufficiently large and common. Second, breeding adults and their offspring return to breed in the local population to a high degree. Third, females have a possibility to assess the breeding sex ratio before laying their eggs. At our study site, the breeding sex ratio was positively correlated between successive years. However, contrary to our prediction, female great reed warblers seemed not to adjust their offspring sex ratio in relation to the local breeding sex ratio.     

Effect of time of artificial insemination on embryo sex ratio in dairy cattle

The objective of the present study was to examine whether different intervals between insemination and ovulation have an influence on the sex of seven-day-old embryos in dairy cattle. Cows were inseminated once with semen of one of two bulls of proven fertility between 36 h before ovulation and 12 h after ovulation. Time of ovulation was assessed by ultrasound at 4-h intervals. In total, 64 embryos were determined to be male or female. Of these 64 embryos, 51.6% were female. The sex ratio in the various insemination-ovulation intervals (early: between 36 and 20 h before ovulation; intermediate: between 20 and 8 h before ovulation; late: between 8 h before and 12 h after ovulation) did not significantly differ from the expected 1:1 sex ratio (50, 50 and 55% females, respectively). Bull (Bull A and B) and Parity (primiparous and multiparous) had no influence on the expected 1:1 sex ratio either. The number of cell cycles was similar for male and female (P = 0.23) embryos when quality of the embryo (P < 0.0001) was included in the model. The results of this study indicate that, in cattle, the interval between insemination and ovulation does not influence the sex ratio of seven-day-old embryos.     

Ecological and phenological covariates of offspring sex ratio in barn swallows

Non-random sex allocation in relation to parental, ecological and phenological factors has been investigated in several correlational studies of birds, mostly based on few breeding seasons and relatively small sample sizes, which have led to different results. We investigated sex ratio of nestling barn swallows (Hirundo rustica) in relation to adult sex ratio, laying date, clutch size, colony size and meteorological conditions in a sample of 553 broods (>2200 nestlings) during 10 years. At the population level, nestling sex ratio varied among years and deviated from parity in two years. Sex ratio among adults did not predict offspring sex ratio in the current or the following year. At the within-family level, the proportion of sons increased with laying date in large clutches, did not vary among clutches of intermediate size, and tended to decline with laying date in small clutches. Large colonies harbored more sons. The proportion of males increased with temperature during laying whereas the effects of temperature during the pre- or post-laying periods and that of rainfall were non-significant. These patterns of variation of offspring sex ratio did not differ between years. Thus, we identified several potential causal sources of variation in barn swallow offspring sex ratio, including temporal, phenological and ecological factors. The observation of an association of offspring sex with temperature during laying is novel for birds and may be mediated by effects on maternal steroid hormones profile. The ecological and evolutionary implications of present findings are discussed in the light of adaptive sex allocation theory.     

Manipulation of offspring sex ratio by second-mated female house wrens

In 1973, Trivers and Willard proposed that offspring sex ratio should be associated with the quality of parental care likely to be provided to the offspring. We tested this hypothesis by comparing fledgling sex ratios in nests of first- and second-mated female house wrens (Troglodytes aedon). In our Wyoming population, second-mated females typically receive little or no male parental assistance and fledge fewer and lower-quality young compared with first-mated females. Assuming that being of lower quality has stronger negative effects on the future reproductive success of males than that of females in this polygynous population, we predicted that fledgling sex ratios in the nests of second-mated females would be female-biased compared with the fledgling sex ratios of first-mated females. Additionally, we asked whether any sex bias at fledging could have resulted from male-biased nestling mortality caused by sex-biased parental provisioning. As predicted, mean fledgling sex ratios in nests of second-mated females were more female-biased than fledgling sex ratios in nests of first-mated females. However, we found no evidence of either sex-biased nestling mortality or sex-biased parental provisioning. These findings suggest that females are responding to their status as second-mated females and to the associated low-quality parental care that their young are likely to receive by producing female-biased clutches rather than manipulating the offspring sex ratio through sex-biased nestling mortality.     

Maternal diet and other factors affecting offspring sex ratio: a review

Mammals usually produce approximately equal numbers of sons and daughters, but there are exceptions to this general rule, as has been observed in ruminant ungulate species, where the sex-allocation hypothesis of Trivers and Willard has provided a rational evolutionary underpinning to adaptive changes in sex ratio. Here, we review circumstances whereby ruminants and other mammalian species, especially rodents and primates, appear able to skew the sex ratio of their offspring. We also discuss some of the factors, both nutritional and nonnutritional, that potentially promote such skewing. Work from our laboratory, performed on mice, suggests that age of the mother and maternal diet, rather than the maternal body condition per se, play directive roles in controlling sex ratio. In particular, a diet high in saturated fats but low in carbohydrate leads to the birth of significantly more male than female offspring in mature laboratory mice, whereas when calories are supplied mainly in the form of carbohydrate rather than fat, daughters predominate. As the diets fed to the mice in these experiments were nutritionally complete and because litter sizes did not differ between treatments, dietary inadequacy seems not to be the cause for sex-ratio distortion. A number of mechanisms, all of which are testable, are discussed to provide an explanation for the phenomenon. We conclude the review by discussing potential implications of these observations to human medicine and agriculture.     

Variable variation: annual and seasonal changes in offspring sex ratio in a bat

Many organisms produce offspring with sex-ratios that deviate from equal numbers of males and females, and numerous adaptive explanations have been proposed. In some species, offspring sex-ratio varies across the reproductive season, again with several explanations as to why this might be adaptive. However, patterns for birds and mammals are inconsistent, and multiple factors are likely involved. Long-term studies on a variety of species may help untangle the complexity. I analyzed a long-term data set on the variation in offspring sex-ratio of the big brown bat, Eptesicus fuscus, a temperate-zone, insectivorous species. Sex ratio varied seasonally, but only in some years. Births early in the season were significantly female biased in years in which parturition occurred relatively early, but not in years with late parturition. Survival of female pups increased with earlier median birth date for the colony, and early-born females were more likely to survive and reproduce as one-year olds, compared to later-born pups. I argue that, due to the unusual timing of reproductive activities in male and female bats that hibernate, producing female offspring early in the year increases their probability of reproducing as one year olds, but this is not the case for male offspring. Thus, mothers that can give birth early in the year, benefit most by producing a female pup. The relative benefit of producing female or male offspring varies depending on the length of the growing season and thus the time available for female pups to reach sexual maturity. This suggests that not only does sex-ratio vary seasonally and among years, depending on the condition of the mother and the environment, but also likely varies geographically due to differences in season length.     

Male phenotypic quality influences offspring sex ratio in a polygynous ungulate

Evolutionary models of sex ratio adjustment applied to mammals have ignored that females may gain indirect genetic benefits from their mates. The differential allocation hypothesis (DAH) predicts that females bias the sex ratio of their offspring towards (more costly) males when breeding with an attractive male. We manipulated the number of available males during rut in a polygynous ungulate species, the reindeer (Rangifer tarandus), and found that a doubling of average male mass (and thus male attractiveness) in the breeding herd increased the proportion of male offspring from approximately 40 to 60%. Paternity analysis revealed indeed that males of high phenotypic quality sired more males, consistent with the DAH. This insight has consequences for proper management of large mammal populations. Our study suggests that harvesting, by generating a high proportion of young, small and unattractive mates, affects the secondary sex ratio due to differential allocation effects in females. Sustainable management needs to consider not only the direct demographic changes due to harvest mortality and selection, but also the components related to behavioural ecology and opportunities for female choice.     

Pollinating fig wasp Ceratosolen solmsi adjusts the offspring sex ratio to other foundresses

Abstract Local mate competition theory predicts that offspring sex ratio in pollinating fig wasps is female‐biased when there is only one foundress, and increased foundress density results in increased offspring sex ratio. Information of other foundresses and clutch size have been suggested to be the main proximate explanations for sex ratio adjustment under local mate competition. Our focus was to show the mechanism of sex ratio adjustment in a pollinating fig wasp, Ceratosolen solmsi Mayr, an obligate pollinator of the functionally dioecious fig, Ficus hispida Linn., with controlled experiments in the field. First, we obtained offspring from one pollinator and offspring at different oviposition sequences, and found that offspring sex ratio decreased with clutch size, and pollinators produced most of their male offspring at the start of bouts, followed by mostly females. Second, we found that offspring sex ratio increased with foundress density, and pollinators did adjust their offspring sex ratio to other females in the oviposition patches. We suggest that when oviposition sites are not limited, pollinators will mainly adjust their offspring sex ratio to other foundresses independent of clutch size changes, whereas adjusting clutch size may be used to adjust sex ratio when oviposition sites are limited.