Sex Ratio In Response Research Articles

A possible case of offspring sex manipulation as result of a biased adult sex ratio

Although random meiosis should prevent the facultative adjustment of offspring sex ratio, theory predicts that females should produce more of the sex with the higher reproductive value. We reported a case of offspring sex ratio manipulation in grass wrens Cistothorus platensis. Males in better body condition would have higher reproductive value than females due to the potential for social polygyny and extra-pair fertilizations. On the other hand, local demography influences reproductive strategies in grass wrens as male abundance affects both social polygyny and extra-pair paternity frequencies. We evaluated whether females bias their brood sex ratio in response to adult sex ratio and nestling body condition (a proxy for female’s prospects of producing high-quality males). Females raised more male offspring when males were less abundant in the population (female-biased adult sex ratio). However, we found no relationship between nestling body condition and brood sex ratio, suggesting that females did not bias the brood sex ratio towards males when able to raise nestlings in better body condition. Taken together, our results provide the first suggestive evidence that female birds can manipulate their offspring sex ratio in response to the adult sex ratio.

Reproductive plasticity in response to the changing cluster size during the breeding period: a case study in a spider mite

Animals living in clusters should adjust their reproductive strategies to adapt to the social environment. Theories predict that the benefits of cluster living would outweigh the costs of competition. Yet, it is largely unknown how animals optimize their reproductive fitness in response to the changing social environment during their breeding period. We used Tetranychus ludeni Zacher, a haplodiploid spider mite, to investigate how the ovipositing females modified their life-history traits in response to the change of cluster size (i.e., aggregation and dispersal) with a consistent population density (1 ♀/cm2). We demonstrate that (1) after females were shifted from a large cluster (16 ♀♀) to small ones (1 ♀, 5 and 10 ♀♀), they laid fewer and larger eggs with a higher female-biased sex ratio; (2) after females were shifted from small clusters to a large one, they laid fewer and smaller eggs, also with a higher female-biased sex ratio, and (3) increasing egg size significantly increased offspring sex ratio (% daughters), but did not increase immature survival. The results suggest that (1) females fertilize more larger eggs laid in a small population but lower the fertilization threshold and fertilize smaller eggs in a larger population, and (2) the reproductive adjustments in terms of egg number and size may contribute more to minimize the mate competition among sons but not to increase the number of inhabitants in the next generation. The current study provides evidence that spider mites can manipulate their reproductive output and adjust offspring sex ratio in response to dynamic social environments.

Dietary yolk supplements and rate of yolk deposition do not influence sex ratios in Japanese Quail.

Birds appear to have the ability to bias offspring sex ratios in response to environmental and social conditions. The mechanisms responsible remain unknown, however one previous study indicated a link between rates of ovarian follicle growth and the sexes of resulting eggs. This could indicate that either follicles destined to retain male or female follicles grow at different rates, or the rate of ovarian follicle growth determines the sex chromosome that will be retained to influence the sex of the resulting offspring. We tested for evidence of both possibilities by staining yolk rings that are indicative of daily growth. First, we tested for a correlation between the number of yolk rings and the sexes of the resulting germinal discs collected from each egg, and second, we tested whether experimentally decreasing follicle growth rates with a dietary yolk supplement impacts the sexes of the resulting germinal discs. There was no significant correlation between the number of yolk rings and the sexes of the resulting embryos, and decreasing follicle growth rates did not impact sexes of resulting germinal discs. These results indicate that offspring sex is not related to the rate of ovarian follicle growth in quail.

Identifying factors affecting captive breeding success in a critically endangered species

ABSTRACT Captive breeding programs are an increasingly important tool for species’ conservation efforts, but not all species reproduce well in captivity. Identifying factors that affect the reproductive success of captive populations is crucial to improving the performance and management of conservation-breeding programs, both by providing individuals for release and informing decision making. We examined breeding records collected from the long-running conservation-breeding program for the critically endangered Orange-bellied Parrot Neophema chrysogaster over an 11-year period. We examined egg hatching rate, nestling survival rate, and offspring sex ratio in response to a wide range of variables related to characteristics of individual birds, breeding events, and the captive environment. The hatch rate of eggs was higher in first clutches compared to second clutches and was lower than the wild population. The survival rate of nestlings through to fledging was variable between years but became higher and more consistent over the last five years of the study period. Variation in brood sex ratio was not related to any of the potential explanatory variables that we examined. This is one of the first studies to examine reproductive data in a long-running conservation-breeding program and shows that many common metrics do not explain reproductive variation. Our approach provides a framework for managers to investigate factors affecting reproductive success in conservation breeding programs more broadly.

Dietary fat supplements influence weight gain and egg production, but not offspring sex ratios in Japanese quail, Coturnix coturnix japonica

Sex ratio theory suggests that females should bias offspring sex ratios based on maternal condition and the availability of critical food resources. Work in birds indicates that females do, indeed, bias sex ratios according to maternal condition and food quality and quantity. Yet it is unknown whether these sex ratio skews occur due to fluctuations in particular micro‐ or macro‐nutrients, caloric content overall or even the perception of food availability. We hypothesized that dietary fats may drive biases in offspring sex ratios, because measures of maternal condition often reflect fat reserves, and fats are critical for the process of egg‐laying in birds. To test this, we provided breeding Japanese quail, a species that biases sex ratios in response to maternal condition, with either a control breeding diet or a diet supplemented with two oils (safflower oil and flaxseed oil). These oils were chosen for their high omega‐3 and omega‐6 fatty acid content as well as their importance in mammalian sex allocation. We then measured influences of these diets on the sex ratio of offspring, the change in maternal weight, and the laying rates of female quail. The dietary oil supplements increased weight gains in quail but decreased the number of eggs laid during the experiment. There was no influence of the oil supplements on offspring sex ratios. This indicates that fat may not be a macro‐nutrient involved in the process of sex ratio adjustment in quail.

Testing the local mate competition rule in a quasi-gregarious parasitoid with facultative superparasitism

Abstract As an important domain of evolutionary ecology, sex allocation theory well explains the evolution of investment into female versus male offspring. Local mate competition (LMC) is a good predictor of sex allocation, where the optimal sex ratio becomes less female-biased and asymptotically approaches 0.5 as the number of foundresses increases. Parasitoid wasps, with haplodiploid sex determination, offer excellent opportunities to test how organisms manipulate their offspring sex ratio in response to environmental variation, and many species have been proved to allocate sex according to predictions under LMC. When hosts are spatially clustered, as in gregarious species, the mating systems of quasi-gregarious parasitoids meet the essential assumptions (female mating before dispersal) of LMC. However, inconsistent with predictions, in the quasi-gregarious species Anastatus disparis (Hymenoptera: Eupelmidae), a strongly female-biased eclosion sex ratio (0.156 ± 0.018 to 0.185 ± 0.016) was observed as the number of females laying eggs in a patch increased. Superparasitism, in which 44.7% of parasitized hosts contained more than one egg but only one adult emerged from each host, was common in A. disparis. However, the egg sex ratio was determined by microsatellites and likely fit the predictions of LMC theory. Male-biased offspring mortality arising from superparasitism during development likely contributes to the shift from the primary sex ratio predicted under LMC to the observed female-biased eclosion sex ratio. Inconsistent with results in gregarious parasitoids, the role of superparasitism in driving sex ratio shifts in quasi-gregarious parasitoids should be incorporated into LMC-based predictions of sex ratios.

A haplodiploid mite adjusts fecundity and sex ratio in response to density changes during the reproductive period.

Population density is one of the main socio-environmental factors that have critical impacts on reproduction of animals. Consequently, they need to adjust their reproductive strategies in response to changes of local population density. In this study we used a haplodiploid spider mite, Tetranychus ludeni Zacher (Acari: Tetranychidae), to test how population density dynamics during the reproductive period altered female reproductive performance. We demonstrate that females produced fewer eggs with a significantly higher female-biased sex ratio in dense populations. Reducing fecundity and increasing daughter production in a dense environment could be an advantageous strategy to minimise the intensity of local food competition. However, females also reduced their fecundity after arrival in a new site of larger area from a dense population, which may be associated with higher web production costs because females need to produce more webs to cover the larger area. There was no trade-off between egg number and size, and egg size had little impact on reproductive fitness. Therefore, T. ludeni females could adapt to the shift of population density during their reproductive period by manipulating the fecundity and offspring sex ratio but not the egg size.

Sex reversal explains some, but not all, climate-mediated sex ratio variation within a viviparous reptile.

Evolutionary transitions in sex-determining systems have occurred frequently yet understanding how they occur remains a major challenge. In reptiles, transitions from genetic to temperature-dependent sex determination can occur if the gene products that determine sex evolve thermal sensitivity, resulting in sex-reversed individuals. However, evidence of sex reversal is limited to oviparous reptiles. Here we used thermal experiments to test whether sex reversal is responsible for differences in sex determination in a viviparous reptile, Carinascincus ocellatus, a species with XY sex chromosomes and population-specific sex ratio response to temperature. We show that sex reversal is occurring and that its frequency is related to temperature. Sex reversal was unidirectional (phenotypic males with XX genotype) and observed in both high- and low-elevation populations. We propose that XX-biased genotypic sex ratios could produce either male- or female-biased phenotypic sex ratios as observed in low-elevation C. ocellatus under variable rates of XX sex reversal. We discuss reasons why sex reversal may not influence sex ratios at high elevation. Our results suggest that the mechanism responsible for evolutionary transitions from genotypic to temperature-dependent sex determination is more complex than can be explained by a single process such as sex reversal.

Density dependence of clutch size and offspring sex ratio in starling colonies

Optimal life‐history theory predicts that individuals should adjust both the number and the sex of their offspring to maximize fitness in response to environmental and social factors such as breeding density. While reductions in optimal clutch size are well‐studied in birds, the evidence for sex ratio adjustments is still equivocal and, so far, we lack a thorough understanding of how these strategies interact to maximize fitness. Here, we investigate how breeding density simultaneously affects brood sex ratio and clutch size in a sexually dimorphic and polygynous bird. We tested the prediction that mothers breeding at a higher density lay smaller clutches and overproduce daughters, the sex with less variable fitness returns and that disperses further away from their natal territory. We distributed nest boxes at either a high (HD) or a low density (LD) and monitored clutch sizes and sex ratios during five years in a wild breeding colony of spotless starlings. While mothers breeding in HD nests produced more daughters than those breeding in LD nests, the density dependence of clutch size varied among years, with a tendency to lay smaller clutches in HD nests. Our results suggest that mothers consistently adjust offspring sex ratio in response to breeding density, whereas adjustments in clutch size varied in a more complex way. These results support the role of sex allocation strategies in response to density and show that further theoretical and empirical research is required to understand the interaction between clutch size and sex ratio adjustments in animals.

Adjustment of fecundity and sex ratio in response to social environments in a haplodiploid mite

Animals can adjust reproductive strategies in favour of corporation or competition in response to local population size and density, the two key factors of social environments. However, previous studies usually focus on either population size or density but ignore their interactions. Using a haplodiploid spider mite, Tetranychus ludeni Zacher, we carried out a factorial experiment in the laboratory to examine how ovipositing females adjust their fecundity and offspring sex ratio during their early reproductive life under various population size and density. We reveal that females laid significantly more eggs with increasing population size and significantly fewer eggs with increasing population density. This suggests that large populations favour cooperation between individuals and dense populations increase competition. We demonstrate a significant negative interaction of population size and density that resulted in significantly fewer eggs laid in the large and dense populations. Furthermore, we show that females significantly skewed the offspring sex ratio towards female-biased in small populations to reduce the local mate competition among their sons. However, population density incurred no significant impact on offspring sex ratio, while the significant positive interaction of population size and density significantly increased the proportion of female offspring in the large and dense populations, which will minimise food or space competition as females usually disperse after mating at crowded conditions. These results also suggest that population density affecting sex allocation in T. ludeni is intercorrelated with population size. This study provides evidence that animals can manipulate their reproductive output and adjust offspring sex ratio in response to various social environments, and the interactions of different socio-environmental factors may play significant roles.

Maternal influence on the skewing of offspring sex ratio: a review

Sex pre-selection of the progeny to suit the livestock production system aids in greatly increasing the efficiency and profitability of the livestock enterprise to meet the demand for animal meat and dairy products. Individual animals can skew the sex ratio in response to various social and environmental stipulations. These social and environmental factors include the composition of the maternal diet, maternal hormonal levels, maternal stress, and the time of insemination. Hence, this present review focuses on these approaches and their success rate as premises for the alterations of offspring sex ratio in different animal species. Numerous studies have linked maternal nutrition and its influence on offspring sex ratio. A maternal diet rich in calcium and magnesium favoured the production of more females, while diets rich in sodium and potassium favoured more males. Furthermore, feeding animals with a particular type of fat diet, including omega-3, omega-6, or omega-9 fatty acids, assists in sex pre-selection. The circulating hormone level in females during conception is associated with the skewing of sex ratio. In addition, maternal stress during the conception period is also found to be associated with the skewing of the sex ratio in favour of female offspring. The timing of insemination relative to the ovulation period has been identified as a promising approach for the pre-selection of offspring sex; however, proper detection of oestrus is crucial. Among all the approaches reported, dietary manipulation could be regarded as the most affordable and stands a better chance of being optimised for commercial livestock production. Reduction in the cost of desired sex production by adopting sex pre-selection techniques will lead to the improvement of the economy and minimise the culling of the undesired sex. However, further research is necessary to focus on the understanding of the underlying molecular mechanisms for the production of animals of the desired sex.

The role of maternal preconception vitamin D status in human offspring sex ratio

Evolutionary theory suggests that some animal species may experience shifts in their offspring sex ratio in response to maternal health and environmental conditions, and in some unfavorable conditions, females may be less likely to bear sons. Experimental data in both animals and humans indicate that maternal inflammation may disproportionately impact the viability of male conceptuses; however, it is unknown whether other factors associated with both pregnancy and inflammation, such as vitamin D status, are associated with the offspring sex ratio. Here, we show that among 1,228 women attempting pregnancy, preconception 25-hydroxyvitamin D concentrations are positively associated with the live birth of a male infant, with notably stronger associations among women with elevated high sensitivity C-reactive protein, a marker of systemic low-grade inflammation. Our findings suggest that vitamin D may mitigate maternal inflammation that would otherwise be detrimental to the implantation or survival of male conceptuses in utero.

A solution to a sex ratio puzzle in Melittobia wasps

The puzzling sex ratio behavior of Melittobia wasps has long posed one of the greatest questions in the field of sex allocation. Laboratory experiments have found that, in contrast to the predictions of theory and the behavior of numerous other organisms, Melittobia females do not produce fewer female-biased offspring sex ratios when more females lay eggs on a patch. We solve this puzzle by showing that, in nature, females of Melittobia australica have a sophisticated sex ratio behavior, in which their strategy also depends on whether they have dispersed from the patch where they emerged. When females have not dispersed, they lay eggs with close relatives, which keeps local mate competition high even with multiple females, and therefore, they are selected to produce consistently female-biased sex ratios. Laboratory experiments mimic these conditions. In contrast, when females disperse, they interact with nonrelatives, and thus adjust their sex ratio depending on the number of females laying eggs. Consequently, females appear to use dispersal status as an indirect cue of relatedness and whether they should adjust their sex ratio in response to the number of females laying eggs on the patch.

Parental relatedness and parasitoid sex ratios under local mate competition

AbstractSex ratio theory predicts that, under local mate competition, a more female‐biased offspring sex ratio will be produced by females when their relatedness to their mates is closer. We assess how the sexual composition of broods responds to mother–mate relatedness using Goniozus legneri Gordh (Hymenoptera: Bethylidae), a parasitoid wasp that has biased sex ratios due to local mate competition. Relatedness was varied by providing virgin females with a mate that was either a sibling, a non‐sibling from the same strain, from a strain with geographically similar origin or from a strain with geographically distant origin. The sex ratios among broods produced by mothers that had mated with a sibling or a same‐strain male were similar and were more biased than broods produced by females mated with males from a different strain. Brood sex variances were higher after mating with different‐strain males. Previous evaluations of parasitoid sex ratio responses to mate relatedness have not found the patterns predicted, possibly because the species investigated can control progeny sex ratio but cannot discriminate kin. In contrast, female G. legneri appear to possess both these abilities and appears to respond to mate relatedness in qualitative agreement with theoretical predictions.

Corticosterone and testosterone treatment influence expression of gene pathways linked to meiotic segregation in preovulatory follicles of the domestic hen.

Decades of work indicate that female birds can control their offspring sex ratios in response to environmental and social cues. In laying hens, hormones administered immediately prior to sex chromosome segregation can exert sex ratio skews, indicating that these hormones may act directly on the germinal disc to influence which sex chromosome is retained in the oocyte and which is discarded into an unfertilizable polar body. We aimed to uncover the gene pathways involved in this process by testing whether treatments with testosterone or corticosterone that were previously shown to influence sex ratios elicit changes in the expression of genes and/or gene pathways involved in the process of meiotic segregation. We injected laying hens with testosterone, corticosterone, or control oil 5h prior to ovulation and collected germinal discs from the F1 preovulatory follicle in each hen 1.5h after injection. We used RNA-sequencing (RNA-seq) followed by DESeq2 and gene set enrichment analyses to identify genes and gene pathways that were differentially expressed between germinal discs of control and hormone-treated hens. Corticosterone treatment triggered downregulation of 13 individual genes, as well as enrichment of gene sets related to meiotic spindle organization and chromosome segregation, and additional gene sets that function in ion transport. Testosterone treatment triggered upregulation of one gene, and enrichment of one gene set that functions in nuclear chromosome segregation. This work indicates that corticosterone can be a potent regulator of meiotic processes and provides potential gene targets on which corticosterone and/or testosterone may act to influence offspring sex ratios in birds.

Exposure of zebrafish to elevated temperature induces sex ratio shifts and alterations in the testicular epigenome of unexposed offspring

Accumulating evidence shows that environmental changes can affect population sex ratios through epigenetic regulation of gene expression in species where sex depends on both genetic and environmental cues. Sometimes, altered sex ratios persist in the next generation even when the environmental cue is no longer present (a multigenerational effect). However, evidence of transgenerational effects (i.e., beyond the first non-exposed generation), which tend to be paternally transmitted, is scarce and a matter of debate. Here, we used the AB strain of zebrafish, where sex depends on both genetic and environmental influences, to study possible multi- (to the F1) and transgenerational (to the F2) effects of elevated temperature during the critical period of sex differentiation. From eight initial different families, five were selected in order to capture sufficient variation between the sex ratio of the control group (28 °C) and the group exposed to elevated (35 °C) temperature only at the parental (P) generation. Results showed a consistent increase in the proportion of males in the P generation in all five families as a result of heat treatment. Sex ratios were then determined in the F1 and F2 offspring derived from both above groups, which were all raised at 28 °C. A persisting male-skewed sex ratio in the 35°C-derived, unexposed offspring of the F1 generation was observed in three families, denoting family-dependent multigenerational effects. However, no transgenerational effects were observed in the F2 generation of any family. DNA methylation was also assessed in the testis of P, F1 and F2 males derived from exposed and non-exposed fathers and grandfathers. DNA methylation was significantly decreased only in the testis of the 35°C-derived males in the F1 generation but not of the F2 generation and, surprisingly, neither in the 35°C-exposed males of the P generation. Taken together, our results show great interfamily variation, not only in sex ratio response to elevated temperature, but also on its multigenerational effects, denoting a strong influence of genetics. Alterations in the testicular epigenome in F1 males calls for attention to possible, previously unnoticed, effects of temperature in the unexposed offspring of heat-exposed parents in a global warming scenario.

No evidence of sex ratio manipulation by Galápagos mockingbirds in response to environment

Birds can adjust investment in reproduction by altering the sex ratios of their broods. When one sex is more costly to raise than the other, producing either more male or female offspring can lower the costs of reproduction. Biasing sex ratios can also be advantageous if the expected fitness of male versus female offspring differs. Here, we investigated whether Galápagos mockingbirds Mimus parvulus bias sex ratios in response to variation in rainfall. Female mockingbirds are smaller and thus females may reduce the costs of reproduction by biasing sex ratios in favor of female offspring. We quantified sex ratios in 131 mockingbird broods over four years with variable rainfall (2012, 2013, 2015 and 2016). We found no evidence that mockingbirds adjusted sex ratios in response to environmental conditions. Mockingbirds may not adjust sex ratios either because they lack the ability to do so, or because the costs of manipulation outweigh its benefits.

Effects of human activities on Komodo dragons in Komodo National Park

Understanding how threatened wildlife can coexist with humans over the long term is a central issue in conservation and wildlife management. Komodo National Park in Eastern Indonesia, harbors the largest extant populations of the endemic Komodo dragon (Varanus komodoensis). Consistent with global trends, this species is expected to be increasingly exposed to human activities and in particular growing ecotourism activities. Here we comprehensively evaluated how human activities affected individual and population level attributes of Komodo dragons. We compared Komodo dragons phenotypic (behaviour, body size, and body condition) and demographic (age structure, sex ratio, survival, and density) responses to variation in human activities across national park. Komodo dragons were found to exhibit pronounced responses to high human activity level relative to sites with low and negligible human activities. Komodo dragons exposed to ecotourism exhibited significantly less wariness, larger body mass, better body condition, and higher survival. These results are entirely consistent with ecotourism activities that provided Komodo dragons with long-term and substantial nutritional subsidies as a consequence of feeding and human food refuse. However, we also noted the potential negative consequences of altered behaviour and adult-biased populations in ecotourism areas which may influence demographic processes through intraspecific competition or predation. To address this issue, we recommend that three management strategies to be implemented in future include: (1) removal of human-mediated nutritional subsidies, (2) alternative ecotourism, and (3) spatial regulation of ecotourism. Furthermore, we advocate the development of approaches to achieve a socio–ecological sustainability that benefits both people and wildlife conservation.

Estrogen exposure overrides the masculinizing effect of elevated temperature by a downregulation of the key genes implicated in sexual differentiation in a fish with mixed genetic and environmental sex determination

Understanding the consequences of thermal and chemical variations in aquatic habitats is of importance in a scenario of global change. In ecology, the sex ratio is a major population demographic parameter. So far, research that measured environmental perturbations on fish sex ratios has usually involved a few model species with a strong genetic basis of sex determination, and focused on the study of juvenile or adult gonads. However, the underlying mechanisms at the time of gender commitment are poorly understood. In an effort to elucidate the mechanisms driving sex differentiation, here we used the European sea bass, a fish species where genetics and environment (temperature) contribute equally to sex determination. Here, we analyzed the transcriptome of developing gonads experiencing either testis or ovarian differentiation as a result of thermal and/or exogenous estrogen influences. These external insults elicited different responses. Thus, while elevated temperature masculinized genetic females, estrogen exposure was able to override thermal effects and resulted in an all-female population. A total of 383 genes were differentially expressed, with an overall downregulation in the expression of genes involved in both in testicular and ovarian differentiation when fish were exposed to Estradiol-17s through a shutdown of the first steps of steroidogenesis. However, once the female phenotype was imposed, gonads could continue their normal development, even taking into account that some of the resulting females were fish that otherwise would have developed as males. The data on the underlying mechanisms operating at the molecular level presented here contribute to a better understanding of the sex ratio response of fish species subjected to a combination of two of the most common environmental perturbations and can have implications in future conservational policies.

Female kin density affects offspring sex ratio in an asocial mammal, the golden-mantled ground squirrel, Callospermophilus lateralis

Evolutionary theory predicts that parents should bias investment in offspring towards the sex that will yield the higher fitness returns, and one outcome may be biased offspring sex ratios. Bias in offspring sex ratios has been proposed to vary with specific social, maternal and environmental conditions that alter the fitness returns of each sex, but empirical evidence is conflicting both within and across taxa. We used 18 years of pedigree and demographic data to investigate variation in offspring sex ratios in a population of golden-mantled ground squirrels. Despite overall parity in offspring sex ratio, we found predictable changes in offspring sex ratio in response to female density at the population level: squirrels produced more daughters when female density was low and more sons when female density was high. At the individual level, females adjusted litter sex ratios similarly, but only in response to high densities of kin, and not in response to density of nonkin. This effect was reversed for older females (≥3 years) in dense kin neighbourhoods, which were more likely to produce daughters, perhaps because older females had the behavioural dominance necessary to recruit daughters at high densities. By contrast, litter sex ratios did not vary with maternal condition or food availability. Our results support the local resource competition theory of offspring sex allocation for this species. Knowledge of female relatedness revealed patterns of sex ratio adjustment that otherwise would have been obscured, highlighting the importance of interactions with kin in an asocial species.