Low Gestational Weight Gain Skews Human Sex Ratios towards Females

Background

Human males are more vulnerable to adverse conditions than females starting early in gestation and continuing throughout life, and previous studies show that severe food restriction can influence the sex ratios of human births. It remains unclear, however, whether subtle differences in caloric intake during gestation alter survival of fetuses in a sex-specific way. I hypothesized that the ratio of male to female babies born should vary with the amount of weight gained during gestation. I predicted that women who gain low amounts of weight during gestation should produce significantly more females, and that, if gestational weight gain directly influences sex ratios, fetal losses would be more likely to be male when women gain inadequate amounts of weight during pregnancy.

Methods

I analyzed data collected from over 68 million births over 23 years to test for a relationship between gestational weight gain and natal sex ratios, as well as between gestational weight gain and sex ratios of fetal deaths at five gestational ages.

Results

Gestational weight gain and the proportion of male births were positively correlated; a lower proportion of males was produced by women who gained less weight and this strong pattern was exhibited in four human races. Further, sex ratios of fetal losses at 6 months of gestation were significantly male-biased when mothers had gained low amounts of weight during pregnancy, suggesting that low caloric intake during early fetal development can stimulate the loss of male fetuses.

Conclusion

My data indicate that human sex ratios change in response to resource availability via sex-specific fetal loss, and that a pivotal time for influences on male survival is early in fetal development, at 6 months of gestation.     

Adjustment of offspring sex ratios in relation to the availability of resources for philopatric offspring in the common brushtail possum

The local-resource-competition hypothesis predicts that where philopatric offspring compete for resources with their mothers, offspring sex ratios will be biased in favour of the dispersing sex. This should produce variation in sex ratios between populations in relation to differences in the availability of resources for philopatric offspring. However, previous tests of local resource competition in mammals have used indirect measures of resource availability and have focused on sex-ratio variation between species or individuals rather than between local populations. Here, we show that the availability of den sites predicts the offspring sex ratio in populations of the common brushtail possum. Female possums defend access to dens, and daughters, but not sons, occupy dens within their mother's range. However, the abundances of possums in our study areas were determined principally by food availability. Consequently, in food-rich areas with a high population density, the per-capita availability of dens was low, and the cost of having a daughter should have been high. This cost was positively correlated with male bias in the sex ratio at birth. Low per capita availability of dens was correlated with male bias in the sex ratio at birth.     

Local adjustment of sex ratio in the spider Pityohyphantes phrygianus

The sex ratio in five populations of the sheetweb spider Pityohyphantes phrygianus in southwest Sweden was investigated in July and September, the spiders being juveniles and subadults, respectively. In July, no heterogeneity between the five populations was found and the pooled samples revealed a sex ratio of 36% males and 64% females. A significant heterogeneity in sex ratio was observed in the September samples; the proportion of males varied between 23% and 40%. In several cases, male mean weight differed significantly between the five populations, comparing the July and September samples separately. This suggests that the prey availability varied considerably between the sites. In September, dead spiders were collected in two sites. This mortality was probably caused by starvation and the mortality rates differed significantly between the two sites. Indirect evidence suggested that the local sex ratio was affected by the prey availability, males being at a relative disadvantage in poor sites. Local environmental conditions may govern the adult sex ratio in this spider by causing differential mortality and/or migration.     

Experimental evolution under varying sex ratio and nutrient availability modulates male mating success in Drosophila melanogaster

Biased population sex ratios can alter optimal male mating strategies, and allocation to reproductive traits depends on nutrient availability. However, there is little information on how nutrition interacts with sex ratio to influence the evolution of pre-copulatory and post-copulatory traits separately. To address this omission, we test how male mating success and reproductive investment evolve under varying sex ratios and adult diet in Drosophila melanogaster, using experimental evolution. We found that sex ratio and nutrient availability interacted to determine male pre-copulatory performance. Males from female-biased populations were slow to mate when they evolved under protein restriction. By contrast, we found direct and non-interacting effects of sex ratio and nutrient availability on post-copulatory success. Males that evolved under protein restriction were relatively poor at suppressing female remating. Males that evolved under equal sex ratios fathered more offspring and were better at supressing female remating, relative to males from male-biased or female-biased populations. These results support the idea that sex ratios and nutrition interact to determine the evolution of pre-copulatory mating traits, but independently influence the evolution of post-copulatory traits.     

Floral sex allocation at individual and branch levels in Betula platyphylla var. japonica (Betulaceae), a tall, wind-pollinated monoecious tree species

Floral sex allocation at the individual and first-order branch levels and the relation between these levels were examined in Betula platyphylla var. japonica, a wind-pollinated monoecious tree. Floral sex allocation at the individual level varied with resource availability in a pattern similar to that predicted by the Masaka and Takada model (Journal of Theoretical Biology 240: 114-125). Thus, individual trees with few reproductive resources produced only female or male inflorescences, whereas individuals with many resources rarely had a high male ratio (i.e., number of male inflorescences/total number of inflorescences). Furthermore, the number of male inflorescences tended to reach an upper limit, whereas the number of female inflorescences increased monotonically with increasing reproductive investment. The patterns of floral sex allocation at the first-order branch level were analogous to those at the individual level. Thus, each first-order branch of B. platyphylla var. japonica behaves like an individual, and the floral sex allocation of a given branch does not necessarily represent the individual tree. The effect of the individual-level floral sex ratio on branch-level floral sex allocation indicates that branch behavior is controlled by the individual.     

Eat or Not to Eat: Reversed Sexual Cannibalism as a Male Foraging Strategy in the Spider Micaria sociabilis (Araneae: Gnaphosidae)

Reversed sexual cannibalism represents an unusual situation in which a male kills and consumes a female. We examined this rare phenomenon in the spider Micaria sociabilis, whose males were observed to regularly cannibalise old females. In this study, we investigated male motivation for such behaviour in the light of ecological conditions such as mate availability and prey availability. We found that male cannibalism is not affected by short‐term starvation but rather by male feeding history during the ontogenetic development in combination with prey availability during the adult stage. Males from the summer generation reached bigger sizes than males from the spring generation and females from both generations. They developed in the period with exceptionally high prey occurrence, but when they reached the adult stage, the prey availability decreased. In this period, we observed the highest frequency of cannibalism, however, only when the sex ratio was female biased. Reversed sexual cannibalism in M. sociabilis seems to represent an advantageous male foraging strategy, which is affected by prey availability and male feeding history, tuned by sex ratio and directed towards females of inferior quality.     

Sex allocation in the ant Camponotus (Colobopsis) nipponicus (Wheeler): II. The effect of resource availability on sex-ratio variability

Sex-ratio studies have played a prominent role in tests of kin selection theory in the eusocial Hymenoptera. The winner in sex-ratio conflict between queens and workers must control the ratio through proximate mechanisms. To determine how a colony adjusts its sex ratio, the mechanism of sex-ratio determination was analyzed in the field in colonies of the ant Camponotus (Colobopsis) nipponicus. A path model including five colony characteristics showed that the resource availability of the colony (quantified as the amount of stored fat in the bodies of the workers) has a large positive effect on the proportion of new queens in the female larvae, but has little effect on male production. The results indicated that a colony adjusts the sex ratio by altering the proportion of new queens obtained from a diploid brood in response to resource availability rather than by eliminating male larvae.     

Sex ratio of Parus major and P. caeruleus broods depends on parental condition and habitat quality

Brood sex ratio was studied in 88 families of Parus caeruleus (blue tit) and 95 families of P. major (great tit) in deciduous and mixed forest habitats differing in food availability. As a food specialist, the blue tit is expected to be more sensitive to the nutritional differences between the habitats than a food generalist such as the great tit. A shift of brood sex ratio towards males was detected for great tits in the high quality habitat, but there was no significant impact of parental condition or the number of nestlings. In contrast, brood sex ratio of blue tits was not affected by habitat quality. In blue tits, male condition correlated positively with a male-biased sex ratio. Habitat quality, however, affected the body mass differences of male and female blue tit siblings, and nestlings developed differently. The low quality habitat had a negative effect on the sexual dimorphism of siblings in male-biased broods, and the condition of offspring was bad. Nevertheless, sexual dimorphism cannot explain the differences between great and blue tits with respect to the correlation of sex ratio and individual condition.     

Photoperiod influences the critical caloric intake necessary to maintain reproduction among male deer mice (Peromyscus maniculatus).

The concept of critical day length is well established among rodents; reproductive function is maintained when day lengths are greater than some specific threshold. In addition to day length cues, seasonal breeding in deer mice can also be regulated by food availability. The caloric threshold necessary to support reproduction remains unspecified for seasonally breeding rodents. The present study examined the interaction between photoperiod and food availability on reproductive function in adult male deer mice (Peromyscus maniculatus). A critical caloric intake profile was constructed in long (16L:8D) and short (8L:16D) photoperiods; groups of deer mice in both photoperiods either received food ad libitum or 90, 80, or 70% of their individual ad libitum food intake for 10 wk. At autopsy, paired testes, epididymides, and seminal vesicles were removed and weighed. Body mass, total body fat, and total body water contents were also obtained. Short, as compared to long, day lengths inhibited the reproductive systems of male deer mice. However, food consumption interacted with photoperiod to affect reproductive function. Significant reductions in reproductive organ size as well as spermatogenic activity were observed among short-day mice after a 10% reduction in ad libitum food intake. Long-day animals required a 20% reduction in caloric intake to depress reproductive function. Body mass and total body water content were generally unaffected by either photoperiod or food consumption. Total body fat content was reduced in short- as compared to long-day mice. Individual reproductive responsiveness to short days increased as food availability decreased.(ABSTRACT TRUNCATED AT 250 WORDS)     

Sex allocation conflict between queens and workers in Formica pratensis wood ants predicts seasonal sex ratio variation

Sex allocation theory predicts parents should adjust their investment in male and female offspring in a way that increases parental fitness. This has been shown in several species and selective contexts. Yet, seasonal sex ratio variation within species and its underlying causes are poorly understood. Here, we study sex allocation variation in the wood ant Formica pratensis. This species displays conflict over colony sex ratio as workers and queens prefer different investment in male and female offspring, owing to haplodiploidy and relatedness asymmetries. It is unique among Formica ants because it produces two separate sexual offspring cohorts per season. We predict sex ratios to be closer to queen optimum in the early cohort but more female‐biased and closer to worker optimum in the later one. This is because the power of workers to manipulate colony sex ratio varies seasonally with the availability of diploid eggs. Consistently, more female‐biased sex ratios in the later offspring cohort over a three‐year sampling period from 93 colonies clearly support our prediction. The resulting seasonal alternation of sex ratios between queen and worker optima is a novel demonstration how understanding constraints of sex ratio adjustment increases our ability to predict sex ratio variation.     

Seasonal Variation in Mate Choice of Photinus ignitus Fireflies

Mate choice by either sex may vary with changes in the associated costs and benefits, determined by factors such as the availability of potential mates and variation in mate quality. We examined seasonal variation in operational sex ratio, courtship behavior, spermatophore mass, egg count, and the relationship between morphological traits and mating success in Photinus ignitus fireflies to determine if mate choice in either sex varied with the availability and relative reproductive investment of fertilizable females and sexually active males. Successfully mating males had larger lanterns than unsuccessful males when the operational sex ratio was male‐biased. In addition, female responsiveness to male signals increased as the number of courting males decreased, and male spermatophore mass decreased with body size across the mating season. Successfully mating females had larger body mass than unsuccessful females. Female body mass predicted egg count and female rejection by males increased as the season progressed and female size decreased. These results suggest that both male and female P. ignitus exhibit mate choice, and that such choice is influenced by seasonal variation in the abundance and quality of potential mates.     

Sex allocation and sex‐specific parental investment in an endangered seabird

Biased offspring sex ratio is relatively rare in birds and sex allocation can vary with environmental conditions, with the larger and more costly sex, which can be either the male or female depending on species, favoured during high food availability. Sex‐specific parental investment may lead to biased mortality and, coupled with unequal production of one sex, may result in biased adult sex ratio, with potential grave consequences on population stability. The African Penguin Spheniscus demersus, endemic to southern Africa, is an endangered monogamous seabird with bi‐parental care. Female adult African Penguins are smaller, have a higher foraging effort when breeding and higher mortality compared with adult males. In 2015, a year in which environmental conditions were favourable for breeding, African Penguin chick production on Bird Island, Algoa Bay, South Africa, was skewed towards males (1.5 males to 1 female). Males also had higher growth rates and fledging mass than females, with potentially higher post‐fledging survival. Female, but not male, parents had higher foraging effort and lower body condition with increasing number of male chicks in their brood, thereby revealing flexibility in their parental strategy, but also the costs of their investment in their current brood. The combination of male‐biased chick production and higher female mortality, possibly at the juvenile stage as a result of lower parental investment in female chicks, and/or at the adult stage as a result of higher parental investment, may contribute to a biased adult sex ratio (ASR) in this species. While further research during years of contrasting food availability is needed to confirm this trend, populations with male‐skewed ASRs have higher extinction risks and conservation strategies aiming to benefit female African Penguin might need to be developed.     

Sex-specific physiological, allocation and growth responses to water availability in the subdioecious plant Honckenya peploides

The gender of dimorphic plant species is often affected by ecophysiological variables. Differences have been interpreted as a response of the sexes to meet specific resource demands associated with reproduction. This study investigated whether sex‐specific variations in ecophysiological traits in response to water availability determine the performance of each sex in different habitats, and therefore promote extreme spatial segregation of the sexes in the subdioecious plant, Honckenya peploides. Twenty‐seven plants of each sex were individually potted in dune sand and assigned randomly to one of three water treatments. Well‐watered plants were watered daily to field capacity, whereas plants in the moderate and high‐water stress treatments received 40% and 20%, respectively, of the water given to well‐watered plants. Photochemical efficiency, leaf spectral properties and components of relative growth rate (leaf area ratio and net assimilation rate) were measured. Photochemical efficiencies integrated over time were higher in male than in female plants. Water deficit decreased maximum quantum yield in female plants more rapidly than in male plants, but female plants (unlike male plants) had recovered to initial values by the end of the experiment. Maximum quantum yield in male plants was more affected by water stress than in female plants, indicating that male plants were more susceptible to photoinhibition. The two sexes did not differ in growth rate, but male plants invested a higher proportion of their biomass in leaves, had a higher leaf area per unit biomass and lower net assimilation rate relative to female plants. Female plants had a higher water content and succulence than male plants. Differences in stomatal density between the sexes depended on water availability. The results suggest that the two sexes of H. peploides have different strategies for coping with water stress. The study also provides evidence of sex differences in allocation traits. We conclude that between‐sex differences in ecophysiological and allocation traits may contribute to explain habitat‐related between‐sex differences in performance and, therefore, the spatial segregation of the sexes.     

Environmental and demographic drivers of male mating success vary across sequential reproductive episodes in a polygynous breeder

Ecological and social factors underpinning the inequality of male mating success in animal societies can be related to sex ratio, sexual conflict between breeders, effects of nonbreeders, resource dispersion, climatic conditions, and the various sequential stages of mating competition that constitute the sexual selection process. Here, we conducted an individual‐based study to investigate how local resource availability and demography interact with annual climate conditions to determine the degree of male mating inequality, and thus opportunity for sexual selection across two sequential reproductive episodes (harem and subsequent mate acquisition) in a naturally regulated (feral) horse population in Sable Island National Park Preserve, Canada. Using a 5‐year, spatially explicit, mark‐resight dataset and hierarchical mixed‐effects linear modeling, we evaluated the influence of adult sex ratio (ASR) on mating success and then tested for effects of freshwater availability, density, unpaired male abundance, and precipitation during each breeding season. Unpaired male abundance, freshwater availability, and ASR differed in their effects on male mating success according to year and selection episode. Opportunity for sexual selection in males associated with harem acquisition increased with ASR, and unpaired male abundance further explained weather‐related interannual variation after accounting for ASR. In contrast, once a harem was secured, ASR had little effect on male mating inequality in regard to acquiring additional females, while interannual variation in mating inequality increased with decreasing freshwater availability. Our findings show that local demography, resource availability, and weather effect opportunity for sexual selection in males differently depending on selection episode, and can attenuate or accentuate effects of ASR.     

Plastic sex-roles in the common goby – the effect of nest availability

One of the most important factors shaping animal sex-roles is the operational sex ratio, since a skew of this ratio promotes mating competition in the more abundant sex. In this study, we wanted to see if a change in sex-roles, related to an environmental induced change in operational sex ratio, could be demonstrated in a field situation. Common goby ( Pomatoschistus microps ) males build nests under bivalve shells and provide exclusive parental care. Therefore, available nest sites are crucial for successful breeding in this species and should also affect the operational sex ratio. We addressed the question of whether the availability of nest sites, through an effect on the operational sex ratio, affects courtship and mating competition in the common goby. We increased nest site availability in the field by adding potential nest material (bivalve shells) to one location. We then compared the reproductive behaviour of the gobies at this and another location with lower nest site abundance. In general, the reproductive behaviour differed as predicted. Under nest shortage, males occupied new nests and received eggs faster than under nest excess. Behavioural observations of nests revealed that males initiated courtship more often than females where nest sites were abundant, whereas female courtship dominated where nests were scarce. Males more often rejected females attempting to enter their nests under nest shortage, male sneaking attempts were also more common in this bay. Male-male aggression was frequent at both locations, whereas agonistic interactions between females only occurred in the nest shortage bay. Thus, males should be subject to sexual selection in both bays even though courtship roles differed. These results suggest that nest site availability affects mating competition and courtship roles in the common goby.     

Maternal Condition but Not Corticosterone Is Linked to Offspring Sex Ratio in a Passerine Bird

There is evidence of offspring sex ratio adjustment in a range of species, but the potential mechanisms remain largely unknown. Elevated maternal corticosterone (CORT) is associated with factors that can favour brood sex ratio adjustment, such as reduced maternal condition, food availability and partner attractiveness. Therefore, the steroid hormone has been suggested to play a key role in sex ratio manipulation. However, despite correlative and causal evidence CORT is linked to sex ratio manipulation in some avian species, the timing of adjustment varies between studies. Consequently, whether CORT is consistently involved in sex-ratio adjustment, and how the hormone acts as a mechanism for this adjustment remains unclear. Here we measured maternal baseline CORT and body condition in free-living blue tits (Cyanistes caeruleus) over three years and related these factors to brood sex ratio and nestling quality. In addition, a non-invasive technique was employed to experimentally elevate maternal CORT during egg laying, and its effects upon sex ratio and nestling quality were measured. We found that maternal CORT was not correlated with brood sex ratio, but mothers with elevated CORT fledged lighter offspring. Also, experimental elevation of maternal CORT did not influence brood sex ratio or nestling quality. In one year, mothers in superior body condition produced male biased broods, and maternal condition was positively correlated with both nestling mass and growth rate in all years. Unlike previous studies maternal condition was not correlated with maternal CORT. This study provides evidence that maternal condition is linked to brood sex ratio manipulation in blue tits. However, maternal baseline CORT may not be the mechanistic link between the maternal condition and sex ratio adjustment. Overall, this study serves to highlight the complexity of sex ratio adjustment in birds and the difficulties associated with identifying sex biasing mechanisms.     

Population differences in female resource abundance, adult sex ratio, and male mating success in Dendrobates pumilio

In this study I examined the relationship among abundance ofreproductive resources, population density, and adult sex ratioin the strawberry dart-poison frog, Dendrobates pumilio, andhow these variables in turn influence the mating system, malereproductive success, and sexual selection. I studied the matingbehavior in two populations of D. pumilio living in a primaryand secondary rainforest on the Caribbean slope of Costa Rica.The abundance of tadpole-rearing sites (reproductive resourcesfor females) was approximately 10-fold higher in the secondary forest. Accordingly, the population density was higher and theadult sex ratio was strongly female biased in the secondaryforest, whereas the adult sex ratio was even in the primaryforest. The female-biased sex ratio was associated with a higherlevel of polygyny and higher male mating and reproductive successin the secondary forest. In contrast, the level of polyandrydid not differ between habitats. As expected, the opportunityfor sexual selection on male mating success was lower in thesecondary forest, the habitat with high female density. Inconclusion, my results suggest that ecological variables suchas resource availability have a great impact on the matingsystem and sexual selection through their effect on population structure. Moreover, the results of this study give furtherevidence that the opportunity for sexual selection is influencedby the adult sex ratio and hence by the operational sex ratioin a population.     

Differences in environmental response between the sexes of the dioecious shrub Baccharis halimifolia (Compositae)

Summary Baccharis halimifolia (Compositae) is a dioecious shrub which grows on the upland fringe of tidal marshes along the Atlantic and Gulf Coasts of North America. We examined the responses of the two sexes to variation in nutrient and moisture availability plant density, and defoliation. By growing plants from seedlings to flowering adults under various combinations of soil type, fertilization rate and plant density, we were able to establish different rates of plant growth and mortality. Plants grown at high density and low nutrient and water supply grew the least, incurrent the most mortality and showed a male-biased sex ratio (73% male). At low density with abundant nutrients and water, plants grew more, survived well, flowered frequently, and were female-biased (75% female). Changes in sex ratio were probably the result of sex-related mortality rather than sexual lability of the seedlings. While changes in sex ratio occurred under experimental conditions in the green-house, no evidence for differences in habitat utilization between the sexes were found in the field and the sex ratio (59% female) did not vary across habitats. In the marsh habitats we sampled where water and nutrients were apparently available, there was no evidence for differential mortality between the sexes. When defoliated (75% of leaf tissue), both sexes showed similar reductions in reproductive effort (number of flower heads/shoot). Our results indicate that differences between the sexes of Baccharis in their response to environmental growing conditions is an important ecological factor associated with the separation of male and female function into separate individuals.     

Social boundaries in a Malagasy Prosimian,the Sifaka (Propithecus verreauxi)

Using focal animal samples, the social organization of sifakas was studied in two forests for 2500 hr spread over 18 months. Data were also obtained on the size and composition of groups at two other sites. The size and adult sex ratio of groups varied widely within populations, although population-wide sex ratios approached unity. During the brief annual mating season, some males mated with females belonging to other groups. The response of both male and female group members to the approach of a nongroup male appeared to depend on his identity. It is argued that while group size may be constrained by the availability of resources, group composition reflects the effects of small-sample demographic variations rather than the outcome of reproductive competition among or between males and females. Spatial boundaries of groups do not coincide with social or reproductive boundaries even within a single breeding season; further study is needed of the processes whereby relationships are established and maintained between individuals from different groups.     

Sex of the first hatched chick influences survival of the brood in the herring gull (Larus argentatus)

Differences in the growth rate of male and female offspring can result in different parental rearing costs for sons and daughters. Such differences may also influence the survival chances of male and female offspring when conditions are unfavourable. In birds, hatching asynchrony leads to hierarchical competition for food between siblings. Therefore, the sex of the chick in the first hatched position in the brood may influence breeding success by affecting the extent to which the later hatched chicks can compete for resources. The interaction between brood sex composition and chick performance in the herring gull Larus argentatus was examined under different environmental conditions. When environmental conditions were relatively good, chick survival within broods was better when a female was first to hatch, an effect that was most obvious later in the season. When conditions were poorer however, sex of the first hatched chicks was not related to brood survival. In neither situation did the overall primary sex ratio differ from equality. However in the year of relatively good food availability, the first chick in the brood was more likely to be male early in the season, which was when the disadvantageous effects on brood survival of males being in this position are weakest.