Evolutionary ecology of human birth sex ratio under the compound influence of climate change, famine, economic crises and wars

1.  Human sex ratio at birth at the population level has been suggested to vary according to exogenous stressors such as wars, ambient temperature, ecological disasters and economic crises, but their relative effects on birth sex ratio have not been investigated. It also remains unclear whether such associations represent environmental forcing or adaptive parental response, as parents may produce the sex that has better survival prospects and fitness in a given environmental challenge.
2.  We examined the simultaneous role of wars, famine, ambient temperature, economic development and total mortality rate on the annual variation of offspring birth sex ratio and whether this variation, in turn, was related to sex-specific infant mortality rate in Finland during 1865–2003.
3.  Our findings show an increased excess of male births during the World War II and during warm years. Instead, economic development, famine, short-lasting Finnish civil war and total mortality rate were not related to birth sex ratio. Moreover, we found no association between annual birth sex ratio and sex-biased infant mortality rate among the concurrent cohort.
4.  Our results propose that some exogenous challenges like ambient temperature and war can skew human birth sex ratio and that these deviations likely represent environmental forcing rather than adaptive parental response to such challenges.     

Differential reproductive success and facultative adjustment of sex ratios among captive female bonnet macaques (Macaca radiata)

In a group of captive bonnet macaques (Macaca radiata) housed at the California Primate Research Center, variance in reproductive success among females is primarily due to differences in infant survival. The infants of low-ranking females have a smaller probability of surviving to 6 months of age than do the infants of other females. In addition, the juvenile daughters of low-ranking females are more vulnerable to behaviourally induced mortality than are other immature animals. Observational evidence indicates that this mortality is the direct result of aggression by unrelated, higherranking adult females. Although infants' sex is not consistently related to survival, yearly fluctuations in the survival of male and female infants are reflected in the extent and direction of the skew in the sex ratio of offspring produced the following year. Years in which the highest proportion of male infants survive are followed by years in which the largest proportions of the birth cohorts are composed of males, and years in which the largest proportions of females survive are followed by years in which the largest proportions of birth cohorts are composed of females. For infant females the probability of surviving is reduced when a substantial proportion of the birth cohort is composed of females. The same pattern is evident among the sons of low-ranking females. The adaptive significance of behaviourally induced variation in reproductive success among females is considered in relation to these data.     

Differential allocation in a lekking bird: females lay larger eggs and are more likely to have male chicks when they mate with less related males

The differential allocation hypothesis predicts increased investment in offspring when females mate with high-quality males. Few studies have tested whether investment varies with mate relatedness, despite evidence that non-additive gene action influences mate and offspring genetic quality. We tested whether female lekking lance-tailed manakins (Chiroxiphia lanceolata) adjust offspring sex and egg volume in response to mate attractiveness (annual reproductive success, ARS), heterozygosity and relatedness. Across 968 offspring, the probability of being male decreased with increasing parental relatedness but not father ARS or heterozygosity. This correlation tended to diminish with increasing lay-date. Across 162 offspring, egg volume correlated negatively with parental relatedness and varied with lay-date, but was unrelated to father ARS or heterozygosity. Offspring sex and egg size were unrelated to maternal age. Comparisons of maternal half-siblings in broods with no mortality produced similar results, indicating differential allocation rather than covariation between female quality and relatedness or sex-specific inbreeding depression in survival. As males suffer greater inbreeding depression, overproducing females after mating with related males may reduce fitness costs of inbreeding in a system with no inbreeding avoidance, while biasing the sex of outbred offspring towards males may maximize fitness via increased mating success of outbred sons.     

Fitness,reproduction and longevity among European aristocratic and rural Finnish families in the 1700s and 1800s

The life histories of two socio-economically different groups of humans comprising birth cohorts from the 1700s and 1800s were investigated. It was discovered that fertility selection was greater among European aristocrats and mortality selection greater among rural Finns. The life history of the rural Finns involved shorter female life spans, a considerably longer period of reproduction, higher juvenile mortality, a greater total production of offspring and slightly higher individual fitness. In a comparison of parental cohorts, it was discovered that longevity and progeny survival improved significantly from the 1700s to the 1800s. Out of the three factors investigated, longevity was found to influence reproduction and fitness more than socio-economic group or birth cohort. The reproductive efficacy and fitness of women increased along with their life span. However, reproductive success and fitness were lower among women with the longest life span (over 80 years). Among men, reproductive success improved consistently along with the increase in longevity. When birth intervals were examined, it was discovered that the sex of previous offspring did not influence the interval between births.     

Reproductive parameters of female Japanese macaques: Thirty years data from the arashiyama troops,Japan

Over a 30-year period from 1954 to 1983, 975 live births were recorded for Japanese macaque females at the Iwatayama Monkey Park, Arashiyama, Japan. Excluding unknown birth dates, primiparous mothers gave birth to 185 infants (182 cases with age of mother known) and multiparous mothers gave birth to 723 infants (603 cases with age of mother known). The peak month of birth was May with 52.3% of the total births occurring during the period. Multiparous females who had not given birth the previous year did so earlier than multiparous females who had given birth the previous year and also earlier than primiparous females. Among the females who had given birth the previous year, females whose infant had died gave birth earlier than females who had reared an infant the previous year. The offspring sex ratio (1:0.97) was not significantly different from 1:1, and revealed no consistent association with mother's age. Age-fecundity exhibited a humped curve. The annual birth rate was low at the age of 4 years but increased thereafter, ranging between 46.7% and 69.0%, at between 5 and 19 years of age, but again decreased for females between 20 and 25 years of age. Some old females displayed clear reproductive senescence. The infant mortality within the first year of age was quite low (10.3%) and the neonatal (less than 1 month old) mortality rate accounted for 49.0% of all infant deaths. There was no significant difference between the mortality rates of male and female infants. A female's rank-class had no apparent effect on the annual birth rate, infant mortality, and offspring sex ratio. These long-term data are compared with those from other primate populations.     

Adaptive Offspring Sex Ratio Depends on Male Tail Length in the Guppy

A biased sex ratio in a brood is considered to be an adaptive strategy under certain circumstances. For example, if the expected reproductive success of one sex is greater than that of the other, parents should produce more offspring of the former sex than the latter. A previous study has documented that in the guppy, Poecilia reticulata, the female offspring of males possessing proportionally longer tails exhibit smaller body sizes and show decreased reproductive outputs than those of males having shorter tails. On the other hand, the total lengths of the male offspring of the long‐tailed males are larger because of their longer tails; consequently, they exhibit greater sexual attractiveness to females. Therefore, it has been hypothesized that this asymmetry in the expected reproductive success between the male and female offspring of long‐tailed males may result in a biased sex ratio that is dependent on the tail lengths of their fathers. This hypothesis was tested in the present study. The results showed that the females that mated with long‐tailed males produced more male offspring than those that mated with short‐tailed males. Logistic regression analysis showed that the ratio of tail length to the standard length of the fathers is a determinant factor of the sex of their offspring. These results suggest that the manipulation of the offspring sex ratios by parents enhances the overall fitness of the offspring.     

Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum)

Female greater horseshoe bats form maternity colonies each summer in order to give birth and raise young. During the mating period, females visit males occupying territorial sites, copulation takes place and sperm are stored until ovulation occurs, normally in April. Using microsatellite markers and a likelihood method of parentage analysis, we studied breeding behaviour and male reproductive success over a five-year period in a population of bats in south-west Britain. Paternity was assigned with 80% confidence to 44% of young born in five successive cohorts. While a small annual skew in male reproductive success was detected, the variance increased over five years due to the repeated success of a few individuals. Mating was polygynous, although some females gave birth to offspring sired by the same male in separate years. Such repeated partnerships probably result from fidelity for either mating sites or individuals or from sperm competition. Females mated with males born both within and outside their own natal colony; however, relatedness between parents was no less than the average recorded for male female pairs. Gene flow between colonies is likely to be primarily mediated by both female and male dispersal during the mating period rather than more permanent movements.     

Trends in Population Sex Ratios May be Explained by Changes in the Frequencies of Polymorphic Alleles of a Sex Ratio Gene

A test for heritability of the sex ratio in human genealogical data is reported here, with the finding that there is significant heritability of the parental sex ratio by male, but not female offspring. A population genetic model was used to examine the hypothesis that this is the result of an autosomal gene with polymorphic alleles, which affects the sex ratio of offspring through the male reproductive system. The model simulations show that an equilibrium sex ratio may be maintained by frequency dependent selection acting on the heritable variation provided by the gene. It is also shown that increased mortality of pre-reproductive males causes an increase in male births in following generations, which explains why increases in the sex ratio have been seen after wars, also why higher infant and juvenile mortality of males may be the cause of the male-bias typically seen in the human primary sex ratio. It is concluded that various trends seen in population sex ratios are the result of changes in the relative frequencies of the polymorphic alleles of the proposed gene. It is argued that this occurs by common inheritance and that parental resource expenditure per sex of offspring is not a factor in the heritability of sex ratio variation.     

Temperature-related birth sex ratio bias in historical Sami: warm years bring more sons

The birth sex ratio of vertebrates with chromosomal sex determination has been shown to respond to environmental variability, such as temperature. However, in humans the few previous studies on environmental temperature and birth sex ratios have produced mixed results. We examined whether reconstructed annual mean temperatures were associated with annual offspring sex ratio at birth in the eighteenth to nineteenth century Sami from northern Finland. We found that warm years correlated with a male-biased sex ratio, whereas a warm previous year skewed sex ratio towards females. The net effect of one degree Celsius increase in mean temperature during these 2 years corresponded to approximately 1% more sons born annually. Although the physiological and ecological mechanisms mediating these effects and their evolutionary consequences on parental fitness remain unknown, our results show that environmental temperature may affect human birth sex ratio.     

Population structure of olive baboons (Papio anubis (J. P. Fischer)) in the Laikipia District of Kenya

A study of the population structure of olive baboons {Papio anubis (J. P. Fischer)) was conducted near Rumuruti and Nanyuki in the Laikipia District of Kenya during 1969. The overall male: female ratio was 96:100 for all animals captured. The sex ratio of immature baboons favoured males, while adult females outnumbered adult males. Male baboons demonstrated an increased mortality during the juvenile stage primarily due to exploratory behaviour. Female baboons demonstrated an increased mortality incurred during the first pregnancy or birth early in the adult stage. About 50 % of adult females had an infant offspring, while about 75% had a juvenile offspring. Adult female baboons in their native environment produce an offspring every 2.5-3.0 years. No birth peak was discernable and births occurred throughout the year.     

An analysis of birth sex ratio bias in captive prosimian species

The extent to which sex ratio bias is a common reproductive characteristic of prosimians has not been well established. The present study analyzed reproduction in 13 breeding groups of captive prosimians for evidence of birth sex ratio bias. A substantial male bias was demonstrated in nongregarious, but not gregarious, breeding groups. Analyses of birth sex ratios of individual mothers suggested that the observed bias did not result from the tendency of a few mothers to overproduce males, but rather from a small but reliable excess of male births in general. An examination of infant mortality revealed that male Otolemur garnettii and Microcebus murinus infants were more vulnerable to preweaning mortality, whereas female Eulemur fulvus albifrons infants were more vulnerable. An analysis of birth order by sex found that mothers of one group (O. garnettii) tended to produce males initially and females later. Additionally, a distinct pattern of birth seasonality was noted among Malagasy prosimians that was absent in the African prosimians. Greater length of period of sexual receptivity for nongregarious females as compared to gregarious females is proposed as a possible mechanism of male birth sex ratio bias. © 1996 Wiley-Liss, Inc.     

The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques,Macaca fascicularis

Demographic changes were recorded throughout a 12-year period for three social groups ofMacaca fascicularis in a natural population at Ketambe (Sumatra, Indonesia). We examined the prediction that females' lifetime reproductive success depended on dominance rank and group size. Average birth rate was 0.53 (184 infants born during 349 female years). For mature females (aged 8–20 yr) birth rate reflected physical condition, being higher in years with high food availability and lower in the year following the production of a surviving infant. High-ranking females were significantly more likely than low-ranking ones to give birth again when they did have a surviving offspring born the year before (0.50 vs 0.26), especially in years with relatively low food availability (0.37 vs 0.10). Controlled comparisons of groups at different sizes indicate a decline in birth rate with rroup size only once a group has exceeded a certain size. The dominance effect on birth rate tended to be strongest in large groups. Survival of infants was rank-dependent, but the survival of juveniles was not. There was a trend for offspring survival to be lower in large groups than in mid-sized or small groups. However, rank and group size interacted, in that rank effects on offspring survival were strongest in large groups. High-ranking females were less likely to die themselves during their top-reproductive years, and thus on average had longer reproductive careers. We estimated female lifetime reproductive success based on calculated age-specific birth rates and survival rates. The effects of rank and group size (contest and scramble) on birth rate, offspring survival, age of first reproduction for daughters, and length of reproductive career, while not each consistently statistically significant, added up to substantial effects on estimated lifetime reproductive success. The group size effects explain why large groups tend to split permanently. Since females are philopatric in this species, and daughters achieve dominance rank positions similar to their mother, a close correlation is suggested between the lifetime reproductive success of mothers and daughters. For sons, too, maternal dominance affected their reproductive success: high-born males were more likely to become top-dominant (in another group). These data support the idea that natural selection has favored the evolution of a nepotistic rank system in this species, even if the annual benefits of dominance are small.     

No evidence for sex biases in milk macronutrients,energy, or breastfeeding frequency in a sample of filipino mothers

Maternal reproductive investment includes both the energetic costs of gestation and lactation. For most humans, the metabolic costs of lactation will exceed those of gestation. Mothers must balance reproductive investment in any single offspring against future reproductive potential. Among mammals broadly, mothers may differentially invest in offspring based on sex and maternal condition provided such differences investment influence future offspring reproductive success. For humans, there has been considerable debate if there are physiological differences in maternal investment by offspring sex. Two recent studies have suggested that milk composition differs by infant sex, with male infants receiving milk containing higher fat and energy; prior human studies have not reported sex‐based differences in milk composition. This study investigates offspring sex‐based differences in milk macronutrients, milk energy, and nursing frequency (per 24 h) in a sample of 103 Filipino mothers nursing infants less than 18 months of age. We found no differences in milk composition by infant sex. There were no significant differences in milk composition of mothers nursing first‐born versus later‐born sons or daughters or between high‐ and low‐income mothers nursing daughters or sons. Nursing frequency also showed no significant differences by offspring sex, sex by birth order, or sex by maternal economic status. In the Cebu sample, there is no support for sex‐based differences in reproductive investment during lactation as indexed by milk composition or nursing frequency. Further investigation in other populations is necessary to evaluate the potential for sex‐based differences in milk composition among humans. Am J Phys Anthropol 152:209–216, 2013. © 2013 Wiley Periodicals, Inc.     

Maternal smoking in pregnancy and sex differences in perinatal death between boys and girls

The sex difference in perinatal mortality in developed countries is largely unexplained. The current study evaluated the differences in the impact of maternal smoking during pregnancy on the risk of perinatal death between males and females. The analysis involved 11,469 and 9,404 newborns derived from two population-based birth cohorts in Northern Finland, for 1966 and 1985-86, respectively. The perinatal mortality rate was 23 per thousand in the 1966 cohort and 9 per thousand in the 1985-86 cohort. The rate ratio (RR) for mortality for males over females is 1.15 and 1.60 in the two cohorts, respectively. Among children whose mothers smoked during pregnancy, the RR was 2.2 (95% CI 1.0, 4.7) for the former cohort and 4.8 (95% CI 1.5, 15.2) for the later cohort; and among the children whose mothers did not smoke the corresponding RR was 1.2 (95% CI 0.9, 1.6) and 1.1 (95% CI 0.6, 1.9). Maternal smoking during pregnancy could be an important determinant accounting for the excess perinatal death for males over females. Our results encourage evaluation of the findings among other populations.     

Maternal smoking in pregnancy and sex differences in perinatal death between boys and girls

Abstract

The sex difference in perinatal mortality in developed countries is largely unexplained. The current study evaluated the differences in the impact of maternal smoking during pregnancy on the risk of perinatal death between males and females. The analysis involved 11,469 and 9,404 newborns derived from two population‐based birth cohorts in Northern Finland, for 1966 and 1985–86, respectively. The perinatal mortality rate was 23 per thousand in the 1966 cohort and 9 per thousand in the 1985–86 cohort. The rate ratio (RR) for mortality for males over females is 1.15 and 1.60 in the two cohorts, respectively. Among children whose mothers smoked during pregnancy, the RR was 2.2 (95% CI 1.0, 4.7) for the former cohort and 4.8 (95% CI 1.5, 15.2) for the later cohort; and among the children whose mothers did not smoke the corresponding RR was 1.2 (95% CI 0.9, 1.6) and 1.1 (95% CI 0.6, 1.9). Maternal smoking during pregnancy could be an important determinant accounting for the excess perinatal death for males over females. Our results encourage evaluation of the findings among other populations.     

The delineation of fertility strategies in a tribal population of India: the Koyas of Koraput District,Orissa

Demographic data collected for a tribal population of India, the Koyas of Koraput District, Orissa, were examined in light of 2 models of reproductive behavior associated with the economic value of children: the replacement effect and son survivorship motivation. Both models are united in the concept that infant/child mortality affects subsequent fertility. The database consists of retrospective fertility histories of Koya women who had completed their reproductive period. The total number was 260, with the total offspring numbering 1407. 2 distinct cohorts of women were formed for the purpose of analysis, separated only by the criterion of offspring survival: women who had experienced infant child mortality (129 women with 739 children); and women who completed their reproductive period without suffering offspring loss of this nature (132 women with 668 children). The cohort without child loss had a mean parity of 5.10, lower than the average parity of 5.73 recorded for the cohort whose reproductive histories included at least 1 infant/child death. Age specific marital fertility and birth interval analyses indicated that this differential was because of biological, not behavioral, factors. The age pattern of fertility of females suffering offspring mortality failed to demonstrate a high rate of childbearing in the later age intervals of the reproductive period, a characteristic pattern of couples attempting to "replace" lost offspring. Birth interval analysis pointed to biological "interval effect," whereby infant/child mortality caused a cessation of lactation and hence a shortening of postpartum amenorrhea. Computer simulation further indicated that the higher fertility differential of the cohort experiencing offspring loss still did not result in high son survivorship values. The findings agree with earlier studies indicating that for predemographic transitional populations, economically motivated fertility strategies are ineffectual.     

Sex differentials in perinatal mortality in china and Finland

Abstract

This study describes patterns of sex differentials in perinatal mortality in China and Finland. The analysis is based on three population‐based one‐year birth cohorts, one from Qingdao, China, in 1992 and two from Northern Finland in 1966 and 1985–86, comprised of 9,219, 11,422 and 9,207 singletons with at least 28 gestational weeks and 1000 g in birthweight, respectively. Both Finnish cohorts had an excess of male over female perinatal deaths, but in the Chinese cohort girls were more likely to die than boys. The adjusted odds ratio (OR) of perinatal mortality for boys was 1.31 (95 per cent confidence interval [CI] 0.98,1.78) and 1.57 (95 per cent CI 0.89, 2.78) in the Finnish 1966 and 1985–86 cohorts, respectively, and 0.82 (95 per cent CI 0.55,1.20) in the Chinese cohort. The corresponding figure for stillbirths in the Chinese was 0.57 (95 per cent CI 0.33, 0.98), which could explain the total excess of female deaths during the perinatal period. Our results suggest that the role of different social and cultural environments on the existing sex differentials in perinatal mortality between the countries needs further evaluation.     

Birth seasonality and offspring production in threatened neotropical primates related to climate

Given the threatened status of many primate species, the impacts of global warming on primate reproduction and, consequently, population growth should be of concern. We examined relations between climatic variability and birth seasonality, offspring production, and infant sex ratios in two ateline primates, northern muriquis, and woolly monkeys. In both species, the annual birth season was delayed by dry conditions and El Niño years, and delayed birth seasons were linked to lower birth rates. Additionally, increased mean annual temperatures were associated with lower birth rates for northern muriquis. Offspring sex ratios varied with climatic conditions in both species, but in different ways: directly in woolly monkeys and indirectly in northern muriquis. Woolly monkeys displayed an increase in the proportion of males among offspring in association with El Niño events, whereas in northern muriquis, increases in the proportion of males among offspring were associated with delayed onset of the birth season, which itself was related, although weakly, to warm, dry conditions. These results illustrate that global warming, increased drought frequency, and changes in the frequency of El Niño events could limit primate reproductive output, threatening the persistence and recovery of ateline primate populations.     

Reproductive alliances and posthumous fitness enhancement in male ants

Ants provide excellent opportunities for studying the evolutionary aspects of reproductive conflict. Relatedness asymmetries owing to the haplodiploid sex determination of Hymenoptera create substantial fitness incentives for gaining control over sex allocation, often at the expense of the fitness interests of nest-mates. Under worker-controlled split sex ratios either the reproductive interests of the mother queen (when workers male bias the sex ratio) or the father (when workers female bias the sex ratio), but never that of both parents simultaneously, are fulfilled. When workers bias sex ratios according to the frequency of queen mating, males which co-sire a colony have a joint interest in manipulating their daughter workers into rearing a more female-biased sex ratio. Here we show that males of the ant Formica truncorum achieve such manipulation by partial sperm clumping, so that the cohort-specific relatedness asymmetry of the workers in colonies with multiple fathers is higher than the cumulative relatedness asymmetry across worker cohorts. This occurs because a single male fathers the majority of the offspring within a cohort. Colonies with higher average cohort-specific relatedness asymmetry produce more female-biased sex ratios. Posthumously expressed male genes are thus able to oppose the reproductive interests of the genes expressed in queens and the latter apparently lack mechanisms for enforcing full control over sperm mixing and sperm allocation.     

The influence of birth timing upon infant growth and survival in Captive Rhesus Macaques (Macaca mulatto)

Weights, growth rates, and mortality data of 815 captive-born Macaca mulattainfants were studied to determine if date of birth influences infant growth and survival. The six groups studied displayed a unimodal spring-summer birth season that has become systematically more restricted since 1977. Males exhibited higher rates of stillbirth and neonatal death and were more frequently born outside the normal birth season, when infant mortality was more common. Within the normal birth season, infant weight increased linearly with birth date, and infant growth rate declined linearly with birth date. Female infants with weights and growth rates near the developmental norm, especially those born in the middle of the birth season, have the greatest probability of survival. Males are more likely to survive if their weights and growth rates exceed the developmental norm, and thus male infants might be initially more costly to produce than female infants. These results are inconsistent with the hypothesis that offspring of high-ranking males, which conceived predominantly in the first third of the breeding season, enjoy a selective advantage.