Reproductive parameters vary with social and ecological factors in the polygynous ant Formica exsecta

Due to their haplo‐diploid sex determination system and the resulting conflict over optimal sex allocation between queens and workers, social Hymenoptera have become important model species to study variation in sex allocation. While many studies indeed reported sex allocation to be affected by social factors such as colony kin structure or queen number, others, however, found that sex allocation was impacted by ecological factors such as food availability. In this paper, we present one of the rare studies that simultaneously investigated the effects of social and ecological factors on social insect nest reproductive parameters (sex and reproductive allocation, nest productivity) across several years. We found that the sex ratio was extremely male biased in a polygynous (multiple queens per nest) population of the ant Formica exsecta. Nest‐level sex allocation followed the pattern predicted by the queen‐replenishment hypothesis, which holds that gynes (new queens) should only be produced and recruited in nests with low queen number (i.e. reduced local resource competition) to ensure nest survival. Accordingly, queen number (social factor) was the main determinant on whether a nest produced gynes or males. However, ecological factors had a large impact on nest productivity and therefore on a nest's resource pool, which determines the degree of local resource competition among co‐breeding queens and at what threshold in queen number nests should switch from male to gyne production. Additionally, our genetic data revealed that gynes are recruited back to their parental nests after mating. However, our genetic data are also consistent with some adult queens dispersing on foot from nests where they were produced to nests that never produced queens. As worker production is reduced in gyne‐producing nests, queen migration might be offset by workers moving in the other direction, leading to a nest network characterized by reproductive division of labour. Altogether our study shows that both, social and ecological factors can influence long‐term nest reproductive strategies in insect societies.     

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.     

Sex change in the Mollusca

Sex change in the Mollusca is almost exclusively protandric (male to female), and has only been reported among gastropods and bivalves. The adaptive value of protandry in these two classes most likely relates to the limited availability of females, and the consequent size-independent nature of male reproductive success (versus the size-dependent nature of reproductive success in females). In two well studied distantly related prosobranch gastropod superfamilies, Calyptracea and Patellacea, individuals of some species respond to local ecological changes by altering the age at which they change sex, although the critical ecological changes appear to be different. The physiological switch that activates sex change also appears to be different: it is found in the cemtral nervous system of the calyptracean Crepidula fornicata, and actually within the gonads of the patellacean Patella vulgata. Although the taxonomic breadth of studies on sex change is necessarily limited, and many questions remain to be answered, research on the Mollusca has produced a remarkable range of perspectives on sex change - from evolutionary to proximal; further research will benefit greatly from this breadth of knowledge.     

The proximate determinants of sex ratio in C. elegans populations

The soil nematode Caenorhabditis elegans is an example of a species in which self-fertilizing hermaphrodites predominate, but functional males continue to persist--allowing outcrossing to persevere at low levels. Hermaphrodites can produce male progeny as a consequence of sex chromosome non-disjunction or via outcrossing with males. Consequently, the genetics of sex determination coupled with the efficiency by which males find, inseminate and obtain fertilizations with hermaphrodites will influence the frequency at which males and outcrossing occurs in such populations. Behavioural and physiological traits with a heritable basis, as well as ecological characters, may influence male reproductive success and therefore sex ratio. Because sex ratio is tied to male reproductive success, sex ratio greatly affects outcrossing rates, patterns of genetic variation, and the ability of natural selection to act within populations. In this paper we explore the determinants of male frequency in C. elegans with a mathematical model and experimental data. We address the role of the genetic machinery of sex determination via sex chromosome non-disjunction on sex ratio and the influence of physiological components of C. elegans' life history that contribute to variation in sex ratio by way of male reproductive success. Finally, we discuss the short-term and long-term factors that are likely to affect sex ratio and breeding system evolution in species like C. elegans.     

Characteristic features of the reproduction of Koshima monkeys,Macaca fuscata fuscata: A summary of thirty-four years of observation

The reproductive data for Japanese monkeys,Macaca fuscata fuscata, which had been recorded for the 34 years from 1952 to 1986 on Koshima, were analyzed in terms of the influence of changes in artificial food supplies, the differences in reproductive success between females, the timing of births, and the secondary sex ratio. Koshima monkeys increased in number until 1971 when the population density was still small and artificial provisioning was copious. As described byMori (1979b), the severe reduction in artificial food supplies, which began in 1972, had an enormous deleterious effect on reproduction: the birth ratio of adult females of 5 years of age or more fell from 57% to 25%; the rate of infant mortality within 1 year of birth rose from 19% to 45%; primiparous age rose from 6 to 9 years old on average; and there was an increased death rate among adult and juvenile females. The prolonged influence of “starvation” may be seen in the significantly delayed first births of those females that were born just before the change in food supplies. When reproductive parameters are compared between the females who belonged to six lineages in the group during these periods, they were found to be rather consistent, although some individual differences can be recognized among females and subgroups. The apparent trend was that some of the most dominant females retained superior reproductive success while that of the second-ranked females has tended to diminish over the years since 1972. Such opposing trends were seen only in the most dominant lineage group and such a difference was not recognized among the females of other lineages. The difference in reproductive success is discussed in relation to both the different situations that arise because of the artificial food supplies and differences in feeding strategies. Multiparous females, after a sterile year, gave birth somewhat earlier than those who reared infants in the preceding year and, when artificial provisioning was intense, they tended to give birth a little earlier than during other periods. There is some evidence that the mortality of later-born infants was higher than that of earlier-born infants after 1972. However, this difference may not be responsible for the differential reproductive success of females since the timing of births did not differ among lineages. Furthermore, during the time when many females gave birth continuously, prior to 1972, the infant mortality did not differ with respect to the timing of births. The differences in infant mortality were not correlated with the reproductive history, parity or age of the mother, or with the sex of the infant. The secondary sex ratio varied by only a small amount, from slightly male-biased ratio (114: 100) when correlated with reproductive history, parity, age of mother, sex and survival ratio for preceding infants, timing of birth, and lineage of the female. Furthermore, the change in artificial food supplies did not cause any modifications of the secondary sex ratios, despite its enormous deleterious effect on reproduction. The secondary sex ratio of Japanese monkeys may not be influenced by the social factors mentioned.     

Skewed birth sex ratios in primates: Should high-ranking mothers have daughters or sons?

Numerous studies have been published on the skewed birth sex ratios among non-human primate populations. Sometimes the observed tendencies in sex ratio variations have been contradictory, and their adaptive significance has been controversial. Recent studies seem to reveal that the local resource competition among philopatric sex is the most important selective force affecting primate birth sex ratios. However, our understanding on this issue is still greatly hampered by the lack of exact knowledge on male reproductive success and the proximate mechanisms to vary sex ratios.     

Emerging sex allocation research in mammals: marsupials and the pouch advantage

• 1 Adaptive adjustments in offspring sex ratios in mammals have long been reported, but the conditions and mechanisms that prompt shifts in the proportion of sons and daughters born are still unclear.
• 2 Empirical evidence indicates that offspring sex in mammals can be related to a diversity of environmental and maternal traits. However, the underlying assumptions regarding offspring and maternal fitness are rarely tested.
• 3 Physiological mechanisms of maternal selection of offspring sex may occur at many stages during the prolonged maternal investment stage, and a pluralistic approach to studying mechanisms might prove fruitful.
• 4 This review highlights the apparent frequency, in marsupial mammals, of sex ratio bias, which has largely been recorded as conforming to one of a few hypotheses.
• 5 Marsupials are ideally suited to experiments involving cross‐fostering of offspring, which can allow rigorous tests of the fitness consequences of rearing one sex vs. the other. The reproductive biology of marsupials lends the group to detailed studies of the timing and physiological correlates of offspring sex biases.
• 6 Many components of metatherian biology may prove advantageous in experimental studies of sex allocation in mammals, and together may provide a prosperous avenue for examining adaptive and mechanistic hypotheses in mammalian sex allocation.

     

SEXUAL COMPOSITION and ANALYSIS OF REPRODUCTIVE FEMALES IN THE NORTH ATLANTIC RIGHT WHALE, EUBALAENA GLACIALIS, POPULATION

To test hypotheses involving reproduction and demographics, the sex of individuals must be established, but many species of Cetacea are not obviously dimorphic. In the North Atlantic right whale, Eubalaena glacialis , population, the sex of 61 males and 55 females had been determined previously by observation of the urogenital region, and the sex of 43 more females had been inferred from repeated sightings with a calf. To confirm the sex of some of these animals and to identify the sex of mote animals, genomic DNA was isolated from skin samples of 95 individual right whales (54 from among those described above and 41 additional recognizable individuals). The DNA was surveyed using the human Y-chromosome probe pDP1007. With Eco RI-digested DNA, a clear, sex-discriminating banding pattern was apparent. This method verified the sex of all 54 animals whose sex was previously known or inferred and identified the sex of an additional 41 recognizable individuals. A total of 89 male and 111 female right whales was identified in the population. The most unbiased estimate of sex ratio available is the 36 male and 34 female calves identified by genital morphology and DNA techniques. The sex ratio of this sample does not differ significantly from unity (P = 0.811). Only 38% (58/152) of the females in the North Atlantic population are known to have been reproductively successful compared with 54% in the population of right whales in the western South Atlantic. The population growth rate reported for the North Atlantic population is only 33% of that reported for right whales in the South Atlantic. Thirteen adult North Atlantic females have been identified that have not been known to calve during the past 11 yr. These data suggest that the absence of measurable recovery may be due to a combination of fewer actively reproducing females and lower reproductive rates of some females.     

Conception date affects litter type and foetal sex ratio in female moose in Estonia

1.  The Trivers–Willard model of optimal sex ratios predicts that in polygynous species mothers in better condition should produce more male than female offspring. However, empirical support for this hypothesis in mammals and especially ungulates has been equivocal. This may be because the fitness of mothers has been defined in different ways, reflecting morphological, physiological or behavioural measures of condition. In addition, factors other than maternal condition can influence a mother's fitness. Given that recent studies of wild ungulates have demonstrated the importance of the timing of conception and birth on offspring fitness, litters conceived at different stages of the rut might be expected to exhibit differences in types and embryonic sex ratio.
2.  Based on a 6-year survey of the reproductive tracts of female moose harvested in Estonia, we investigated the effect of conception date on the types of litters produced and on the foetal sex ratio.
3.  There was a clear relationship between conception date and litter characteristics. Overall, earlier conceived litters were more likely than those conceived late to contain multiple embryos and a high proportion of males. However, while foetal sex ratio varied nonlinearly with conception date in yearlings and subadults, no relationship was found in adults.
4.  We conclude that female moose adjust foetal sex ratio and litter type/size depending on their age and the date of conception, and that these adjustments are in accordance with the Trivers–Willard hypothesis if females that conceive earlier are in better condition.     

Sex-specific effects of glucose deprivation on cell-mediated immunity and reproduction in Siberian hamsters (<Emphasis Type="Italic">Phodopus sungorus</Emphasis>)

In most species, sexes differ in levels of parasitism. These differences have traditionally been believed to be static, but a capacity for adjusting anti-parasite investments would allow sexes to allocate resources adaptively contingent on environmental conditions. During stressful periods, such as a food shortage, allocation decisions would be mandated in males and females, but the biasing of resources may differ depending on the value of various physiological alternatives to the fitness of each sex. To determine whether sexes sacrifice immune or reproductive capacity when stressed, male and female Siberian hamsters (Phodopus sungorus) were pharmacologically deprived of glucose. Glucose deprivation was expected to compromise immune activity (delayed-type hypersensitivity) more than reproductive capacity in males because male fitness is limited by reproductive opportunities. The opposite was predicted for females because of the greater value of surviving to breed in favorable conditions. Contrary to expectations, glucoprivation compromised immune activity in female, but not male, hamsters. Conversely, glucoprivation reduced male, but not female, reproductive organ masses. These results may reflect the adjustments made by wild hamsters during food shortages, or they may be influenced by the study design; neither sex was permitted to incur other behavioral and physiological costs, such as lactation and parental care. Regardless, our results indicate that sex differences in parasitism are likely to be plastic in many circumstances, but further work in free-living animals is critical to ascertain whether results of the present study are naturally representative.     

Birth sex ratios relate to mare condition at conception in Kaimanawa horses

Several hypotheses have been proposed to explain variation inbirth sex ratios, based on the premise that variation is expectedwhen the profitability of raising sons and daughters variesbetween individual parents. We tested the Trivers-Willard hypothesisthat mothers in better condition produce relatively more sonsand that mothers in poorer condition produce relatively more daughterswhen male reproductive success is more variable. We examinedbirth sex ratios in relation to mare body condition at conceptionin horses in which male reproductive success is differentiallyhelped by slight advantages in condition. Horses meet the assumptionsof the Trivers-Willard hypothesis better than many species onwhich it has been tested and in which sex ratio biases are notconfounded by sexual size dimorphism such that one sex is more likelyto die in utero in females in poor condition. Mares that hada female foal were in poorer condition at conception than thosethat had a male foal, and mares that had foals of differentsexes in different years were in significantly poorer conditionwhen they conceived their female foal. There was no relationshipbetween offspring sex and mid-gestation condition, and therewas no difference in foaling rates in relation to body conditionat conception. Consequently, sex ratio deviations are not explainedby fetal loss in utero. Furthermore, differential fetal lossof the less viable sex cannot explain the greater proportionof males produced by mares in better condition. Therefore, ourresults suggest that sex ratio modification occurs at conceptionin wild horses.     

Adaptive sex ratio variation in pre-industrial human (Homo sapiens) populations?

Sex allocation theory predicts that in a population with a biased operational sex ratio (OSR), parents will increase their fitness by adjusting the sex ratio of their progeny towards the rarer sex, until OSR has reached a level where the overproduction of either sex no longer increases a parent''s probability of having grandchildren. Furthermore, in a monogamous mating system, a biased OSR is expected to lead to lowered mean fecundity among individuals of the more abundant sex. We studied the influence of OSR on the sex ratio of newborns and on the population birth rate using an extensive data set (n = 14,420 births) from pre-industrial (1775-1850) Finland. The overall effect of current OSR on sex ratio at birth was significant, and in the majority of the 21 parishes included in this study, more sons were produced when males were rarer than females. This suggests that humans adjusted the sex ratio of their offspring in response to the local OSR to maximize the reproductive success of their progeny. Birth rate and, presumably, also population growth rate increased when the sex ratio (males:females) among reproductive age classes approached equality. However, the strength of these patterns varied across the parishes, suggesting that factors other than OSR (e.g. socioeconomic or environmental factors may also have influenced the sex ratio at birth and the birth rate.     

Turtle mating patterns buffer against disruptive effects of climate change

For organisms with temperature-dependent sex determination (TSD), skewed offspring sex ratios are common. However, climate warming poses the unique threat of producing extreme sex ratio biases that could ultimately lead to population extinctions. In marine turtles, highly female-skewed hatchling sex ratios already occur and predicted increases in global temperatures are expected to exacerbate this trend, unless species can adapt. However, it is not known whether offspring sex ratios persist into adulthood, or whether variation in male mating success intensifies the impact of a shortage of males on effective population size. Here, we use parentage analysis to show that in a rookery of the endangered green turtle (Chelonia mydas), despite an offspring sex ratio of 95 per cent females, there were at least 1.4 reproductive males to every breeding female. Our results suggest that male reproductive intervals may be shorter than the 2-4 years typical for females, and/or that males move between aggregations of receptive females, an inference supported by our satellite tracking, which shows that male turtles may visit multiple rookeries. We suggest that male mating patterns have the potential to buffer the disruptive effects of climate change on marine turtle populations, many of which are already seriously threatened.     

Silence of the killers: discovery of male-killing suppression in a rearing strain of the small brown planthopper,Laodelphax striatellus

According to evolutionary theory, sex ratio distortions caused by reproductive parasites such as Wolbachia and Spiroplasma are predicted to be rapidly normalized by the emergence of host nuclear suppressors. However, such processes in the evolutionary arms race are difficult to observe because sex ratio biases will be promptly hidden and become superficially unrecognizable. The evolution of genetic suppressors has been reported in just two insect species so far. In the small brown planthopper, Laodelphax striatellus, female-biases caused by Spiroplasma, which is a ‘late’ male-killer, have been found in some populations. During the continuous rearing of L. striatellus, we noted that a rearing strain had a 1 : 1 sex ratio even though it harboured Spiroplasma. Through introgression crossing experiments with a strain lacking suppressors, we revealed that the L. striatellus strain had the zygotic male-killing suppressor acting as a dominant trait. The male-killing phenotype was hidden by the suppressor even though Spiroplasma retained its male-killing ability. This is the first study to demonstrate the existence of a late male-killing suppressor and its mode of inheritance. Our results, together with those of previous studies, suggest that the inheritance modes of male-killing suppressors are similar regardless of insect order or early or late male killing.     

Spiders do not escape reproductive manipulations by Wolbachia

Background  

Maternally inherited bacteria that reside obligatorily or facultatively in arthropods can increase their prevalence in the population by altering their hosts' reproduction. Such reproductive manipulations have been reported from the major arthropod groups such as insects (in particular hymenopterans, butterflies, dipterans and beetles), crustaceans (isopods) and mites. Despite the observation that endosymbiont bacteria are frequently encountered in spiders and that the sex ratio of particular spider species is strongly female biased, a direct relationship between bacterial infection and sex ratio variation has not yet been demonstrated for this arthropod order.     

Low Socioeconomic Status and Female-Biased Parental Investment: The Mukogodo Example

Hierarchies of wealth and ethnic prestige among East African herders present an opportunity to test the Trivers-Willard hypothesis that low socioeconomic status should correlate with female biases in parental investment. The Mukogodo are at the bottom of such a regional hierarchy due to their poverty and low status as former hunters. As a result of these factors, Mukogodo men have lower polygyny rates than their neighbors, and Mukogodo women have higher mean reproductive success than Mukogodo men. The data fulfill the prediction that there should be a bias in parental investment in favor of daughters. The sex ratio of the 0–4 age group and the reported sex ratio at birth are both female-biased. Although there is no evidence of infanticide, sons may be neglected in favor of daughters. Evidence from a dispensary and from a clinic run by a Catholic mission both show that the Mukogodo take daughters for treatment more often than they take sons. Also, daughters may be nursed longer than sons.     

Sons are made from old stores: sperm storage effects on sex ratio in a lizard

Sperm storage is a widespread phenomenon across taxa and mating systems but its consequences for central fitness parameters, such as sex ratios, has rarely been investigated. In Australian painted dragon lizards (Ctenophorus pictus), we describe elsewhere that male reproductive success via sperm competition is largely an effect of sperm storage. That is, sperm being stored in the female reproductive tract out-compete more recently inseminated sperm in subsequent ovarian cycles. Here we look at the consequences of such sperm storage for sex allocation in the same species, which has genetic sex determination. We show that stored sperm have a 23% higher probability of producing sons than daughters. Thus, shifts in sex ratio, for example over the reproductive season, can partly be explained by different survival of son-producing sperm or some unidentified female mechanism taking effect during prolonged storage.     

Mating frequency, genetic structure, and sex ratio in the intermorphic female producing ant species Myrmecina nipponica

1. Myrmecina nipponica has two types of colonies: a queen colony type, in which the reproductive females are queens and new colonies are made by independent founding, and an intermorphic female colony type, in which reproductive females belong to a wingless intermediate morphology between queen and worker, and where colonies multiply through colonial budding. 2. The mating frequencies of reproductive females in both types indicate monoandry. The relatedness among nestmates in both types was almost 0.75, however relatedness between mother and daughter in intermorphic female colonies was slightly higher than that of queen colonies. 3. The sex ratio (corrected investment female ratio) was 0.70 at the population level, suggesting that the sex ratio is controlled by workers in this species, however the ratio differed greatly between the two types of colonies. Queen colonies (n = 37) had a female‐biased sex ratio of 0.77 while intermorphic female colonies (n = 33) had a ratio of 0.56. 4. Each reproductive intermorphic female was accompanied by an average of 2.9 workers (including virgin intermorphic females) in the colonial budding, and when the investment to those workers was added to the female investment, the sex ratio reached 0.81. 5. The frequency distribution of sex ratio was bimodal, with many colonies producing exclusively males or females, however mean estimated relatedness within colonies was almost 0.75. These data are inconsistent with the genetic variation hypothesis, which is one of the predominant hypotheses accounting for the between‐colony variation in sex ratio.     

Facultative adjustment of mammalian sex ratios in support of the Trivers-Willard hypothesis: evidence for a mechanism

Evolutionary theory predicts that mothers of different condition should adjust the birth sex ratio of their offspring in relation to future reproductive benefits. Published studies addressing variation in mammalian sex ratios have produced surprisingly contradictory results. Explaining the source of such variation has been a challenge for sex-ratio theory, not least because no mechanism for sex-ratio adjustment is known. I conducted a meta-analysis of previous mammalian sex-ratio studies to determine if there are any overall patterns in sex-ratio variation. The contradictory nature of previous results was confirmed. However, studies that investigated indices of condition around conception show almost unanimous support for the prediction that mothers in good condition bias their litters towards sons. Recent research on the role of glucose in reproductive functioning have shown that excess glucose favours the development of male blastocysts, providing a potential mechanism for sex-ratio variation in relation to maternal condition around conception. Furthermore, many of the conflicting results from studies on sex-ratio adjustment would be explained if glucose levels in utero during early cell division contributed to the determination of offspring sex ratios.