Extra-pair paternity, offspring mortality and offspring sex ratio in the socially monogamous coal tit (Parus ater)

Females of many socially monogamous bird species commonly engage in extra-pair copulations. Assuming that extra-pair males are more attractive than the females’ social partners and that attractiveness has a heritable component, sex allocation theory predicts facultative overproduction of sons among extra-pair offspring (EPO) as sons benefit more than daughters from inheriting their father’s attractiveness traits. Here, we present a large-scale, three-year study on sex ratio variation in a passerine bird, the coal tit (Parus ater). Molecular sexing in combination with paternity analysis revealed no evidence for a male-bias in EPO sex ratios compared to their within-pair maternal half-siblings. Our main conclusion, therefore, is that facultative sex allocation to EPO is absent in the coal tit, in accordance with findings in several other species. Either there is no net selection for a deviation from random sex ratio variation (e.g. because extra-pair mating may serve goals different from striving for ‘attractiveness genes’) or evolutionary constraints preclude the evolution of precise maternal sex ratio adjustment. It is interesting to note that, however, we found broods without EPO as well as broods without mortality to be relatively female-biased compared to broods with EPO and mortality, respectively. We were unable to identify any environmental or parental variable to co-vary with brood sex ratios. There was no significant repeatability of sex ratios in consecutive broods of individual females that would hint at some idiosyncratic maternal sex ratio adjustment. Further research is needed to resolve the biological significance of the correlation between brood sex ratios and extra-pair paternity and mortality incidence, respectively.     

The interplay of sex ratio, male success and density-independent mortality affects population dynamics

Environmental constraints can limit a population to a certain size, which is usually called the carrying capacity of a habitat. Besides to this ‘external’ factor, which is mainly determined by the limitation of resources, we investigate here another set of population-intrinsic factors that can limit a population size significantly below the maximum sustainable size. Firstly, density-independent mortality is a prominent factor in all organisms that show age-related and/or accidental death. Secondly, in sexually reproducing organisms the sex ratio and the success of pairing is important for finding reproductive partners. Using a simple model, we demonstrate how sex ratio, mating success and gender-specific mortality can strongly affect the speed of population growth and the maximum population size. In addition, we demonstrate that density-independent mortality, which is often neglected in population models, adds a very important feature to the system: it strongly enhances the negative influence of unbiased sex ratios and inefficient pairing to the maximum sustainable population size. A decrease of the maximum population size significantly affects a population's survival chance in inter-specific competition. Thus, we conclude that the inclusion of density-independent mortality is crucial, especially for models of species that reproduce sexually. We show that density-independent mortality, together with biased sex ratios, can significantly lower the abilities of a population to survive in conditions of strong inter-specific competition and due to the Allee effect. We emphasize that population models should incorporate the sex ratio, male success and density-independent mortality to make plausible predictions of the population dynamics in a gender-structured population. We show that the population size is limited by these intrinsic factors. This is of high ecological significance, because it means that there will always be resources available in any habitat that allows other species (e.g., invaders) to use these resources and settle successfully, if they are sufficiently adapted.     

Effects of food availability on dispersal and cub sex ratio in the Mednyi Arctic fox

Since the Pleistocene, Arctic foxes, Alopex lagopus, on Mednyi Island in the North Pacific have been isolated in a small area with rich food resources and no other terrestrial carnivores. This situation provides an unusually simple system within which the effect of food dispersion on demography and social organisation was examined. We studied the composition, location and dispersal of 67 Arctic fox groups and mapped their major food resources (seabird colonies) during 1994–2000 on Mednyi. We compared our observations with the predictions of models of sex-ratio determination. Our observations are most consistent with the predictions of Julliard's (2000) model, where mothers are expected to produce more offspring of the most dispersing sex in low-quality habitats, and more offspring of the most philopatric sex in high-quality habitats. The polygynous foxes on Mednyi Island lived where the principal food resources were patchily distributed (present on 11% of the shoreline), and cub survival to dispersal age or reproductive adult was higher in rich (25/45) than in poor (24/79) home ranges. Furthermore, dispersal was strongly sex-biased: most females (60%) remained on their natal ranges, whereas very few males (9%) did so. Significantly more female than male cubs (54 compared with 24) emerged from dens in resource rich ranges, whereas the sex ratio on poor ranges was approximately equal (51 females and 56 males). While our observations are also to some extent consistent with the local resource enhancement (LRE) hypothesis (which predicts a bias towards the sex most likely to cooperate with parents), this does not account for the observed spatial variability.     

Dual mechanism of queen influence over sex ratio in the ant Pheidole pallidula

Social Hymenoptera are general models for the study of parent-offspring conflict over sex ratio, because queens and workers frequently have different reproductive optima. The ant Pheidole pallidula shows a split distribution of sex ratios with most of the colonies producing reproductives of a single sex. Sex ratio specialization is tightly associated with the breeding system, with single-queen (monogynous) colonies producing male-biased brood and multiple-queen (polygynous) colonies female-biased brood. Here, we show that this sex specialization is primarily determined by the queens influence over colony sex ratio. Queens from monogynous colonies produce a significantly more male-biased primary sex ratio than queens from polygynous colonies. Moreover, queens from monogynous colonies produce a significantly lower proportion of diploid eggs that develop into queens and this is associated with lower rate of juvenile hormone (JH) production compared to queens from polygynous colonies. These results indicate that queens regulate colony sex ratio in two complementary ways: by determining the proportion of female eggs laid and by hormonally biasing the development of female eggs into either a worker or reproductive form. This is the first time that such a dual system of queen influence over colony sex ratio is identified in an ant.     

The sex in short supply for matings varies over small spatial scales in a katydid (Kawanaphilanartee, Orthoptera: Tettigoniidae)

In katydids such as Kawanaphilanartee, a female bias in the operational sex ratio (OSR) results in female competition for mates and male choice of mates. Previous work showed that the excess of sexually active females occurs when food availability is low, in part because less food increases the propensity of females to mate as they forage for the large edible spermatophores produced by males. In this study with K.nartee, a pollen-feeding species, we estimate natural variation in numbers of sexually active males and females by assessing male calling activity and the propensity of females to respond to experimental calling males. We found an excess of sexually active males at a site with many flowers and an excess of sexually active females at a site with few flowers about 900 m away. Between-site differences in gut masses of calling males were consistent with the hypothesis that pollen availability controls OSR. Finally, at a third site where flowers were at first scarce, we found that the initial excess in sexually active females changed to an excess of sexually active males after a clump of grass-trees flowered. The mean gut mass of all sampled males from this site increased after flowering. The large variation in OSR that we document for K. nartee highlights the importance of identifying the appropriate spatial and temporal scales over which OSRs are measured in studies of factors controlling sexual selection. Received: 13 May 1997 / Accepted after revision: 27 October 1997     

Removal process estimation of population size for a population with a known sex ratio

A removal model for estimating population size which uses the known population sex ratio is studied. A maximum likelihood estimate and an optimal martingale estimate of the population size are proposed. Their standard errors and large sample properties are obtained. Simulation studies are reported, and the performance of the proposed estimators are compared with the standard maximum likelihood estimator which ignores the sex ratio information. An example on a capture study of deer mice is given.     

Tests for a biased sex ratio when the data are clustered

In behavioral ecology the overall sex ratio in a population of birds is often tested to see if it differs from a 50/50 ratio. In recent publications the binomial test or the ² test are carried out although the sexes of chicks within the same nest may not be independent. The lack of independence occurs since female birds can adjust the sex ratio in an adaptive way as demonstrated in recent studies. In order to take dependence into consideration the Wilcoxon signed rank test based on the within-brood differences between the proportions of sons and daughters was performed in a study investigating great tit hatchling sex ratios. We compare this test with a test based on an optimally weighted estimator recently proposed for medical studies with clustered binary data. According to our simulation results, this novel test is more powerful than the Wilcoxon signed rank test and should be used for the analysis of avian sex ratios. The methods are illustrated with real data from the great reed warbler.     

Human digit ratios depend on birth order and sex of older siblings and predict maternal fecundity

In men, the length ratio of the second to fourth finger (2D:4D) is smaller, while the length of the fourth finger relative to body height (4D:H) is larger than in women. Inter- and intrasexual variations in 2D:4D and 4D:H may depend on variation in fetal androgen and oestrogen environment. As maternal physiology varies with parity and is differentially affected by gestation of either sex, offspring 2D:4D and 4D:H may change according to sex and number of older siblings and may predict subsequent maternal performance. We analysed 2D:4D and 4D:H in Caucasian university students. 2D:4D was smaller and 4D:H was larger in males than in females, but no sexual dimorphism existed in 2D:H. In males, length ratios did not vary with birth order. 2D:4D became more masculine with increasing proportion of males among older siblings, and 2D:4D and 4D:H became more feminine as the number of older sisters increased. In females, length ratios did not vary with the number of older sisters or brothers. 2D:4D was also not related to birth order, but 4D:H became more masculine with birth order. In females, residual maternal fecundity (number of maternal offspring after the participant) decreased as 4D:H became more masculine. These findings are partly consistent with those from previous studies and suggest that maternal fecundity co-varies with length ratios and thus possibly fetal hormone environment of older offspring. 2D:4D and 4D:H may therefore represent powerful tools to investigate the relationships between fetal environment, offspring phenotype and maternal life history at mechanistic and evolutionary levels.     

Variance in female quality, operational sex ratio and male mate choice in a bushcricket

Male bushcrickets, Kawanaphila nartee, exercise mate choice when nutrients are limited. Male mate choice is associated with a female-biased operational sex ratio (OSR) that arises from an increased relative paternal investment under nutrient limitation. However, increased male choosiness could be attributable to the fact that females vary more in fecundity, and consequently in mate quality, when nutrient limited. Our objective was to experimentally partition the influences of OSR (male or female bias) and variance in mate quality (high or low) and to assess their relative influence on the intensity of mate choice by male bushcrickets. Female quality was manipulated by controlled feeding regimes that directly affected female fecundity. We found that males and females engaged in sexual interactions sooner under a male-biased than a female-biased OSR. Males were more likely to reject females on their first encounter when variance in female quality was high. However, the effect of quality variance on the total number of rejections during a 4-h observation period was dependent on the perceived OSR. A male's prior experience of variance in female quality did not influence male choosiness. Our observed rates of mate rejection conformed well with those predicted from recent theoretical models of sexual differences in choosiness. In conclusion, our results show that the opportunity for selection via male mate choice is influenced by an interaction between OSR and the variance in mate quality that arises within nutrient-limited populations of females. Received: 5 January 1998 / Accepted after revision: 25 October 1998     

Adult sex ratio affects divorce rate in the monogamous endoparasite Schistosoma mansoni

“Divorce” (mate switching) rate is known to vary largely both between and within socially monogamous species. Although the adult sex ratio can have an important influence on mating patterns, very few studies have investigated the influence of sex ratio on divorce rate in monogamous species, and even less so from an experimental point of view. In addition, most studies on the causes and consequences of divorce have been performed on vertebrate species, whereas data for invertebrate monogamous species remain scarce. Schistosoma mansoni is a monogamous endoparasite with a complex life cycle characterized by asexual reproduction in the intermediate host and sexual reproduction in the definitive host. In the wild, populations of S. mansoni inside their definitive hosts are characterized by a male-biased sex ratio. We studied the influence of experimentally varying the adult sex ratio on divorce rate in S mansoni, using controlled infections of hosts with clonal populations. The more male-biased the sex ratio was, the more the divorce rate increased, whereas no such effect was observed under a female-biased sex ratio. In this study and for the first time, we showed, by handling the sex ratio, that the divorce rate increases in adult male-biased sex ratio conditions in a monogamous species.     

Offspring sex ratio variation in the bridled nailtail wallaby, Onychogalea fraenata

The bridled nailtail wallaby is a sexually size dimorphic, promiscuous, solitary macropod. Sex ratios of pouch young were studied at two sites over 3 years, beginning with 14 months of severe drought. Females that were in better condition were more likely to have sons, and condition was dependent on body size. Females at one site were heavier, were consequently in better condition, and produced more sons than females at the other site. Females that declined in condition had more daughters during the most severe part of the drought than females that maintained condition, but endoparasite infection did not affect the pouch young sex ratio. Age also appeared to affect sex ratio adjustment, because weight was strongly influenced by age. Sex ratio bias was not caused by early offspring mortality, but occurred at conception. Mothers did not appear to bias energy expenditure on sons or daughters; males and females did not differ in condition at the end of pouch life. Pouch young sex ratio variation was most consistent with the Trivers-Willard hypothesis, but could also have been influenced by local resource competition, since sons dispersed further than daughters. Offspring condition was related to survival, and was correlated with maternal condition. Received: 14 April 1998 / Accepted after revision: 10 November 1998     

Birth sex ratios in sheep over nine lambing seasons: years 7–9 and the effects of ageing

The birth sex ratio of a commercial flock of Suffolk cross sheep, Ovis aries, was studied over nine consecutive lambing seasons. In all data from 2704 lambs were recorded and analysed. The overall (1985–1993) birth sex ratio was 49.96% male lambs. Ewes with single lambs produced significantly more males (53.04%) than ewes with triplets (45.54% male). A significant positive correlation was found between the flock age and the birth sex ratio (1985–1992). As the flock aged the birth sex ratio changed from female biased to male biased, remained male biased for a number of years, and then became female biased again. This pattern is evident first in single, then in twin and later in triplet births. Among like sex twins (males and females) (1985–1993) more males (53.88%) were born in the first half and more females (45.57% males) in the second half of the lambing season. The difference between the two halves is significant.     

Spatial and space-time scan statistics to detect low rate clusters of sex ratio

Whether general environmental exposures to endocrine disrupting chemicals (including pesticides and dioxin) might induce decreased sex ratios (male/female ratio at birth) is discussed. To address this issue, the authors looked for a space-time clustering test which could detect local areas of significantly low risk, assuming a Bernoulli distribution. As a matter of fact, if the endocrine disruptor hypothesis holds true, and if the sex ratio is a sentinel health event indicative of new reproductive hazards ascribed to environmental factors, then in a given region, either a cluster of low male/female ratio among newborn babies would be expected in the vicinity of polluting municipal solid waste incinerators (MSWIs) (supporting the dioxin hypothesis), or local clusters would be expected in some rural areas where large amounts of pesticides are sprayed. Among cluster detection tests, the spatial scan statistic has been widely used in various applications to scan for areas with high rates, and rarely (if ever) with low rates. Therefore, the goal of this paper was to check the properties of the scan statistics under a given scenario (Bernoulli distribution, search for clusters with low rates) and to assess its added value in addressing the sex ratio issue. This study took place in the Franche-Comté region (France), mainly rural, comprising three main MSWIs, among which only one had high dioxin emissions level in the past. The study population consisted of 192,490 boys and 182,588 girls born during the 1975–1999 period. On the whole, the authors conclude that: (i) spatial and space-time scan statistics provide attractive features to address the sex ratio issue; (ii) sex ratio is not markedly affected across space and does not provide a reliable screening measure for detecting reproductive hazards ascribed to environmental factors.     

Paternal expenditure is related to brood sex ratio in polygynous great reed warblers

In many polygynous animals, parents invest more heavily in individual sons than in daughters. However, it is unclear if these differences in investment are a consequence of sex differences in the demand of offspring related to sexual size dimorphism or a consequence of parental manipulation. Here, we report on parental food delivery frequency in relation to brood size and brood sex ratio in a wild population of polygynous great reed warblers Acrocephalus arundinaceus. We used the polymorphic microsatellite loci on the Z chromosome to sex chicks. We found that paternal feeding frequency (times/h per nest) increased not with brood size, but with the proportion of males in the brood, although the demand per nest was more closely related to brood size than to brood sex ratio. Additionally, the increase in rate of paternal feeding frequency in relation to the brood sex ratio was much higher than the increase in rate of nestling food demands. Maternal feeding frequency was independent of both brood size and brood sex ratio. These results strongly suggest that fathers preferentially invest in their sons. We propose that parents can afford sex-biased parental care in animals in which food provisioning is enough for all offspring to survive. Received: 22 January 1996/Accepted after revision: 30 June 1996     

Relatedness and sex ratio in a primitively eusocial halictine bee

Lasioglossum laevissimum was studied in Calgary, Alberta, where it is eusocial with one worker brood. Estimates of relatedness were obtained among various categories of nestmate based upon four polymorphic enzyme loci, two of which exhibited significant levels of linkage disequilibrium. Relatedness estimates among workers and among reproductive brood females were very close to the expected 0.75 value that obtains when nests are headed by one, singly mated queen. However, relatedness between workers and the reproductive brood females they reared was significantly lower than 0.75. A low frequency of orphaning with subsequent monopolisation of oviposition by one worker brood female in orphaned nests may explain these results. Workers were significantly more and queens significantly less closely related to male reproductives than expected if all males were to have resulted from queen-laid eggs. Orphaning and worker-produced males contribute to this result. The sex investment ratio was 1:2.2 in favour of females, in excellent agreement with the predictions based upon relative relatednesses between workers and reproductive brood males and females. Adaptive intercolony variation in investment ratios was detected: the sex ratio was more heavily female-biased in nests in which the relative relatedness asymmetry between workers and reproductive brood was more female-biased. The study species is the most weakly eusocial hymenopteran for which relatedness estimates and sex ratio data are available. With high relatedness among nestmates and a strongly female-biased sex ratio, this study suggests the importance of indirect fitness contributions in the early stages of social evolution. Correspondence to: L. Packer     

Clutch loss affects the operational sex ratio in the strawberry poison frog Dendrobates pumilio

Both modelling and field data from three breeding seasons show that an environmental factor, clutch loss (CL), affects the operational sex ratio (OSR) and therefore male mating frequency in strawberry poison frogs. Clutch loss affects the length of reproductive cycles of both sexes: with increasing clutch losses, males spend proportionately more time than females in parental investment activities. Because of this, males spend relatively less time in the mating pool, i.e. exhibit proportionately more time-out than females in comparison to a situation with low or no clutch loss. Hence, clutch loss leads to a less male-biased OSR, coupled with a decrease in the opportunity for sexual selection. Furthermore, this study resolves an apparent paradox, the negative correlation between mating frequency and reproductive success (=number of produced tadpoles) of individual males in one breeding season. Clutch loss decouples the correlation between mating frequency and reproductive success because females re-enter the mating pool when they lose their offspring. However, clutch loss diminishes the reproductive output. Similar consequences of clutch loss on the OSR may be true for many species where both sexes reproduce frequently in one breeding season.Communicated by J. Christensen-Dalsgaard     

Offspring sex ratio in relation to female size in southern elephant seals,Mirounga leonina

Southern elephant seals Mirounga leonina display extreme sexual dimorphism. In addition females show great variation in size and stored resources at parturition. Therefore they present an excellent opportunity for examination of responses of sex ratio to resource availability. We studied the relationships between the size of southern elephant seal females at parturition and the size and sex of their pups at South Georgia over four breeding seasons. We found a large individual variation in maternal post-partum mass (range 296–977 kg, n=151). Larger mothers gave birth to larger pups, irrespective of the sex of their pup. Male pups were on average 14% larger than females at birth and consequently more costly to bring to parturition. Our results suggest that female southern elephant seals must weigh more than 300 kg if they are to breed at all, and more than 380 kg if they are to give birth to a male pup. Above this threshold the proportion of males among offspring rapidly increases with maternal mass, and stabilizes at a level not significantly different from parity. These results show that smaller females of southern elephant seals vary offspring sex ratio in a way that is consistent with theories on adaptive offspring sex ratio. A smaller mother with a male foetus may benefit from terminating her pregnancy and allocating the resources she saves to her own growth. She could then give birth to and raise a larger pup in the subsequent season.     

Test of the adaptiveness of sex ratio manipulation in a parasitoid wasp

In behavioral ecology it is generally assumed that behavior is adaptive. This assumption is tested here for sex ratio manipulation in response to host size in the parasitoid wasp Spalangia cameroni. Females produce a greater proportion of daughters on larger hosts. If this behavior is adaptive, it is not through a positive effect of host size on the fitness of daughters, as theory suggests and as found for other species. Females that developed on larger hosts were not more successful at drilling into hosts, were not more successful at interspecific competition for hosts, and did not have greater dispersal ability as measured by wing loading (weight/area of wing and thorax). The possibility that S. cameroni's sex ratio manipulation may be adaptive through a negative effect of host size on the fitness of sons cannot be ruled out. Relative to males from larger hosts, males from smaller hosts had lower wing loading and thus potentially greater dispersal ability. The actual effect of wing loading on fitness remains to be tested.     

Birth sex ratios in toque macaques and other mammals: integrating the effects of maternal condition and competition

Mammalian life histories suggest that maternal body condition and social dominance (a measure of resource-holding potential) influence the physical and social development of offspring, and thereby their reproductive success. Predictably, a mother should produce that sex of offspring which contributes most to her fitness (as measured by the number of her grandchildren) and that she is best able to raise within the constraints imposed by her condition, social rank, and environment. Such combined effects were investigated by monitoring variations in body condition (weight) and behavior of female toque macaques, Macaca sinica of Sri Lanka, in a changing forest environment over 18 years. Maternal rank, by itself, had no influence on offspring sex, but did affect maternal body condition. The combined effects of rank and condition indicated the following: mothers in robust condition bore more sons, whereas those in moderate condition bore more daughters, but both effects were expressed most strongly among mothers of high rank. Where the consequences of low rank were felt most acutely, as shown by poor condition, mothers underproduced daughters. Environmental quality directly influenced rank and condition interactions, and thus sex ratios. These relationships, and data from other mammals suggest an empirically and theoretically consistent pattern of sex allocation in mammals. New predictions integrate effects, proposed by Trivers and Willard, that are rooted in male mate competition, which is universal among polygynous mammals, with those of local resource competition (and/or female reproductive competition), which are not universal and differ in intensity between the socioecologies and local environments of different species. Received: 30 May 1998 / Accepted after revision: 29 August 1998     

Biased primary sex ratio in the bushcricket Poecilimon veluchianus,an insect with sex chromosomes

Offspring sex ratio at hatching was examined in the bushcricket Poecilimon veluchianus. Offspring sex ratios varied significantly between females (Fig. 1). Low mortality prior to sex determination established that this heterogeneity was already present in the primary offspring sex ratio. Sperm age and female age had no influence on offspring sex ratio (Fig. 2). Male age at copulation, however, correlated significantly with offspring sex ratio (Fig. 3). There were two types of males: one type produced predominantly daughters when young and an increasing proportion of sons with age. The other type produced, independent of age, 1:1 offspring sex ratios (Fig. 4). The two types of males seem to occur in approximately equal numbers. Sex ratio variation (1) may adaptively compensate for local sex ratio biases caused by sex-specific motility, or (2) it may be adaptive if there is a sex-differential effect of laying date on offspring fitness. Received: 14 March 1996/Accepted after revision: 24 June 1996