Birth sex ratio in captive mammals: Patterns,biases, and the implications for management and conservation

Sex allocation theory predicts that a female should produce the offspring of the sex that most increases her own fitness. For polygynous species, this means that females in superior condition should bias offspring production toward the sex with greater variation in lifetime reproductive success, which is typically males. Captive mammal populations are generally kept in good nutritional condition with low levels of stress, and thus populations of polygynous species might be expected to have birth sex ratios biased toward males. Sex allocation theory also predicts that when competition reduces reproductive success of the mother, she should bias offspring toward whichever sex disperses. These predicted biases would have a large impact on captive breeding programs because unbalanced sex ratios may compromise use of limited space in zoos. We examined 66 species of mammals from three taxonomic orders (primates, ungulates, and carnivores) maintained in North American zoos for evidence of birth sex ratio bias. Contrary to our expectations, we found no evidence of bias toward male births in polygynous populations. We did find evidence that birth sex ratios of primates are male biased and that, within primates, offspring sex was biased toward the naturally dispersing sex. We also found that most species experienced long contiguous periods of at least 7 years with either male‐ or female‐biased sex ratios, owing in part to patterns of dispersal (for primates) and/or to stochastic causes. Population managers must be ready to compensate for significant biases in birth sex ratio based on dispersal and stochasticity. Zoo Biol 19:11–25, 2000. © 2000 Wiley‐Liss, Inc.     

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.     

Female common lizards (Lacerta vivipara) do not adjust their sex-biased investment in relation to the adult sex ratio

Sex allocation theory predicts that facultative maternal investment in the rare sex should be favoured by natural selection when breeders experience predictable variation in adult sex ratios (ASRs). We found significant spatial and predictable interannual changes in local ASRs within a natural population of the common lizard where the mean ASR is female-biased, thus validating the key assumptions of adaptive sex ratio models. We tested for facultative maternal investment in the rare sex during and after an experimental perturbation of the ASR by creating populations with female-biased or male-biased ASR. Mothers did not adjust their clutch sex ratio during or after the ASR perturbation, but produced sons with a higher body condition in male-biased populations. However, this differential sex allocation did not result in growth or survival differences in offspring. Our results thus contradict the predictions of adaptive models and challenge the idea that facultative investment in the rare sex might be a mechanism regulating the population sex ratio.     

Pterygodermatites nycticebi infections in golden lion tamarins (Leontopithecus rosalia rosalia) and aye‐ayes (Daubentonia madagascariensis) from a German zoo

In a golden lion tamarin (Leontopithecus rosalia rosalia) colony kept indoors in a German zoo, two animals presented a sudden onset of reduced general condition, lethargy, and diarrhea. At animal capture for clinical examination, adult nematode stages were observed after stress‐induced defecation. Despite treatment, two golden lion tamarins died in the following 2 days. At necropsy, spirurid stages were found in the lungs and intestine. Additionally, adult Pterygodermatites spp. were identified in histopathological samples of intestine and pancreas, confirming the previous diagnosis. Upon diagnosis, all animals were treated with ivermectin (0.2 mg/kg; SC). Thereafter, the general condition of the golden lion tamarins improved, whereby some of them excreted spirurid nematodes over 3 days. Four weeks after treatment, 20 fecal samples from the colony were examined and proved negative for parasitic stages. Given that common German cockroaches (Blattella germanica) are suitable intermediate hosts of Pterygodermatites nycticebi, 30 specimens were collected from seven different locations around the golden lion tamarins housing. Third‐stage larvae of Pterygodermatites spp. were recovered from those cockroaches. Regular anthelmintic treatments, coprological screenings, and controls for intermediate hosts were recommended. More than 2 years later, P. nycticebi infection was diagnosed again histopathologically in an aye‐aye (Daubentonia madagascariensis) which suddenly died. Coprological analysis confirmed the presence of spirurid eggs. Due to prosimian primates' cockroach‐eating habits and given that total cockroach eradication proved impossible, continuous cockroach control strategies and regular treatments of primates are currently performed to prevent further P. nycticebi infections.     

Female resistance behaviour and progeny sex ratio in two Bradysia species (Diptera: Sciaridae) with paternal genome elimination

The relationship between female mating preferences and sex allocation has received considerable theoretical and empirical support. Typically, choosier females adjust their progeny sex ratio towards sons, who inherit the attractive traits of their father. However, in species with paternal genome elimination, where male sperm do not contain the paternal genome, predictions for the direction of progeny sex ratio biases and their relationship with female choosiness are atypical. Paternal genome elimination also creates a potential for male–female conflict over sex allocation, and any influence of female mate choice on sex ratio outcomes have interesting implications for sexually antagonistic coevolution. Within the Sciaridae (Diptera) are species that produce single‐sex progeny (monogenic species) and others in which progeny comprise both sexes (digenic species). Paternal genome elimination occurs in both species. We explore female mate resistance behaviour in a monogenic and digenic species of mushroom gnat from the genus Bradysia. Our experiments confirmed our theoretical predictions, revealing that in the monogenic and digenic species, females producing female‐biased progeny were more likely to have resisted at least one mating attempt.     

Mechanisms that influence sex ratio variation in the invasive hymenopteran Sirex noctilio in South Africa

Sirex noctilio is an economically important invasive pest of commercial pine forestry in the Southern Hemisphere. Newly established invasive populations of this woodwasp are characterized by highly male‐biased sex ratios that subsequently revert to those seen in the native range. This trend was not observed in the population of S. noctilio from the summer rainfall regions in South Africa, which remained highly male‐biased for almost a decade. The aim of this study was to determine the cause of this persistent male bias. As an explanation for this pattern, we test hypotheses related to mating success, female investment in male versus female offspring, and genetic diversity affecting diploid male production due to complementary sex determination. We found that 61% of females in a newly established S. noctilio population were mated. Microsatellite data analysis showed that populations of S. noctilio from the summer rainfall regions in South Africa are far less genetically diverse than those from the winter rainfall region, with mean Nei's unbiased gene diversity indexes of 0.056 and 0.273, respectively. These data also identified diploid males at low frequencies in both the winter (5%) and summer (2%) rainfall regions. The results suggest the presence of a complementary sex determination mechanism in S. noctilio, but imply that reduced genetic diversity is not the main driver of the male bias observed in the summer rainfall region. Among all the factors considered, selective investment in sons appears to have the most significant influence on male bias in S. noctilio populations. Why this investment remains different in frontier or early invasive populations is not clear but could be influenced by females laying unfertilized eggs to avoid diploid male production in populations with a high genetic relatedness.     

Haematological and metabolic profiles associated with age and sex in giant kokopu (Galaxias argenteus) (Gmelin 1789) broodstock

This study characterized selected peripheral blood (PB) haematological parameters, liver, serum and muscle metabolic features in 3- and 5-year-old male and female giant kokopu (Galaxias argenteus) broodstock reared indoor at 16°C. Sex and age did not affect PB total cell count and haematocrit values. Nonetheless, higher erythrocytes in 5-year-old fish, elevated thrombocyte and lymphocyte counts in 3-year-old fish indicate age-specific cellular regulation. Higher thrombocyte counts in female fish suggest sex-specific regulation. At a metabolic level, liver abundance for long chain saturated fatty acids (FAs) was higher in males, whereas females had elevated levels of polyunsaturated FAs. Essential and non-essential amino acids (AAs) in liver and serum were also elevated in females compared to males. These findings suggest differential allocation of FAs and AAs to reflect requirements for gonadal, development and provisioning. Similarly, age significantly resulted in higher liver and serum abundances of some non-essential AAs in 3-year-olds compared to 5-year-old fish, suggesting higher metabolism in younger fish. Overall, results enhance our understanding of sex- and age-based differences in fish haematology, muscle, liver, and serum metabolite profiles in healthy G. argenteus. Future studies should carefully consider potential age- and sex-specific differences in metabolic responses.     

A comparison of sex ratio,birth periods and calf survival among Serengeti wildebeest sub‐populations,Tanzania

Although adaptation and environmental conditions can easily predict demographic variation in most savannah ungulates, no study on demographic consequences arising from natural and anthropogenic factors among Serengeti wildebeest (Connochaetes taurinus) sub‐populations in Tanzania has been carried out. Here, I report estimates of annual sex ratio, calf and yearling survival rate and birth seasonality between resident and migratory sub‐populations to explore demographic patterns arising from the different age and sex structure. The results indicate significantly higher female‐biased sex ratios in the resident and almost even sex ratios among individual migrants. The calf recruitment estimated as mother: offspring ratios indicate a more synchronous birth in the migrant than the resident sub‐population. Also, birth seasonality in the migratory sub‐population coincided with seasonal variability of rainfall and the timing of the birth peak was more variable in the migrants than the resident sub‐population. The migratory sub‐population had a higher annual proportional mean calf survival estimate (0.84) than that of the residents (0.44) probably due to higher mortality resulting from predation in the western corridor. However, the proportion of yearling survival estimates was much lower (0.31) in the migrants and relatively higher (0.39) in the residents. Different demographic outcomes resulting from environment, predation, movements and ecological factors including resource competition have conservation implications for the two sub‐populations.     

Facultative adjustment of the offspring sex ratio and male attractiveness: a systematic review and meta‐analysis

Females can benefit from mate choice for male traits (e.g. sexual ornaments or body condition) that reliably signal the effect that mating will have on mean offspring fitness. These male‐derived benefits can be due to material and/or genetic effects. The latter include an increase in the attractiveness, hence likely mating success, of sons. Females can potentially enhance any sex‐biased benefits of mating with certain males by adjusting the offspring sex ratio depending on their mate's phenotype. One hypothesis is that females should produce mainly sons when mating with more attractive or higher quality males. Here we perform a meta‐analysis of the empirical literature that has accumulated to test this hypothesis. The mean effect size was small (r = 0.064–0.095; i.e. explaining <1% of variation in offspring sex ratios) but statistically significant in the predicted direction. It was, however, not robust to correction for an apparent publication bias towards significantly positive results. We also examined the strength of the relationship using different indices of male attractiveness/quality that have been invoked by researchers (ornaments, behavioural displays, female preference scores, body condition, male age, body size, and whether a male is a within‐pair or extra‐pair mate). Only ornamentation and body size significantly predicted the proportion of sons produced. We obtained similar results regardless of whether we ran a standard random‐effects meta‐analysis, or a multi‐level, Bayesian model that included a correction for phylogenetic non‐independence. A moderate proportion of the variance in effect sizes (51.6–56.2%) was due to variation that was not attributable to sampling error (i.e. sample size). Much of this non‐sampling error variance was not attributable to phylogenetic effects or high repeatability of effect sizes among species. It was approximately equally attributable to differences (occurring for unknown reasons) in effect sizes among and within studies (25.3, 22.9% of the total variance). There were no significant effects of year of publication or two aspects of study design (experimental/observational or field/laboratory) on reported effect sizes. We discuss various practical reasons and theoretical arguments as to why small effect sizes should be expected, and why there might be relatively high variation among studies. Currently, there are no species where replicated, experimental studies show that mothers adjust the offspring sex ratio in response to a generally preferred male phenotype. Ultimately, we need more experimental studies that test directly whether females produce more sons when mated to relatively more attractive males, and that provide the requisite evidence that their sons have higher mean fitness than their daughters.     

Evolutionarily stable oviposition and sex ratio in parasitoid wasps with single‐sex broods

Abstract 1. The flexibility of hymenopteran sex ratios is well documented, particularly in structured populations featuring sib mating. 2. Using game theoretic models, the present study examines species producing single‐sex broods in which sib mating is unlikely, and focuses on the role of population density in determining evolutionarily stable oviposition strategies. 3. Since only mated females can produce offspring of both sexes while unmated females produce only male offspring, mated females are under selection to produce more females overall to balance the primary sex ratio. 4. As the proportion of all females that are mated should increase with density, offspring sex ratio of mated females is strongly linked to density at low to moderate densities. The present study shows that when density becomes low enough for fewer than half of all females to have mated, then female offspring generate higher fitness. 5. In this low density situation, females may gain a fitness benefit from waiting at their emergence site or from using other costly means to find and mate with males before ovipositing. 6. The predicted correspondence between females waiting at the emergence site and fewer than half of females in the population containing sperm, can be tested empirically, as can the somewhat counter‐intuitive prediction that greater access to males should yield a more male‐biased sex ratio in the offspring of mated females. 7. The present study also indicates how measuring the variance in giving up times by females waiting for males at low density, can provide insight into mechanisms determining waiting times.     

Combined influence of maternal and paternal quality on sex allocation in red-capped robins

Sex allocation theory predicts females will adaptively manipulate sex ratios to maximize their progeny's reproductive value. Recently, the generality of biased sex allocation in birds has been questioned by meta-analytic reviews, which demonstrate that many previously reported significant results may simply reflect sampling error. Here, we utilize a robust sample size and powerful statistical approach to determine whether parental quality is correlated with biased sex allocation in red-capped robins. Indices of maternal quality (including interactive effects of age and condition) were strongly related to sex allocation. These relationships were in the predicted directions, with larger effect sizes than those of previous studies in this field. There were also paternal correlates, involving age and the source of paternity. We propose that biased sex allocation occurs in this species, and is maintained by differing production costs of each sex and genetic benefits to females of producing sons when fertilized by high-quality males.     

Sex choice in plants: facultative adjustment of the sex ratio in the perennial herb Begonia gracilis

Sex allocation theory predicts that reproducing individuals will increase their fitness by facultatively adjusting their relative investment towards the rarer sex in response to population shifts in operational sex ratio (OSR). The evolution of facultative manipulation of sex ratio depends on the ability of the parents to track the conditions favouring skewed sex allocation and on the mechanism controlling sex allocation. In animals, which have well-developed sensorial mechanisms, facultative adjustment of sex ratios has been demonstrated on many occasions. In this paper, we show that plants have mechanisms that allow them to evaluate the population OSR. We simulated three different conditions of population OSR by manipulating the amount of pollen received by the female flowers of a monoecious herb, and examined the effect of this treatment on the allocation to male vs. female flowers. A shortage of pollen on the stigmas resulted in a more male-skewed sex allocation, whereas plants that experienced a relatively pollen rich environment tended to produce a more female-skewed sex allocation pattern. Our results for Begonia gracilis demonstrate that the individuals of this species are able to respond to the levels of pollination intensity experienced by their female flowers and adjust their patterns of sex allocation in accordance to the expectations of sex allocation theory.     

Frequency‐dependent selection acting on the widely fluctuating sex ratio of the aphid Prociphilus oriens

Frequency‐dependent selection is a fundamental principle of adaptive sex ratio evolution in all sex ratio theories but has rarely been detected in the wild. Through long‐term censuses, we confirmed large fluctuations in the population sex ratio of the aphid Prociphilus oriens and detected frequency‐dependent selection acting on these fluctuations. Fluctuations in the population sex ratio were partly attributable to climatic factors during the growing season. Climatic factors likely affected the growth conditions of host plants, which in turn led to yearly fluctuations in maternal conditions and sex ratios. In the process of frequency‐dependent selection, female proportion higher or lower than ca. 60% was associated with a reduction or increase in female proportion, respectively, the next year. The rearing of aphid clones in the laboratory indicated that mothers of each clone produced an increasing number of females as maternal size increased. However, the mean male number was not related to maternal size, but varied largely among clones. Given genetic variance in the ability to produce males among clones, selection should favour clones that can produce more numerous males in years with a high female proportion. Population‐level sex allocation to females was on average 71%–73% for three localities and more female‐biased when maternal conditions were better. This tendency was accounted for by the hypothesis of competition among foundresses rather than the hypothesis of local mate competition. We conclude that despite consistent operation of frequency‐dependent selection, the sex ratio continues to fluctuate because environmental conditions always push it away from equilibrium.     

Spiderling sex ratio and maternal investment in the bolas spider Mastophora cornigera (Araneae,Araneidae)

Male Mastophora cornigera exit egg sacs as adults, which allowed us to determine spiderling sex ratios and patterns of maternal investment in this species. We collected 15 egg sacs produced by seven mothers, which yielded 1945 emergent spiderlings which were sexed, 1850 of which were weighed. Two emergent broods were significantly male and female biased and were unaffected by pre-emergence mortality. The weights of male and female spiderlings differed in eight broods, with males and females being heavier in four cases each. Five of these broods were derived from multiple egg sac sets produced by one mother, and in each case, the total mean male and female spiderling weights for all broods in a set were biased in the same direction as the biased brood(s) within that set. Mean emergent spiderling weight was independent of brood size and sex ratio for both males and females. Despite such independence, sex allocation in M. cornigera can favor sons, daughters, or both equally, and by numbers, by weight, or both at once. The proximate mechanisms and adaptive significance of such variability is unknown. We also review evidence for gender-biased allocations in arachnid offspring and suggested mechanisms for their applicability to M. cornigera.     

Do females adjust the sex of their offspring in relation to the breeding sex ratio?

When the adult sex ratio differs between years in local populations, but still is predictable between adjacent years, it has been proposed that the best strategy would be to bias the offspring sex ratio in favour of the rare sex. We tested this hypothesis using a data set of great reed warbler offspring, sexed by molecular techniques, that were collected over 11 breeding seasons at two adjacent reed marshes. Three important assumptions for this hypothesis are fulfilled in the studied great reed warbler population. First, a substantial proportion of great reed warblers are living in small local populations where sex ratio distortions would be sufficiently large and common. Second, breeding adults and their offspring return to breed in the local population to a high degree. Third, females have a possibility to assess the breeding sex ratio before laying their eggs. At our study site, the breeding sex ratio was positively correlated between successive years. However, contrary to our prediction, female great reed warblers seemed not to adjust their offspring sex ratio in relation to the local breeding sex ratio.     

A demographic model for sex ratio evolution and the effects of sex‐biased offspring costs

The evolution of the primary sex ratio, the proportion of male births in an individual's offspring production strategy, is a frequency‐dependent process that selects against the more common sex. Because reproduction is shaped by the entire life cycle, sex ratio theory would benefit from explicitly two‐sex models that include some form of life cycle structure. We present a demographic approach to sex ratio evolution that combines adaptive dynamics with nonlinear matrix population models. We also determine the evolutionary and convergence stability of singular strategies using matrix calculus. These methods allow the incorporation of any population structure, including multiple sexes and stages, into evolutionary projections. Using this framework, we compare how four different interpretations of sex‐biased offspring costs affect sex ratio evolution. We find that demographic differences affect evolutionary outcomes and that, contrary to prior belief, sex‐biased mortality after parental investment can bias the primary sex ratio (but not the corresponding reproductive value ratio). These results differ qualitatively from the widely held conclusions of previous models that neglect demographic structure.     

Effective size of density‐dependent two‐sex populations: the effect of mating systems

Density dependence in vital rates is a key feature affecting temporal fluctuations of natural populations. This has important implications for the rate of random genetic drift. Mating systems also greatly affect effective population sizes, but knowledge of how mating system and density regulation interact to affect random genetic drift is poor. Using theoretical models and simulations, we compare N_e in short‐lived, density‐dependent animal populations with different mating systems. We study the impact of a fluctuating, density‐dependent sex ratio and consider both a stable and a fluctuating environment. We find a negative relationship between annual N_e/N and adult population size N due to density dependence, suggesting that loss of genetic variation is reduced at small densities. The magnitude of this decrease was affected by mating system and life history. A male‐biased, density‐dependent sex ratio reduces the rate of genetic drift compared to an equal, density‐independent sex ratio, but a stochastic change towards male bias reduces the N_e/N ratio. Environmental stochasticity amplifies temporal fluctuations in population size and is thus vital to consider in estimation of effective population sizes over longer time periods. Our results on the reduced loss of genetic variation at small densities, particularly in polygamous populations, indicate that density regulation may facilitate adaptive evolution at small population sizes.