Sex ratio adjustment and maternal condition in two aphid species

We analyzed how offspring sex ratio varies with maternal condition in order to obtain evidence on the population structure in two aphid species with different life cycles. When fitness returns per unit investment differ for the production of daughters and sons, selection will favor an increasing investment into the sex with the higher returns. Therefore, the offspring sex ratios of individual mothers should become more biased towards the sex with the higher fitness returns as their condition or fecundity improves. The pattern of sex ratio adjustment we found in Uroleucon cirsii indicates local mate competition among males, while the pattern we found in Rhopalosiphum padi suggests local resource competition among sexual females. This might be the first evidence for local resource competition among females in an invertebrate species. Local mate competition means that fitness returns are limited by the availability of females as mates within local breeding groups, whereas local resource competition means that fitness returns are limited by the availability of resources for females competing within local groups. We discuss how the life cycles of both species fit to these hypotheses.

Sex ratio manipulation in response to maternal condition in pigeons: evidence for pre-ovulatory follicle selection

A number of recent reports have documented offspring sex ratio biases in birds. However, to date the potential mechanisms that have been put forward to explain the proximate basis for these deviations are entirely speculative. Using a captive population of domestic pigeons (Columba livia domestica), I tested the hypothesis that mothers in relatively poor physical condition should overproduce daughters by manipulating maternal body condition around the time of egg laying by continuous egg removal and differing feeding regimes. During treatment, females were fed a controlled quantity of food. This, combined with the high energetic costs of repeated egg production caused a significant reduction in maternal body weight. In contrast, during control when food was available ad libitum, maternal body weight did not decline, despite repeated egg production. No significant deviation from parity was evident in the sex ratio of either the first or second eggs during control, whereas during treatment a significant female bias was evident in not only the first egg, but also in the second egg. The absence of single-egg clutches, the rarity of infertile eggs and the lack of laying delays between eggs strongly suggests that the mechanism of sex ratio adjustment in pigeons occurs prior to ovulation. The highly skewed sex-distribution within the two-egg clutches and the unexpectedly large amount of variation in the yolk weight of eggs produced during treatment (but not control) are consistent with the expectations of pre-ovulatory selective resorption of wrong sex ovarian follicles.     

Sex ratio and sex change in wild and laboratory populations ofTyposyllis prolifera (Polychaeta)

Sex determination and sex differentiation in three local Istrian (Yugoslavia) populations of the polychaeteTyposyllis prolifera were studied both in the field and the laboratory. Significant differences in sex habits were revealed among the populations, the biological significance of which is unknown. (1) Sex ratios (% ) in natural populations from the Adriatic Sea amounted to 50% (Rovinj), 62% (Pore) and 77% (Pula). In the Pula-(but not in the Rovinj-)population, a correlation was found between population density on individualHalopteris scoparia thalli (the favorite habitat ofT. prolifera) and the respective sex ratio: The mean male protion was only a little more than 50% in densely populated thalli, and increased to more than 80% in sparsely populated thalli. Laboratory studies provided the information necessary to explain these field findings. (2) Laboratoryraised progenies showed an overall 1:1 primary (first sexual phase) sex ratio, independent of the local origin of the material and of whether worms were raised singly or under conditions of social contact. Nevertheless, the studied populations may differ with respect to the genetic mechanisms of sex determination: In the Pore- and Pulapopulation individual progenies often departed significantly from the 1:1 sex ratio, whereas individual progenies in the Rovinj- population never did so. (3) The populations proved to be partially protogynous. Sex differentiation in that half of the individuals which differentiated into males (primary males) was absolutely stable during sequential sexual phases. Worms which differentiated into females, however, often changed sex at an earlier or later stage of their life cycle (secondary males). Sex change was irreversible. As to the degree of lability of female differentiation under conditions of isolation, the findings suggest a genetic divergence among both populations and individuals of the same population. Female differentiation in the Rovinj-population was virtually stable, but Pula-females underwent rapid and complete masculinization. Pore-females were between these extremes. (4) In addition to genetic factors, exogenous conditions affected the incidence and time of sex change (Pula-population): Under conditions of social contact, sex change was delayed or suppressed as compared with isolated individuals. The degree of delay or inhibition was independent of the sex of the social partners, yet increased (to the point of saturation) with population density.     

Fissioning minimizes ranging costs in spider monkeys: a multiple-level approach

The adjustment to deal with intragroup food competition is probably the most plausible explanation of high levels of fission–fusion dynamics. However, studies did not always support expected relations between food availability, ranging costs, and subgroup size. We used several levels of analysis differing in the time and spatial scale in order to investigate this explanation in spider monkeys. In our study, subgroups were larger when food availability was higher across most levels of analyses used. We also found a fine-scale adjustment: compared to the food patch previously visited, spider monkeys traveled to larger patches just after fusions. This was not without an immediate travel cost: the interpatch distance and travel time after a fusion were longer than that before the fusion. This rapid adjustment shows the flexibility that fission–fusion dynamics can offer. Spider monkeys are in large subgroups only when food conditions are favorable, as evidenced by the fact that at all the other time-scale levels larger subgroups did not experience greater ranging costs than smaller subgroups. Our results indicate that on the whole spider monkeys successfully minimize ranging costs by fission and fusion of subgroups.     

Time as a constraint on group size in spider monkeys

An animal can only survive in a given habitat if it has enough time to find, process and digest food whilst avoiding predation. The time it has for food acquisition is affected by the vegetation and competition with conspecifics, which depends on aggregation tendencies. We used the relationships between time allocations, on the one hand, and climatic variables (as a proxy for habitat quality) and group size, on the other, to develop a model that predicts maximum ecologically tolerable group size at different locations for spider monkeys. Spider monkeys are particularly interesting because the social communities often split up into small units. Temperature variation and rainfall variation were the main determinants of time budgets. Community size and average annual rainfall determined party size. The model correctly predicted presence or absence of spider monkeys at 78–83% of 217 New World forest sites. Within the geographical range of the species, this time budget model predicted the presence of spider monkeys better than a model based directly on climate variables. Predicted community and party sizes were significantly larger at sites where spider monkeys are present than at sites where they are absent. As required by the model, predicted maximum community sizes were significantly larger than observed community sizes. Moving time showed a U-shaped relationship with party size, which suggests that moving time is the factor that keeps spider monkey communities from travelling together in a tight group.     

Growth rates in a wild primate population: ecological influences and maternal effects

Growth rate is a life-history trait often linked to various fitness components, including survival, age of first reproduction, and fecundity. Here we present an analysis of growth-rate variability in a wild population of savannah baboons (Papio cynocephalus). We found that relative juvenile size was a stable individual trait during the juvenile period: individuals generally remained consistently large-for-age or small-for-age throughout development. Resource availability, which varied greatly in the study population (between completely wild-foraging and partially food-enhanced social groups), had major effects on growth. Sexual maturity was accelerated for animals in the food-enhanced foraging condition, and the extent and ontogeny of sexual dimorphism differed with resource availability. Maternal characteristics also had significant effects on growth. Under both foraging conditions, females of high dominance rank and multiparous females had relatively large-for-age juveniles. Large relative juvenile size predicted earlier age of sexual maturation for both males and females in the wild-feeding condition. This confirmed that maternal effects were pervasive and contributed to differences among individuals in fitness components.Communicated by J. Setchell     

Maternal dominance rank and lifetime survivorship of male and female rhesus monkeys

Summary The longitudinal survivorship of a group of free-ranging male and female rhesus monkeys from La Parguera, Puerto Rico, was analyzed. Males had lower age-specific survivorship than females. There were no differences in the survivorship of daughters of high- and low-ranking mothers and there was no correlation between total number of offspring born and maternal rank for females. However, the sons of low-ranking mothers had lower survivorship than the sons of high-ranking females. This sex-related difference in survivorship, in conjunction with other evidence, indicates that the average lifetime reproduction of sons of low-ranking females is lower than that of daughters and vice versa for offspring of high-ranking females.     

Association patterns of spider monkeys: the influence of ecology and sex on social organization

Summary In this paper I consider how the costs and benefits of group living in spider monkeys (Ateles geoffroyi) vary between troop members. The results suggest that ecological factors set an upper limit to the number of spider monkeys that can associate and still efficiently exploit the available resources. In addition, the needs of the individual appears to influence the type and size of the subgroup it chooses. Adult males band together, travel over a large area, and are frequently sighted near the community's boundary. In contrast, adult females spend more time solitary than males and have association patterns that are strongly influenced by the presence of a dependent infant. Females with dependent infants tend to travel in small subgroups or alone, avoid the boundaries of the community's home range, and exhibit a restricted pattern of use of their range. The results suggest that males may be attempting to locate females with which they can breed, while mothers attempt to protect their infants by avoiding conspecifics and potentially dangerous situations near territorial boundaries.     

Sex ratio and host size in a parasitoid wasp

Summary Parasitoid wasps often lay male eggs in small hosts and female eggs in larger hosts. The selective advantage of this strategy can be explained by assuming wasp fitness increases with host size and that this fitness increase is greater in females than in males. I conducted experiments to test a model based on this explanation and found the results generally supported the model with one exception; unlike what the model assumed, these wasps were unable to adjust their offspring sex ratios in each generation to different host size distributions. This finding suggests an alternate view as to how selection might operate in the evolution of parasitoid sex ratios.     

Sex differences in maternal investment by Macaca mulatta

Summary The possibility that male offspring are more costly to produce than female offspring was investigated in captive Macaca mulatta. Differential maternal investment into 187 infants was evaluated by comparing birth weight, infant growth rate, month of birth, and interbirth interval of males and females. There were no statistically significant differences between male and female infants for any of these variables.     

Mating patterns of woolly spider monkeys,Brachyteles arachnoides: implications for female choice

Summary Woolly spider monkeys show a promiscuous, polygynous mating system in which a receptive female mates with several males, often in rapid succession. Copulation is prolonged with an average duration of 4.1±1.5 (SD) min. Coitus consists of a stationary phase with the male in intromission, followed by stercotypic behaviours of the female which appear to cue and/or accompany male climax and ejaculation. Subadult and adult males show different association patterns with individual females. Subadult males form long-term consortships with particular females while adult males appear strongly attracted to a particular female only when the is receptive. These different behavior patterns of males are viewed as age-specific mating tactics. Males in a mating aggregation show little intermale aggression for sexual access to a receptive female. Large testis size in this species suggests that much intermale competition for reproductive success may be carried out at a postcopulatory level, perhaps by sperm competition. The copulatory pattern of woolly spider monkeys may function primarily as a mechanism of female choice, aiding a female in assessing the quality of males in hei mating aggregation while helping to ensure that maximal high quality spermatozoa will be available at the proper time for fertilization.     

Optimal investment in sons and daughters when parents do not know the sex of their offspring

Optimal parental investment usually differs depending on the sex of the offspring. However, parents in most organisms cannot discriminate the sex of their young until those young are energetically independent. In a species with physical male–male competition, males are often larger and usually develop sexual ornaments, so male offspring are often more costly to produce. However, Onthophagus dung beetles (Coleoptera; Scarabaeidae) are highly dimorphic in secondary sexual characters, but sexually monomorphic in body size, despite strong male–male competition for mates. We demonstrate that because parents provide all resources required by their offspring before adulthood, O. atripennis exhibits no sexual size dimorphism irrespective of sexual selection pressure favoring sexual dimorphism. By constructing a graphic model with three fitness curves (for sons, daughters, and expected fitness return for parents), we demonstrate that natural selection favors parents that provide both sons and daughters with the optimal amount of investment for sons, which is far greater than that for daughters. This is because the cost of producing small sons, that are unable to compete for mates, is far greater than the cost of producing daughters that are larger than necessary. This theoretical prediction can explain sexual dimorphism without sexual size dimorphism, widely observed in species with crucial parental care such as dung beetles and leaf-rolling beetles, and may provide an insight into the enigmatic relationship between sexual size dimorphism and sexual dimorphism.     

Maternal nutrition affects offspring performance via maternal care in a subsocial spider

Provisioning of nutrients to the young during parental care is one of the mechanisms by which parents can affect growth and survival of their young and thus their reproductive success. We examined the hypothesis that food quality, i.e., ratio of macronutrients, provided to the young via maternal care affects their performance and the female’s reproductive success. The subsocial spider Stegodyphus lineatus exhibits intensive maternal care behaviors, including feeding the young and matriphagy (consumption of the mother). Our results showed that a protein-enriched diet resulted in larger females at maturation and higher survival of young, relative to intermediate or lipid-enriched diets. However, fecundity was not affected by female diet. We suggest that most of the nutrients are provided to the young during maternal care rather than deposited in the eggs, allowing females to economize on limited nutritional reserves. Females before maternal care showed a low protein and high lipid content relative to females before maturation and oviposition, suggesting a change in the nutritional requirement of females before maternal care. This change in macronutrient composition may be adaptive for the success of the young in the wild and shows a novel approach to animals’ ability to increase their reproductive success. Field-collected females showed a similar macronutrient composition as that of protein-enriched females in the lab, suggesting a high reproductive success of females in the wild. To our knowledge, this is the first time the importance of different macronutrients to females’ reproductive success is examined during reproduction.     

The influence of maternal rank and infant sex on maternal investment trends in rhesus macaques: birth sex ratios,inter-birth intervals and suckling patterns

Summary In the new colony of rhesus macaques at Madingley, no overall difference was found in the length of the inter-birth intervals following the birth of male and female infants. The lack of overall differences in the reproductive costs of raising sons and daughters, was associated with an absence of differences in suckling patterns between male and female infants. It is argued that similar pre-weaning investment in sons and daughters may be related to the presence of similar growth rates for male and female infants during the first year of life. Most high ranking mothers reproduced in consecutive years, while low ranking mothers were more likely to experience two year long inter-birth intervals. Further analyses revealed that this difference was mainly due to the fact that low ranking mothers always failed to reproduce the year after raising a daughter. Thus, no difference was found in the length of inter-birth intervals between high ranking mothers with infants of either sex and low ranking mothers with sons. The daughters of low ranking females suckled more frequently and making more nipple contacts per bout, and such high nipple stimulation was responsible for the reproductive inhibition experienced by their mothers. It is suggested that the high degrees of nipple stimulation may have been a consequence of the high levels of aggression that low ranking females with daughters have been shown to receive, since their mothers could have allowed frequent ventro-ventral contact in order to protect them. Given that low ranking mothers find daughters reproductively costly to raise, it is possible that such high reproductive costs have played a significant role in the evolution of sex ratio biases at birth. As in other primate populations, in this colony low ranking females produced a greater proportion of sons than daughters, and high ranking mothers showed the opposite trend.     

Mind the gap: the ratio of yolk androgens and antioxidants varies between sons and daughters dependent on paternal attractiveness

Females are expected to partition resources between offspring in a context-dependent way to maximise total fitness returns from a reproductive attempt. Female zebra finches (Taeniopygia guttata) vary the allocation of yolk androgens and antioxidants among offspring. Importantly, the balance between androgens and antioxidants in yolks may be more important than their independent absolute amounts in terms of fitness consequences for developing young. Therefore, we tested whether the relative allocation of these two resources in yolks varies according to either the Trivers–Willard, positive or compensatory maternal investment hypothesis. We manipulated male attractiveness using coloured leg bands (red-banded males appear attractive; green-banded males, unattractive) and measured yolk androgens and antioxidants in each egg, egg sex, clutch sex ratio and female condition. While female zebra finches manipulated the balance of androgens and antioxidants within and between clutches in response to mate attractiveness, offspring sex and their own condition, they did not do so in a way that consistently followed any of the hypotheses. Mothers paired with unattractive males allocated a larger antioxidant/androgen ratio to daughters than sons. This pattern was reversed when paired to an attractive male; sons received a larger antioxidant/androgen ratio than daughters. We also found offspring sex ratio decreased with increasing female condition for unattractive males, but not for attractive males. However, without knowing the fitness consequences of the balance of different egg constituents, it is difficult to interpret the patterns consistently in terms of the Trivers–Willard, compensatory and positive investment hypotheses.     

Sex ratio responses to other parasitoid wasps: multiple adaptive explanations

In an effort to distinguish among adaptive models and to improve our understanding of behavioral mechanisms of sex ratio manipulation, this study examines sex ratio responses to other wasps in the solitary parasitoid wasp Spalangia cameroni. Relative to when alone, females produced a greater proportion of sons in the presence of conspecifics, regardless of whether the conspecifics were female or male. In addition, females produced a greater proportion of sons after a day with a conspecific male, and after a day with a conspecific female, but only if the females had been ovipositing. Relative to when alone, females did not produce a greater proportion of sons in the presence of females of the confamilial Muscidifurax raptor or in response to hosts that had already been parasitized by a conspecific. A combination of evolutionary models may explain S. cameroni’s sex ratios. An increased proportion of sons in response to conspecific females is common among parasitoid wasps and is usually explained by local mate competition (LMC) theory. However, such a response is also consistent with the perturbation model, although not with the constrained females model. The response to conspecific males is not consistent with LMC theory or the perturbation model but is consistent with the constrained females model.     

Dominance rank,female reproductive synchrony,and male reproductive skew in wild Assamese macaques

In groups with multiple males, direct mate competition may select for the evolution of dominance hierarchies that sort males into a queue for access to fertile females. The priority-of-access (PoA) model proposed by Altmann in 1962 makes explicit predictions about the resulting paternity distribution based on an interaction between male dominance rank and the overlap of female receptive phases. Here, we investigated whether the logic of the PoA model predicted the distribution of paternity across ranks in a seasonal breeder with high reproductive synchrony over six consecutive mating seasons. We studied 18 males that resided in a group of wild Assamese macaques (Macaca assamensis) in their natural habitat at Phu Khieo Wildlife Sanctuary, Thailand, between 2006 and 2011 with 5 to 13 conceptions per season. We assessed whether mate guarding increased paternity success, described “short-term” deviations from predicted paternity distribution, and examined how these are related to the number of competitors and fertile females. We determined genetic paternity of 43 (93 %) offspring born into the study group and found reproductive skew to be relatively low with 29 % alpha male paternity in accordance with the high degree of female reproductive synchrony observed. Short-term deviations from expected paternity distribution over ranks were not explained by the number of resident males or the number of conceiving females or their interaction. Within the limits of this study, these results suggest that even if males cannot discern female fertile phases, if reproduction is seasonal, and if reproductive synchrony is high, males may also compete directly over access to females.     

Sex ratio, sexual dimorphism and mating structure in bethylid wasps

Sexual dimorphism has been linked to parasitoid mating structure by several authors. In turn mating structure has an important influence on predicted sex ratio optima. Here we test the relationship between sexual dimorphism and sex ratio using data from 19 species of bethylid wasps. Using phylogenetically based comparative methods we confirm the findings of a previous cross-species analysis that sex ratio (proportion of males) is strongly and negatively correlated with clutch size. Using cross-species comparisons we show an additional positive correlation of sex ratio and relative male size, as predicted. The relationship however is not significant when using phylogenetically based methods. The cross-species result is largely due to differences between two bethylid sub-families: the Epyrinae have relatively large males and relatively high sex ratios, whereas the Bethylinae have relatively small males and lower sex ratios. Our study illustrates the benefits and drawbacks of using cross-species versus phylogenetically based comparisons. Received: 13 May 1997 / Accepted after revision: 12 January 1998