Sex differences in parental care: Gametic investment,sexual selection,and social environment

Male and female parents often provide different type and amount of care to their offspring. Three major drivers have been proposed to explain parental sex roles: (1) differential gametic investment by males and females that precipitates into sex difference in care, (2) different intensity of sexual selection acting on males and females, and (3) biased social environment that facilitates the more common sex to provide more care. Here, we provide the most comprehensive assessment of these hypotheses using detailed parental care data from 792 bird species covering 126 families. We found no evidence for the gametic investment hypothesis: neither gamete sizes nor gamete production by males relative to females was related to sex difference in parental care. However, sexual selection correlated with parental sex roles, because the male share in care relative to female decreased with both extra‐pair paternity and frequency of male polygamy. Parental sex roles were also related to social environment, because male parental care increased with male‐biased adult sex ratios (ASRs). Taken together, our results are consistent with recent theories suggesting that gametic investment is not tied to parental sex roles, and highlight the importance of both sexual selection and ASR in influencing parental sex roles.     

杂色山雀双亲差异性育雏策略

社会性单配制鸟类的配偶双方在抚育子代时常存在性别差异,不同鸟种的雌雄双亲往往采取不同的育雏策略。以杂色山雀(Sittiparus varius)为研究对象,2017年3—7月对繁殖巢箱进行录像监测,记录杂色山雀育雏期亲代投入情况。分析结果显示:1)双亲递食率在育雏前期(4—6日龄)无显著差异,而育雏后期(10—12日龄)雌性的递食率显著高于雄性。2)雌性亲鸟后期递食率较育雏前期显著增加;而雄性亲鸟育雏前期和后期递食率无显著差异。3)雌性递食率与自身喙宽呈极显著正相关,雄性递食率与双亲体征参数均无相关关系。总的来说,在育雏阶段,杂色山雀雌性亲鸟的递食率随着雏鸟的需求和自身身体质量发生调整,雌性在育雏后期递食率显著升高,而雄性亲鸟递食率无变化,这可能与育雏期双亲投入分工不同有关。     

Sex allocation and sex‐specific parental investment in an endangered seabird

Biased offspring sex ratio is relatively rare in birds and sex allocation can vary with environmental conditions, with the larger and more costly sex, which can be either the male or female depending on species, favoured during high food availability. Sex‐specific parental investment may lead to biased mortality and, coupled with unequal production of one sex, may result in biased adult sex ratio, with potential grave consequences on population stability. The African Penguin Spheniscus demersus, endemic to southern Africa, is an endangered monogamous seabird with bi‐parental care. Female adult African Penguins are smaller, have a higher foraging effort when breeding and higher mortality compared with adult males. In 2015, a year in which environmental conditions were favourable for breeding, African Penguin chick production on Bird Island, Algoa Bay, South Africa, was skewed towards males (1.5 males to 1 female). Males also had higher growth rates and fledging mass than females, with potentially higher post‐fledging survival. Female, but not male, parents had higher foraging effort and lower body condition with increasing number of male chicks in their brood, thereby revealing flexibility in their parental strategy, but also the costs of their investment in their current brood. The combination of male‐biased chick production and higher female mortality, possibly at the juvenile stage as a result of lower parental investment in female chicks, and/or at the adult stage as a result of higher parental investment, may contribute to a biased adult sex ratio (ASR) in this species. While further research during years of contrasting food availability is needed to confirm this trend, populations with male‐skewed ASRs have higher extinction risks and conservation strategies aiming to benefit female African Penguin might need to be developed.     

Some evolutionary properties of parental investment per offspring in a heterogeneous environment

The possibility of protected polymorphisms and of monomorphic evolutionarily stable strategies for parental investment per offspring in a heterogeneous environment is theoretically analysed. A high density two-niche model of the classical soft selection kind is used, although it incorporates the possibility of rare strategies invading an empty niche the contribution of which is not constant. Protected polymorphisms can be found whether or not both strategies included produce surviving offspring in both niches. However, a monomorphic evolutionarily stable strategy exists unless offspring of the optimal size in one of the niches cannot survive in the other. The robustness of the model is graphically illustrated under a variety of circumstances, and some evolutionary consequences are briefly discussed.     

Analyzing the function of a hox gene: an evolutionary approach

We present an evolutionary approach to dissecting conserved developmental mechanisms. We reason that important mechanisms for making the bodyplan will act early, to generate the major features of the body and that they will be conserved in evolution across many metazoa, and thus, that they will be available in very different animals. This led to our specific approach of microarrays to screen for very early conserved developmental regulators in parallel in an insect, Drosophila and a vertebrate, Xenopus. We screened for the earliest conserved targets of the ectopically expressed hox gene Hoxc6/Antennapedia in both species and followed these targets up, using in situ hybridization, in the Xenopus system. The results indicate that relatively few of the early Hox target genes are conserved: these are mainly involved in the specification of the antero-posterior body axis and in gastrulation.     

The evolution of parental investment in caecilian amphibians: a comparative approach

Parental care is widespread among vertebrates and the observed patterns of parental care and investment are extremely diverse. Among amphibians, caecilians (Gymnophiona) exhibit considerable variation in reproductive modes, including both oviparity and viviparity, combined with highly unusual investment strategies (e.g. skin‐feeding and intrauterine feeding). In the present study, current knowledge on the reproductive modes is integrated into an analysis of the evolutionary scenario of parental investment of caecilians. Phylogenetically basal caecilians possessing a biphasic life cycle that includes an aquatic larval stage invest in macrolecithal eggs directly corresponding to size at hatching. Some phylogenetically derived caecilians (i.e. the Teresomata) have a smaller clutch size and show a reduction to either medium‐yolked (mesolecithal) or small‐yolked (microlecithal) eggs. Via alternative pathways of parental investment, such as intrauterine feeding in viviparous taxa and maternal dermatotrophy in oviparous taxa, teresomatan caecilians increase both offspring size and quality. However, more data regarding reproductive biology are needed to obtain a fully resolved understanding of the evolution of reproduction in caecilian amphibians.     

The parental investment conflict in continuous time: St. Peter's fish as an example

The parental investment conflict considers the question of how much each sex should invest in each brood, thereby characterizing different animal species. Each species usually adopts a certain parental care pattern: female-care only, male-care only, biparental care, or even no parental care at all. The differences in care patterns are usually explained by the different costs and benefits arising from caring for the offspring in each animal species. This paper proposes a game-theoretical model to the parental investment conflict based on the parental behavior of St. Peter's fish. St. Peter's fish exhibit different parental care patterns, allowing the examination of the factors which determine the particular behavior in each mating. We present a continuous time, two-stage, asymmetric game, with two types of players: male and female. According to the model's results, three parental care patterns: male-only care, female-only care and biparental care, are possible evolutionarily stable strategies. The evolutionarily stable parental care pattern in a certain mating depends on a parent's increase in mortality due to parental care, and on its advantage from biparental care. These results may explain the different parental care patterns observed in a variety of animal species, including those found in the St. Peter's fish.     

Cues of parental investment as a factor in attractiveness

One prediction derived from parental investment theory is that women will be more attentive than men are to cues of a prospective mate's dispositions to invest in children. Research with 1793 Internet participants, representing a diverse population sample, found that (a) women tend to be generally more critical than men are in their evaluations of potential mates, but not potential friends or neighbors, and (b) cues of a positive disposition towards parental investment (DPI) have a positive influence on female evaluations of the attractiveness of males. This latter effect, however, is less domain-specific than previous research [La Cerra, M. M. (1995). Evolved mate preferences in women: Psychological adaptations for assessing a man's willingness to invest in offspring (doctoral dissertation, University of California, Santa Barbara). Dissertation Abstracts International: Section B: the Sciences & Engineering Mar, 55(9-B), 4149] indicated; it is not limited to mating contexts and to cues focusing on parental investment. In fact, much of the sex difference appears to be due to indifference by males towards cues of female DPI. A second study further clarified that the previous findings were not due solely to the Internet methodology or the immediate accessibility of images being evaluated.     

Sex differences in adrenocortical structure and function. XI

Summary Adrenal glands from orchectomized and ovariectomized rats, with and without replacement therapy, and also from intact controls of both sexes, were examined by autoradiography with ³H-thymidine. The labelling index after 1 or 2 nucleoside injections was higher in the zona glomerulosa of females than in male rats, while no differences were found in the fascicular and reticular zones. Orchiectomy increased the labelling index in the fascicular and reticular zones, an effect prevented by testosterone. Ovariectomy did not change the labelling index, while estradiol lowered it in the zona glomerulosa. Duration of the S phase was longer in the zona fasciculata cells of males than in females. Both orchiectomy and testosterone shortened this phase in cells of the zona fasciculata and zona reticularis. Ovariectomy prolonged the S phase in the zona fasciculata and shortened this time in the reticular zone, an effect reversed by estradiol.In the glomerular and fascicular zones, cell cycle time was longer in males than in females. Orchiectomy shortened this time in all adrenocortical zones, an effect reversed by testosterone. Ovariectomy shortened cell cycle time in the glomerular and reticular zones and prolonged it in the zona fasciculata; these effects were reversed by estradiol. Turnover rate in adrenocortical cells was markedly higher in females than in males, a difference due to testosterone which markedly decreased turnover rate.     

Sex differences in life history drive evolutionary transitions among maternal,paternal, and bi‐parental care

Evolutionary transitions among maternal, paternal, and bi‐parental care have been common in many animal groups. We use a mathematical model to examine the effect of male and female life‐history characteristics (stage‐specific maturation and mortality) on evolutionary transitions among maternal, paternal, and bi‐parental care. When males and females are relatively similar – that is, when females initially invest relatively little into eggs and both sexes have similar mortality and maturation – transitions among different patterns of care are unlikely to be strongly favored. As males and females become more different, transitions are more likely. If females initially invest heavily into eggs and this reduces their expected future reproductive success, transitions to increased maternal care (paternal → maternal, paternal → bi‐parental, bi‐parental → maternal) are favored. This effect of anisogamy (i.e., the fact that females initially invest more into each individual zygote than males) might help explain the predominance of maternal care in nature and differs from previous work that found no effect of anisogamy on the origin of different sex‐specific patterns of care from an ancestral state of no care. When male mortality is high or male egg maturation rate is low, males have reduced future reproductive potential and transitions to increased paternal care (maternal → paternal, bi‐parental → paternal, maternal → bi‐parental) are favored. Offspring need (i.e., low offspring survival in the absence of care) also plays a role in transitions to paternal care. In general, basic life‐history differences between the sexes can drive evolutionary transitions among different sex‐specific patterns of care. The finding that simple life‐history differences can alone lead to transitions among maternal and paternal care suggests that the effect of inter‐sexual life‐history differences should be considered as a baseline scenario when attempting to understand how other factors (mate availability, sex differences in the costs of competing for mates) influence the evolution of parental care.     

Sex differences in bone loss--an evolutionary perspective on a clinical problem

The dramatic increase in the world's population that has occurred over the past 100 years has come largely through reductions in death due to infectious disease. An epidemiologic transition to a preponderance of deaths due to degenerative conditions such as cardiovascular disease and cancer is occurring in the developing countries as well as in the industrialized ones. In the industrialized countries, demographic profiles now reflect the increased life expectancies of both sexes. However, female life expectancies exceed male by six or more years. Further change in mortality patterns will accompany success in the reduction of the number of mortalities attributable to such degenerative conditions as cardiovascular disease and cancer. In the 21st century, conditions associated with sensescence will be of increasing concern. Adaptive strategies that enhanced reproductive success throughout most of human evolution may now prove detrimental to human health as average life expectancies reach unprecedented length. In this environment, differences in the survival mechanisms deployed by males as opposed to females will become increasingly important.     

Intrafamilial conflict and parental investment: a synthesis

We outline and develop current theory on how inherent genetic conflicts of interest between the various family members can affect the flow of parental investment from parents to offspring, and discuss the problems for empirical testing that this generates. The parental investment pattern realized in nature reflects the simultaneous resolution of all the conflicts between the family players. This depends on the genetic mechanism, the mating system and reproductive constraints, on whether extra demand by progeny affects current or future sibs, and particularly on the behavioural mechanisms underlying demand (begging or solicitation) and supply (provision of parental investment by parents). The direction of deviation from the optimal parental investment for the parent(s) depends on the slope of what we term the 'effect of supply on demand', the mechanism that determines how changes in food supply affect begging levels. If increasing food increases begging (positive slope), less parental investment is supplied than the parental optimum and if increasing food decreases begging (negative slope), more parental investment is supplied. The magnitude of deviation depends on both the 'effect of supply on demand' and on the 'effect of demand on supply' (the mechanism determining how changes in begging affect food supply, which always has a positive slope). We conclude that it will often be impossible to deduce the extent of underlying conflict by establishing the amount of parental investment given relative to the ideal optimum for the parent. Some possible directions for future research are discussed.     

Sex differences in adrenocortical structure and function

Summary Adrenal glands of adult female rats are heavier than the glands of corresponding male rats. Postpubertal orchiectomy increases the adrenal weight, an effect restored by testosterone replacement. Under the same conditions ovariectomy of 8 weeks duration does not change the adrenal weight while estradiol replacement enhances the relative adrenal weight.Karyometric studies have shown that nuclei in the female zona fasciculata cells are larger (app. 18%) than those of the male. Similar but only slight differences (2%) were observed in the zona reticularis. Orchiectomy results in enlargement of cell nuclei within all zones of the adrenal cortex; testosterone replacement has the opposite effect. Ovariectomy of 8 weeks duration slightly enhances the volume of nuclei of the zona glomerulosa cells, has no effect on the nuclei of the zona fasciculata and reduces the volume of nuclei in the zona reticularis. Estradiol replacement reduces the volume of nuclei of the zona glomerulosa cells but increases nuclear volume in the zona fasciculata and in the zona reticularis.Thus testosterone has an inhibitory effect on the adrenal cortex of the rat while the physiologic effect of estradiol on the morphology of this gland, particularly on the zona fasciculata cells is rather dubious.The author wishes to thank Mrs. B. Westerska and Miss K. Siejak for excellent technical assistance.This research was supported in part by a grant from the Zoological Committee, 2nd Department, Polish Academy of Sciences.This paper is dedicated to the memory of late Kazimierz Mietkiewski, M.D., Ph.D. whose encouragements and suggestions were most stimulating for my work.     

Sex differences in adrenocortical structure and function

Summary Adrenal glands of adult male hamsters are larger and secrete more cortisol than those of females. Stereology was therefore used to study zonal and cellular aspects of development of the adrenal cortex of male and female hamsters. Adrenal glands were studied at weekly intervals from day 21 to day 77 of postnatal ontogenesis. Within this period, body weight did not differ significantly between the sexes. During development, absolute and relative adrenal weights were higher in males; their zona glomerulosa (ZG), zona fasciculata (ZF) and zona reticularis (ZR) become markedly larger than those in females. No marked changes in the volume of individual ZG cells occurred although ZF cells and ZR cells become larger in male than female animals. The total number of adrenocortical cells increased within the period studied, a greater increase being observed in ZG and ZF in males. No distinct sex difference was observed in the number of ZR cells throughout development. From day 56 of postnatal life the adrenal cortex of male hamster contained more parenchymal cells than the female gland. These results thus indicate that sex differences in hamster adrenal cortex depend upon changes in number and size of parenchymal cells.Supported in part by a grant from the Committee of Zoology, Polish Academy of Sciences     

Sex differences in adrenocortical structure and function

Summary The zonation and cellular composition of the adrenal cortex of intact mature male and female rats of different strains (Chbb Thomm, CFY) and three strains of Wistar rats (W1, W2 and W3) at the age of 84–90 days were compared using morphometry.Both absolute and relative adrenal gland weights were higher in female than male rats. Rats of W3 and Chbb Thomm strains had the largest adrenals. These differences depended upon the higher volume of the zona fasciculata (ZF) and zona reticularis (ZR) in the W3 and Chbb Thomm strains than in the remaining animals. Females had larger adrenocortical zones than corresponding males. The average volume of the ZF cell ranged in males from 1589 m³ (W1 strain) to 2111 m³ (Chbb Thomm) and in females from 2249 m³ (W1 strain) to 2894 m³ (W3 strain). The average nuclear volume of the ZF cells was higher in female rats whereas there were no strain-and sex-differences in the size of zona glomerulosa (ZG) and ZR cells.The total number of parenchymal cells per pair of adrenals varied markedly among the studied strains, with the highest number in W3 and Chbb Thomm females. W3, Chbb Thomm and CFY females had larger number of parenchymal cells than males; the reverse was true for W1 strain whereas no differences were found among W2 male and female rats.     

Sex differences in adrenocortical structure and function

Summary The cytological aspects of sexual dimorphism in the rat adrenal cortex and its relationship to the gonads have been investigated. The adrenal glands of mature female rats were heavier than those of males, and morphometry showed that this was almost exclusively due to conspicuous differences in the volume of cells of the zona fasciculata (ZF) and zona reticularis (ZR). Stereology demonstrated that the volume of the mitochondrial and lipid droplet compartments, as well as the surface area per cell of mitochondrial cristae and smooth endoplasmic reticulum tubules, were markedly higher in the ZF and ZR cells of female animals. Orchiectomy increased and ovariectomy decreased the adrenal weight, by eliciting hypertrophy and atrophy, respectively, of ZF and ZR cells; these effects of gonadectomy were reversed by the appropriate gonadal hormone replacement. It is suggested that the sexual dimorphism of the rat adrenal cortex may depend upon the inhibitory action of testosterone and the stimulatory effect of estradiol on the hypothalamo-hypophyseal-adrenal axis.     

Reproductive synchrony,parental investment,and the evolutionary dynamics of sexual selection

Computer simulations showed that reproductive synchrony in the greater investing sex can evolve as a strategy for increasing the investment of mates. The potential for synchrony to increase in frequency for this reason decreased with (a) increasing population size, (b) decreasing importance of synchrony-enforced investment, (c) increasing variance in quality among members of the lesser investing sex, and (d) decreasing male: female sex ratio. By reducing the payoffs to desertion, synchrony may result in the evolution of uniquely effective forms of parental care by the lesser investing sex, making desertion unprofitable regardless of the availability of potential mates. Thus relative levels of optimal parental investment are subject to change through the action of sexual selection itself.