Evidence that Mammalian Sex Ratios at Birth are Partially Controlled by Parental Hormone Levels at The Time of Conception

Evidence is adduced for the hypothesis that mammalian (including human) sex ratios at birth are partially controlled by the hormone levels of both parents at the time of conception. Sex ratio variation is considered under three main headings viz that identified by Clutton-Brock & Iason (1986); that identified since that paper; and other variation mainly relating to human beings. Some of the evidence is strong.     

SEX RATIO VARIATION IN THE LESSONIA NIGRESCENS COMPLEX (LAMINARIALES,PHAEOPHYCEAE): EFFECT OF LATITUDE,TEMPERATURE, AND MARGINALITY1

Little is known about variation of sex ratio, the proportion of males to females, in natural populations of seaweed, though it is a major determinant of the mating system. The observation of sexual chromosomes in kelps suggested that sex is partly genetically determined. However, it is probably not purely genetic since the sex ratio can be modified by environmental factors such as salinity or temperature. In this paper, sex ratio variation was studied in the kelp Lessonia nigrescens Bory complex, recently identified as two cryptic species occurring along the Chilean coast: one located north and the other south of the biogeographic boundary at latitude 29°–30° S. The life cycle of L. nigrescens is characterized by an alternation of microscopic haploid gametophytic individuals and large macroscopic fronds of diploid sporophytes. The sex ratio was recorded in progenies from 241 sporophytic individuals collected from 13 populations distributed along the Chilean coast in order (i) to examine the effect of an environmental gradient coupled with latitude, and (ii) to compare marginal populations to central populations of the two species. In addition, we tested the hypothesis that the sex ratios of the two cryptic species would be affected differently by temperature. First, our results demonstrate that sex ratio seems to be mainly genetically determined and temperature can significantly modify it. Populations of the northern species showed a lower frequency of males at 14°C than at 10°C, whereas populations of the southern species showed the opposite pattern. Second, both species displayed an increased variation in sex ratio at the range limits. This greater variation at the margins could be due either to differential mortality between sexes or to geographic parthenogenesis (asexual reproduction).     

Does predation result in adult sex ratio skew in a sexually dimorphic insect genus?

Theory proposes that sexually dimorphic, polygynous species are at particularly high risk of sex-biased predation, because conspicuous males are more often preyed upon compared to females. We tested the effects of predation on population sex ratio in a highly sexually dimorphic insect genus (Hemideina). In addition, introduction of a suite of novel mammalian predators to New Zealand during the last 800 years is likely to have modified selection pressures on native tree weta. We predicted that the balance between natural and sexual selection would be disrupted by the new predator species. We expected to see a sex ratio skew resulting from higher mortality in males with expensive secondary sexual weaponry; combat occurs outside refuge cavities between male tree weta. We took a meta-analytic approach using generalized linear mixed models to compare sex ratio variation in 58 populations for six of the seven species in Hemideina. We investigated adult sex ratio across these populations to determine how much variation in sex ratio can be attributed to sex-biased predation in populations with either low or high number of invasive mammalian predators. Surprisingly, we did not detect any significant deviation from 1 : 1 parity for adult sex ratio and found little difference between populations or species. We conclude that there is little evidence of sex-biased predation by either native or mammalian predators and observed sex ratio skew in individual populations of tree weta is probably an artefact of sampling error. We argue that sex-biased predation may be less prevalent in sexually dimorphic species than previously suspected and emphasize the usefulness of a meta-analytic approach to robustly analyse disparate and heterogeneous data.     

Sexual size dimorphism and sex ratio in arthropod ectoparasites: contrasting patterns at different hierarchical scales

The aims of this study were to determine whether sexual size dimorphism in fleas and gamasid mites (i) conforms to Rensch’s rule (allometry of sexual size dimorphism) and (ii) covaries with sex ratio in infrapopulations (conspecific parasites harboured by an individual host), xenopopulations (conspecific parasites harboured by a population of a given host species in a locality) and suprapopulations (conspecific parasites harboured by an entire host community in a locality). Rensch’s rule in sexual size dimorphism was tested across 150 flea and 55 mite species, whereas covariation between sexual size dimorphism and sex ratio was studied using data on ectoparasites collected from small mammalian hosts in Slovakia and western Siberia. For fleas, we controlled for the confounding effect of phylogeny. The slope of the linear regression of female size on male size was significantly smaller than 1 in fleas, but did not differ from 1 in mites. The proportion of males in flea infrapopulations significantly increased with an increase in the female-to-male body size ratio. The same was true for obligatory haematophagous mites. No relationship between sex ratio and sexual size dimorphism was found for xenopopulations of either taxon or for mite suprapopulations. However, when controlling for the confounding effect of phylogeny, a significant negative correlation between sex ratio and sexual size dimorphism was revealed for flea suprapopulations. We conclude that (i) some macroecological patterns differ between ectoparasite taxa exploiting the same hosts (allometry in sexual size dimorphism), whereas other patterns are similar (sexual size dimorphism-sex ratio relationship in infrapopulations), and (ii) some patterns are scale-dependent and may demonstrate the opposite trends in parasite populations at different hierarchical levels.     

Sexually antagonistic coevolution in a mating system: combining experimental and comparative approaches to address evolutionary processes

We combined experimental and comparative techniques to study the evolution of mating behaviors within in a clade of 15 water striders (Gerris spp.). Superfluous multiple mating is costly to females in this group, and consequently there is overt conflict between the sexes over mating. Two alternative hypotheses that could generate interspecific variation in mating behaviors are tested: interspecific variation in optimal female mating rate versus sexually antagonistic coevolution of persistence and resistance traits. These potentially coevolving traits include male grasping and female antigrasping structures that further the interests of one sex over the other during premating struggles. Both processes are known to play a role in observed behavioral variation within species. We used two large sets of experiments to quantify behavioral differences among species, as well as their response to an environmentally (sex-ratio) induced change in optimal female mating rate. Our analysis revealed a large degree of continuous interspecific variation in all 20 quantified behavioral variables. Nevertheless, species shared the same set of behaviors, and each responded in a qualitatively similar fashion to sex-ratio alterations. A remarkably large proportion (> 50%) of all interspecific variation in the magnitude of behaviors, including their response to sex ratio, could be captured by a single multivariate axis. These data suggest tight coevolution of behaviors within a shared mating system. The pattern of correlated evolution was best accounted for by antagonistic coevolution in the relative abilities of each sex to control the outcome of premating struggles. In species where males have a relative advantage, mating activity is high, and the opposite is found in species where females have gained a relative advantage. Our analyses also suggested that evolution has been unconstrained by history, with no consistent evolutionary tendency toward or away from male or female relative advantage.     

SEX RATIOS AND CONDITIONS REQUIRED FOR ENVIRONMENTAL SEX DETERMINATION IN ANIMALS

Environmental sex determination (ESD) is a system of sexual determination that is influenced by a variable environment. Once sex is determined it is then fixed for life. The model of Charnov & Bull (1977) proposes that ESD is favoured by natural selection when an individual's fitness as a male or female is strongly influenced by environmental conditions and when the individual has little control over which environment it will experience. Adaptive sex ratio variation is considerably easier for organisms with ESD, and this feature is the ultimate cause for the evolution and maintenance of ESD. ESD is taxonomically widely expressed, and more cases are likely to be discovered. Both environmental and genotypic sex determination mechanisms are found in closely related species. Evidence of geographical variation in the degree and in the critical environmental values of ESD within the same species has also been discovered, e.g. in the fish Menidia menidia and in the crustacean Gammarus duebeni. The factors causing sex determination in invertebrates include temperature, daylength, nutrition, density, humidity, ionic composition of the environment, pH, carbon dioxide, UV light, metabolic products, parasites, exposure to the opposite sex of the same species, and in parasitoids also host size, age and type. In vertebrates temperature is the dominant factor causing sex determination, though in fish also pH, salinity, light, water quality and nutrition, and in turtles water potential of the substrate have some effect on the sex expression. Most of these factors influence growth through resource availability or developmental speed. In most cases of ESD in invertebrates and fish, the environmental factor has a gradual effect on the sex expression, in contrast to the typical steep threshold mode found in reptiles. These differences might be due to the fact that invertebrates exhibiting ESD are commonly parasitic or confined to aquatic environments, where less spatial microhabitat differentiation exists. Sex ratio data available from nature for animals with ESD are quite limited, except for reptiles. In the laboratory sex ratios can be varied more widely than what is observed in nature. There are a number of characteristic features some of which are found in each species exhibiting ESD: (1) Patchy environments, (2) variable sex ratios, (3) parthenogenesis in addition to bisexuality, (4) parasitism, (5) aquatic habitats, (6) sexual dimorphism, (7) females larger than males, and (8) local mate competition.     

Between-year variation in population sex ratio increases with complexity of the breeding system in Hymenoptera

While adaptive adjustment of sex ratio in the function of colony kin structure and food availability commonly occurs in social Hymenoptera, long-term studies have revealed substantial unexplained between-year variation in sex ratio at the population level. In order to identify factors that contribute to increased between-year variation in population sex ratio, we conducted a comparative analysis across 47 Hymenoptera species differing in their breeding system. We found that between-year variation in population sex ratio steadily increased as one moved from solitary species, to primitively eusocial species, to single-queen eusocial species, to multiple-queen eusocial species. Specifically, between-year variation in population sex ratio was low (6.6% of total possible variation) in solitary species, which is consistent with the view that in solitary species, sex ratio can vary only in response to fluctuations in ecological factors such as food availability. In contrast, we found significantly higher (19.5%) between-year variation in population sex ratio in multiple-queen eusocial species, which supports the view that in these species, sex ratio can also fluctuate in response to temporal changes in social factors such as queen number and queen-worker control over sex ratio, as well as factors influencing caste determination. The simultaneous adjustment of sex ratio in response to temporal fluctuations in ecological and social factors seems to preclude the existence of a single sex ratio optimum. The absence of such an optimum may reflect an additional cost associated with the evolution of complex breeding systems in Hymenoptera societies.     

Prenatal sex ratios and expression of sexually dimorphic traits in three snake species

Variation in intrauterine exposure to hormones associated with variation in the sex of litter mates has well-established and far-reaching effects on sexual development in some mammals. Research on this phenomenon in reptiles is scant, but suggests that lizards may follow the mammalian model whereas snakes may be affected differently. We examined sex-specific expression of four sexually dimorphic traits (tail length, head length, ventral scale count, swimming speed) in three species of snakes (Nerodia sipedon, Thamnophis sirtalis, T. sauritus) relative to litter sex ratios. We found little evidence that traits in either sex were masculinized or feminized in response to variation in litter sex ratio. The one significant result appeared best explained as a statistical artifact attributable to a single litter. Our results indicate that snakes are different from the one lizard studied to date. Unlike previous suggestions that prenatal hormonal mechanisms operate differently in snakes and lizards, however, the difference appears to be that development of sexually dimorphic traits in lizards is affected by litter sex ratios whereas in snakes it is not.     

Facultative sex ratio adjustment in response to male tarsus length in the Varied Tit Parus varius

During the last decade, evidence from a number of studies has suggested systematic deviations from a 1 : 1 primary sex ratio in birds, in spite of the fact that birds have chromosomal sex determination systems; the mechanism of sex allocation is not fully understood. However, it still remains uncertain whether adaptive manipulations of primary sex ratio occur, especially in Parus species. We studied sex ratio variation in the Varied Tit Parus varius , which is a socially monogamous species similar to the Great Tit P. major and the Blue Tit P. caeruleus . In total, 362 chicks that hatched from 72 broods over 3 years were sexed. Of all nestlings, 51.9% (188/362) were male. The nestling sex ratio did not differ significantly from unity. However, the proportion of sons in each brood was significantly and positively related to the father's tarsus length. This corresponds with our predictions, given that larger males have higher resource holding potential if tarsus length is a heritable character between fathers and sons.     

Evidence of oligogenic sex determination in the apple snail <Emphasis Type="Italic">Pomacea canaliculata</Emphasis>

A small number of genes may interact to determine sex, but few such examples have been demonstrated in animals, especially through comprehensive mating experiments. The highly invasive apple snail Pomacea canaliculata is gonochoristic and shows a large variation in brood sex ratio, and the involvement of multiple genes has been suggested for this phenomenon. We conducted mating experiments to determine whether their sex determination involves a few or many genes (i.e., oligogenic or polygenic sex determination, respectively). Full-sib females or males that were born from the same parents were mated to an adult of the opposite sex, and the brood sex ratios of the parents and their offspring were investigated. Analysis of a total of 4288 offspring showed that the sex ratios of offspring from the full-sib females were variable but clustered into only a few values. Similar patterns were observed for the full-sib males, although the effect was less clear because fewer offspring were used (n?=?747). Notably, the offspring sex ratios of all full-sib females in some families were nearly 0.5 (proportion of males) with little variation. These results indicate that the number of genotypes of the full-sibs, and hence genes involved in sex determination, is small in this snail. Such oligogenic systems may be a major sex-determining system among animals, especially those with variable sex ratios.     

Phenology, sex ratio, and spatial distribution among dioecious species of Trichilia (Meliaceae)

The flowering, sex ratio, and spatial distribution of four dioecious species of Trichilia (Meliaceae) were studied in a semi-deciduous forest in southeastern Brazil. All reproductive trees (T. clausseni, T. pallida and T. catigua) with dbh > or = 5 cm within a 1-ha plot were collected, sexed, mapped and, for individuals of each species, the distances to the nearest neighbour of the same and opposite sex were measured. For the shrub species T. elegans (dbh < 5 cm), all reproductive individuals were sampled randomly in 10 samples of 10 x 10 m. The reproductive phenology was observed at weekly to monthly intervals from May 1988 to January 1990. The species are strictly dioecious, did not present any sex-mixed trees or sex switching during the study, and sex ratio did not differ significantly from 1 : 1. The size distributions and the relative size variation were not significantly different between sexes. There was no significant segregation or clumping between individuals of either sex and no fruit production without pollination. Onset of flowering and flowering peak were synchronous between male and female plants for all species studied. Flower synchrony was related to outcrossing and pollinator attraction rather than climatic factors.     

Sex ratio, life-history invariants, and patterns of sex change in a family of protandrous gastropods

Application of optimality theory to the evolution of life histories has been broadly successful in predicting the conditions favoring sex change, the type of change, and the timing of such changes. The size advantage hypothesis predicts that the optimal size at which an individual should change sex is a function of its size and the size and sex of its potential mates. I collected data on the size, sex, and grouping of individuals of 27 populations of 19 species of the calyptraeids, a family of protandrous marine gastropods that includes Crepidula. These data are used to test the following predictions about variation in size at sex change: (1) sex ratio is biased toward the first sex; (2) the ratio of the size at sex change to the maximum size is a life-history invariant; and (3) species that form variable-sized groups or stacks have more variation in size at sex change than species that show less variation in stack formation. Across all 19 species, sex ratio was not significantly more often biased toward the first sex than it was toward the second sex, although sex ratios were significantly male biased more often than they were significantly female biased. Sex ratios ranged from 0.05 to 0.91, and this variation was related to mode of development, skew in size distribution, and frequency of stacking, but not with maximum body size. There was little evidence that the ratio of size at sex change and maximum size is invariant. There is evidence that one of the main underlying assumptions of this life-history invariant, that male fertility increases with the same function of size in all species, is invalid for calyptraeids and probably for other animals. Finally, species that form larger stacks or mating groups had more variation in size at sex change within a population than species that were generally solitary. These results suggest that information about individual groupings should be included in predictions of life-history theory and that more information about the relationship between male fitness and size is also needed.     

Neither Biased Sex Ratio nor Spatial Segregation of the Sexes in the Subtropical Dioecious Tree Eurycorymbus cavaleriei (Sapindaceae)

Knowledge of sex ratio and spatial distribution of males and females of dioecious species is both of evolutionary interest and of crucial importance for biological conservation. Eurycorymbus cavaleriei, the only species in the genus Eurycorymbus (Saplndaceae), is a dioecious tree endemic to subtropical montane forest in South China. Sex ratios were investigated in 15 natural populations for the two defined ages (young and old). Spatial distribution of males and females was further studied in six large populations occurring in different habitats (fragmented and continuous). The study revealed a slight trend of malebiased sex ratio in both ages of E. cavaleriei, but sex ratio of most populations (13 out of 15) did not display statistically significant deviation from equality. All of the four significantly male-biased populations in the young class shifted to equality or even female-biased. The Ripley's K analysis of the distribution of males with respect to females suggested that individuals of the opposite sexes were more randomly distributed rather than spatially structured. These results suggest that the male-biased sex ratio in E. cavaleriei may result from the precocity of males and habitat heterogeneity. The sex ratio and the sex spatial distribution pattern are unlikely to constitute a serious threat to the survival of the species.     

Species richness in mammalian herbivores: patterns in the boreal zone

Latitudinal gradients in species diversity are well established for a number of plant and animal taxa. Both historical and present-day environmental factors have been suggested to be responsible for observed patterns. We tested the hypothesis that current environmental features of the environment (primary productivity and regional landscape structure) may explain the longitudinal variation in species richness of mammalian herbivores in the Holarctic boreal zone. Mammalian herbivore species diversity was strongly correlated with a number of environmental variables measured. We reduced the data set by a principal components analysis (PCA), and found that in the Palearctic, species richness is positively related to warm climate (high temperature sum), the number of hardwood species, and the area of boreal forest. In the Nearctic, species richness increases as the length of the growing season and the number of coniferous tree species increase. Thus indirect measures of primary productivity as well as tree species number may accurately predict species richness in mammalian herbivores. In addition, there seems to be a strong species-area effect at the regional level. The larger and more homogeneous in terms of forest coverage a boreal section is, the more species coexist there.     

The variations of human sex ratio at birth with time of conception within the cycle, coital rate around the time of conception, duration of time taken to achieve conception, and duration of gestation: a synthesis

There is a large research literature on the variation of human sex ratio (proportion of males at birth) with (1) time of insemination within the mother's fruitful cycle (TWC), (2) duration of gestation (DOG), (3) coital frequency, here called ‘coital rate’ (CR) and (4) duration of time taken to achieve conception in a period of risk (viz. in the absence of birth limitation methods) (TTC). The variation of sex ratio with each of these four variables has usually been treated as a discrete topic. Consider the four propositions that each of these sorts of variation exists. Here it is argued that these propositions entail one another to varying degrees, and that, for that reason, empirical failures to detect (at conventional levels of significance) one such form of variation (as e.g. with time to conception) should not justify rejecting the hypothesis that such variation exists until the whole network of propositions has been considered. Evidence that offspring sex ratio varies with time of conception within the cycle is strong. It is argued here that, as a consequence, the available data constitute evidence that sex ratio varies with CR and with time to achieve conception, although this variation is small, difficult to detect and of no clinical significance. Lastly, sex ratio varies substantially with DOG, though the explanation for this is not established: it is suggested that the present treatment provides a testable framework for such an explanation.     

Primary structure from amino acid and cDNA sequences of two Cu,Zn superoxide dismutase variants from Xenopus laevis

A mixture of two different amino acid sequences was discovered in Cu,Zn superoxide dismutase purified from the amphibian Xenopus laevis. No N-terminal post-translational modification was found. The high number of substitutions in the sequence suggested that protein heterogeneity was a product of gene duplication. This was confirmed by isolation of two different cDNA clones. Nucleotide sequence analysis allowed the primary structure of the two peptide chains to be unambiguously assigned. The observed changes (19 in 150 residues) are distributed along the peptide chain to give similar protein net charges although substitutions of the same polarity and/or charge were the exception rather than the rule. The degree of diversity between the two Xenopus variants is comparable to that between mammalian sequences and shows that the putative increase of the rate of mutation for Cu,Zn superoxide dismutase at later evolution stages (Y. M. Lee et al., 1985, Arch. Biochem. Biophys. 241, 577-589; G. J. Steffens et al., 1986, Biol. Chem. Hoppe-Seyler 367, 1017-1024) is observed in amphibians. This is the first time complete sequences for Cu,Zn superoxide dismutase variants from the same organism have been found to be products of divergent genes and not simply allelic mutations.     

Sex ratio, dominance status and maternal hormone levels at the time of conception

Sex ratio is a topic which has attracted the attention of epidemiologists and evolutionary biologists. But their work has been conducted largely in parallel: hitherto they seem not to have found much inspiration in one another's results. Their attitudes, environments and problems have all been strikingly different. The present note shows how one of the biologists' findings may be explained by a hypothesis based on epidemiological observation. The hypothesis (that sex ratio of offspring is partially controlled by maternal hormone levels at the time of conception) needs testing in a number of species.     

Life-history and sex allocation in Trypoxylon (syn. Trypargilum) lactitarse (Hymenoptera; Crabronidae)

Hymenopterans have become a model for the study of factors that govern sex allocation. In 1983, Seger proposed a model to study Sphecidae wasps with a strong prediction that sex ratio for univoltine wasps should be 1 : 1 (female : male), and for partially bivoltine species it should be male-biased. The present study investigates if Trypoxylon lactitarse (Saussure, 1867) is a univoltine or a bivoltine species and if Seger's model prediction fits the pattern of sex ratio found in this species. The study was carried out at Parque Municipal das Araucárias, in the municipality of Guarapuava, state of Paraná, southern Brazil, from December 2001 to December 2004. Nests of T. lactitarse were obtained using trap-nests drilled longitudinally to a depth to 80 mm with 7.0, 10.0 and 13.0 mm opening diameter. They were placed in a very heterogeneous site filled with araucaria forests, swamps and grasslands. Trypoxylon lactitarse showed two alternative life histories: either they pupated immediately and emerged as adults later in the same season (direct development), or they entered diapause, overwintering and pupating the following spring (delayed development). Its annual sex ratios were not significantly different from 1 : 1, and both sex ratio of overwintering and sex ratio of direct-developing wasps were also not significantly different from 1 : 1, in all years of this study. By examining these results, it was possible to conclude that although T. lactitarse is a multivoltine species, with four generations per year and two alternative life histories, its sex ratio did not support Seger's model.     

Meadow Voles (Microtus pennsylvanicus) and Prairie Voles (M. ochrogaster) Differ in Their Responses to Over-Marks from Opposite- and Same-Sex Conspecifics

Over‐marking occurs when one individual deposits its scent mark on the scent mark of a conspecific. Previous studies have shown that meadow voles (Microtus pennsylvanicus) and prairie voles (M. ochrogaster) that were exposed to an over‐mark of two same‐sex conspecifics, later responded similarly to the top‐scent mark but differed in their response to the bottom‐scent mark. In the present study, we examined the responses of meadow voles and prairie voles to same‐sex and mixed‐sex over‐marks to ascertain whether their responses reflect the different tactics which males and females in promiscuous (meadow voles) and monogamous (prairie voles) species use to attract opposite‐sex conspecifics and to compete with same‐sex conspecifics. Males and females of both species spent more time investigating the mark of the top‐scent donor than that of the bottom‐scent donor of an over‐mark. Meadow voles exposed to a mixed‐sex over‐mark spent more time investigating the mark of the opposite‐sex conspecific independently of whether it was from the top‐ or bottom‐scent donor. In contrast, prairie voles spent more time investigating the mark of the opposite‐sex donor if it was from the top‐scent donor. These results suggest that: (i) over‐marking serves a competitive function; (ii) the scent marks of individuals attract multiple mates in promiscuous species such as the meadow vole; and (iii) the scent marks of individuals establish and maintain pair bonds between familiar opposite‐sex conspecifics in monogamous species such as the prairie vole.     

Parental hormone levels and the possibility of establishing that some mammalian sex ratio variation is adaptive

The problem of whether some mammalian sex ratio variation is adaptive is proving intractable. A fresh approach to the problem is suggested here.