Why Parental Sex Ratio Manipulation is Rare in Higher Vertebrates (Invited Article)

The debate over adaptive parental sex ratio adjustment in higher vertebrates appears neither to be resolvable by the current approach, nor does it necessarily make sense. It rests on the a priori supposition of parental manipulation, which is questioned here from first principle. It is considered an unlikely biological hypothesis if we extend our perspective to gametic and offspring optimal strategies, and to the potential mechanisms existing in the avian and mammalian reproductive systems. Evenness of primary sex ratios is expected to be optimal from the gametic point of view and is supposed here to be the more likely evolutionary outcome. Also, manipulations by sex-selective offspring mortality is argued to be unlikely as usually the benefits will be surpassed by the costs incurred. Furthermore, parents can adjust behavioural and energetic investment patterns to their offspring sex (ratio), thereby minimizing any costs of sex ratio control inability. Slight biases in offspring sex ratios are then viewed as resulting from physiological limitations ultimately relating to sex differences in embryonic development. Contrary to recent attempts to understand higher vertebrate sex ratio variation by further refinement of functional models (of parental optima) and data analysis, Bayesian logic precludes those approaches to gain useful new insights. To prove the basic assumption of parental manipulation, apart from defining gametic and offspring optima, the emphasis should lie on identifying control mechanisms by experimental verification.     

The hypothesized hormonal control of mammalian sex ratio at birth--a second update.

Further evidence is adduced to support the hypothesis that the sexes of mammalian (including human) offspring are partially controlled by parental hormone levels at the time of conception. The evidence relates to variation of sex ratios at birth with (1) time of insemination within the cycle of several species, (2) excision of accessory sex glands in rodents, (3) occupation of parents, (4) dominance rating of human mothers and (5) the ordinal rank of wives in polygynous marriages. Much medical research will stem from the hypothesis if it proves to be true. (a) If it were, there would be implications for the testing of causes of many diseases: and it is noted here that the sex ratios of offspring of victims of two types of cancer (prostatic cancer and non-Hodgkin's lymphoma) are consistent with the suspected causes of these diseases. (b) There are a large number of rheumatic diseases associated with the HLA markers B 27 and B 8. These markers are apparently associated respectively with high testosterone levels in men and low testosterone levels in women. If these finding should be confirmed, a causal role for this hormone seems likely in some of these diseases. It will be interesting to examine sex ratios of relatives of probands with these diseases.     

Acute corticosterone administration during meiotic segregation stimulates females to produce more male offspring

Birds have demonstrated a remarkable ability to manipulate offspring sex. Previous studies suggest that treatment with hormones can stimulate females to manipulate offspring sex before ovulation. For example, chronic treatments with corticosterone, the primary stress hormone produced by birds, stimulated significant skews toward female offspring. It has been suggested that corticosterone acts by influencing which sex chromosome is donated by the heterogametic female bird into the ovulated ovarian follicle. However, it is difficult to pinpoint when in developmental time corticosterone affects offspring sex, because in previous studies corticosterone treatment was given over a long period of time. We treated laying hens with acute high-dose corticosterone injections 5 h before the predicted time of ovulation and quantified the sexes of the subsequently ovulated eggs to determine whether mechanisms exist by which corticosterone can skew offspring sex ratios just before ovulation. We hypothesized that an injection of corticosterone coincident with segregation of the sex chromosomes would stimulate hens to produce more female than male offspring. Contrary to our predictions, hens injected with corticosterone produced a significant bias toward male offspring, nearly 83%. These results suggest that acute corticosterone treatment during meiosis I can influence primary sex ratios in birds, potentially through nonrandom chromosome segregation. Furthermore, acute corticosterone exposure, compared with chronic exposure, may act through different mechanisms to skew offspring sex.     

Parental hormone levels and mammalian sex ratios at birth

I have previously suggested that parental levels of several hormones (gonadotrophin, oestrogen, testosterone) at the time of conception affect the sex of mammalian offspring (James, 1986, J. theor. Biol. 118, 427). In this note it is suggested that progesterone also has such an effect. Clutton-Brock & Iason (1986, Q. Rev. Biol. 61, 339) concluded that variation of sex ratio had been reasonably well established with a number of variables in a number of non-human mammalian species. In this note, discussion centres on the adequacy of my hypothesis to accommodate these and other data. The evidence now is strong that hormonal variation is associated with variation of sex ratio at birth in some mammalian species: in a few species (e.g. man and the vole) there is a strong presumption that the relationship is causal. However the same sort of cause apparently affects the sex ratio in opposite directions in different species: so it may be speculated that the same hormone has opposite effects on sex ratio in different species.     

The categories of evidence relating to the hypothesis that mammalian sex ratios at birth are causally related to the hormone concentrations of both parents around the time of conception

This note categorizes the evidence for the hypothesis that mammalian offspring sex ratios (proportions male) are causally related to the hormone levels of both parents around the time of conception. Most of the evidence may be acknowledged to be correlational and observational. As such it might be suspected of having been selected; or of having been subject to other forms of bias or confounding; or, at any rate, of being inadequate as a firm basis for causal inference. However, there are other types of evidence that are not vulnerable to these types of criticism. These are from the following sources: (1) previously neglected data from Nazi Germany and Soviet Russia; (2) fulfilled predictions; (3) genetics; and (4) a network of logically (mathematically) related propositions, for some of which there is overwhelming empirical evidence. It is suggested that this variety of evidence confers greater overall credibility on the hypothesis than would be the case if all the evidence were of the same observational/correlational status. This observational/correlational evidence is tabulated to illustrate its consistency.     

Further support for the hypothesis that parental hormone levels around the time of conception are associated with human sex ratios at birth

During the past year, data have been published on the offspring sex ratios of people diagnosed with toxoplasmosis, hepatitis B, and pre- and post-menopausal breast cancer. It is shown here how these offspring sex ratios constitute further support for the hypothesis that mammalian (including human) parental hormone concentrations around the time of conception partially control the sexes of the resulting infants. If this interpretation were correct, then hormonal treatments might be considered for some or all of these conditions. It is intended that anyone who has read the present note and my two previous papers (James, 1996, 2004) should be aware of all the data relating to the hypothesis.     

The “balance” argument and the evolution of sex

The “balance” argument suggests that if sex were maladaptive at the individual level, it would be quickly lost from species with asexual/sexual alternation. Williams has suggested an “Aphid-Rotifer” model for such species. It has the following characteristics (a) parthenogenesis is favoured when the environment is stable (b) when the environment changes qualitatively, sex generates offspring with an increased fitness variance compared to parthenogenetic progeny (c) if selection is intense and sib competition occurs then sex is favoured. It is argued here that condition (b) is not essential to the model. An increased fitness variance may be generated by the recombination of unfavourable mutations when one or more of the following occur; (1) founder effects (2) inbreeding (3) haplo-diploidy (4) intra-male competition. Parthenogenesis sustains an advantage when selection is relaxed and the possession of mutations is not reflected in differences in fitness. Sex is favoured when selection is intense and fitness reflects the possession of unfavourable mutations.     

Are oral clefts a consequence of maternal hormone imbalance? evidence from the sex ratios of sibs of probands

BACKGROUND: The causes of oral clefts (cleft lip with or without cleft palate, CL/P, and cleft palate alone, CP) have not been established. However, maternal intrauterine hormone profiles have been suspected of being involved. There is now substantial evidence that maternal hormone concentrations around the time of conception partially control the sexes of offspring. It is possible that the hormone profiles that control sex of offspring share features of the profiles suspected of causing clefts. This can be tested by examining the sex ratios (proportions male) of the unaffected sibs of probands. If these sex ratios are skewed in the same direction as that of probands, that suggests, ex hypothesi, maternal hormonal involvement in the causation of clefts. METHODS: Accordingly, a search was made for data on the sex ratios of the unaffected sibs of probands with clefts. For reasons given in the text, this search was informal rather than based on electronic data retrieval systems. Nine papers were located giving sex ratios of sibs of probands with CL/P and CP. RESULTS: Published data suggest that the sibs of probands with CL/P have a significantly higher sex ratio than the sibs of probands with CP. Thus the sib sex ratios are skewed in the same direction as those of the probands themselves. In other words, parents (mothers) of CL/P patients apparently have a tendency to produce boys, and parents of CP patients to produce girls. CONCLUSION: Accordingly, it is suggested that maternal hormone profiles may partially explain the unusual sex ratios (of probands and their sibs), as well as the malformations.     

Adaptive Offspring Sex Ratio Depends on Male Tail Length in the Guppy

A biased sex ratio in a brood is considered to be an adaptive strategy under certain circumstances. For example, if the expected reproductive success of one sex is greater than that of the other, parents should produce more offspring of the former sex than the latter. A previous study has documented that in the guppy, Poecilia reticulata, the female offspring of males possessing proportionally longer tails exhibit smaller body sizes and show decreased reproductive outputs than those of males having shorter tails. On the other hand, the total lengths of the male offspring of the long‐tailed males are larger because of their longer tails; consequently, they exhibit greater sexual attractiveness to females. Therefore, it has been hypothesized that this asymmetry in the expected reproductive success between the male and female offspring of long‐tailed males may result in a biased sex ratio that is dependent on the tail lengths of their fathers. This hypothesis was tested in the present study. The results showed that the females that mated with long‐tailed males produced more male offspring than those that mated with short‐tailed males. Logistic regression analysis showed that the ratio of tail length to the standard length of the fathers is a determinant factor of the sex of their offspring. These results suggest that the manipulation of the offspring sex ratios by parents enhances the overall fitness of the offspring.     

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.     

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.     

Female blue tits adjust parental effort to manipulated male UV attractiveness

The differential allocation hypothesis predicts that parents should adjust their current investment in relation to perceived mate attractiveness if this affects offspring fitness. It should be selectively advantageous to risk more of their future reproductive success by investing heavily in current offspring of high reproductive value but to decrease investment if offspring value is low. If the benefits of mate attractiveness are limited to a particular offspring sex we would instead expect relative investment in male versus female offspring to vary with mate attractiveness, referred to as 'differential sex allocation'. We present strong evidence for differential allocation of parental feeding effort in the wild and show an immediate effect on a component of offspring fitness. By experimentally reducing male UV crown coloration, a trait known to indicate attractiveness and viability in wild-breeding blue tits (Parus caeruleus), we show that females, but not males, reduce parental feeding rates and that this reduces the skeletal growth of offspring. However, differential sex allocation does not occur. We conclude that blue tit females use male UV coloration as an indicator of expected offspring fitness and adjust their investment accordingly.     

Maternal nutrition affects reproductive output and sex allocation in a lizard with environmental sex determination

Life-history traits such as offspring size, number and sex ratio are affected by maternal feeding rates in many kinds of animals, but the consequences of variation in maternal diet quality (rather than quantity) are poorly understood. We manipulated dietary quality of reproducing female lizards (Amphibolurus muricatus; Agamidae), a species with temperature-dependent sex determination, to examine strategies of reproductive allocation. Females maintained on a poor-quality diet produced fewer clutches but massively (twofold) larger eggs with lower concentrations of yolk testosterone than did conspecific females given a high-quality diet. Although all eggs were incubated at the same temperature, and yolk steroid hormone levels were not correlated with offspring sex, the nutrient-deprived females produced highly male-biased sex ratios among their offspring. These responses to maternal nutrition generate a link between sex and offspring size, in a direction likely to enhance maternal fitness if large body size enhances reproductive success more in sons than in daughters (as seems plausible, given the mating system of this species). Overall, our results show that sex determination in these animals is more complex, and responsive to a wider range of environmental cues, than that suggested by the classification of 'environmental sex determination'.     

Experimental alteration of litter sex ratios in a mammal

Adaptive theory predicts that mothers would be advantaged by adjusting the sex ratio of their offspring in relation to their offspring's future reproductive success. Studies investigating sex ratio variation in mammals, including humans, have obtained notoriously inconsistent results, except when maternal condition is measured around conception. Several mechanisms for sex ratio adjustment have been proposed. Here, we test the hypothesis that glucose concentrations around conception influence sex ratios. The change in glucose levels resulted in a change in sex ratios, with more daughters being born to females with experimentally lowered glucose, and with the change in glucose levels being more predictive than the glucose levels per se. We provide evidence for a mechanism, which, in tandem with other mechanisms, could explain observed sex ratio variation in mammals.     

Adaptive biases in offspring sex ratios established before birth in a marsupial, the common brushtail possum Trichosurus vulpecula

Offspring sex ratios in the common brushtail possum are malebiased in many populations, and there is evidence that inter-populationdifferences in sex ratios represent adaptive responses to localconditions. However, how these biases are produced is not known.Using comparisons between populations with and without biasedoffspring sex ratios, we show that biases in this species arenot produced by sex-differential mortality between birth andweaning or sex-selective termination of pregnancy. Rather,adjustment in the sex ratio of offspring are evidently dueto shifts in the probability of conceiving male and femaleoffspring.     

SEX-RATIO MANIPULATION IN COLOR-BANDED POPULATIONS OF ZEBRA FINCHES

Significant correlations were found between attractiveness of leg-band color (determined by preference tests [Burley et al., 1982]) and sex ratio of offspring in two long-term breeding experiments involving zebra finches. In both experiments, birds with attractive band colors produced more same-sex offspring, while birds with unattractive band colors produced more opposite-sex offspring. The results of these experiments are consistent with those of a previous experiment (Burley, 1981). To explain the earlier results, I hypothesized that parents adjust their allocation to sons and daughters to produce offspring they “expect” to be most attractive. The purpose of such sex-ratio manipulation is to enhance fitness by the production of offspring with superior mate-getting opportunities. Two alternative hypotheses are presented here. One is that sex ratios change with parental age and/or experience. Evidence does not support this hypothesis. There were no temporal trends in sex ratio independent of band color. A second possibility is that sex ratios reflect differential parental ability to rear sons and daughters. This hypothesis cannot be conclusively tested on the basis of present evidence, but available evidence does not support it. Within color classes, weights of sons and daughters did not differ. Evidence indicates that parents effect secondary sex-ratio manipulation through the selective rejection of young, usually within six days of hatching. There is no evidence of manipulation prior to egg-laying. The costs associated with brood reduction probably set limits on the extent to which secondary manipulation can be profitably employed.     

The variations of human sex ratio at birth during and after wars, and their potential explanations

Data on wartime sex ratios (proportions male at birth) are reviewed. Two sorts of variation are empirically well supported viz. (a) rises during and just after both World Wars and (b) a fall in Iran during the Iran-Iraq War. Potential explanations are offered here for these rises and fall. The fall seems plausibly explained by psychological stress causing pregnant women disproportionately to abort male fetuses. The rises may be explained by either or both of two different forms of hypothesis viz. (i) Kanazawa's “returning soldier” hypothesis and (ii) variation in coital rates. The coital rate hypothesis potentially accounts, in slightly different ways, for the rises both during, and just after, some wars. The argument that coital rate affects sex ratio just after wars seems to be supported by evidence that in some combatant countries, dizygotic (DZ) twinning rates (which also reportedly vary with coital rate) peaked after the World Wars. The suggestion that war is associated with rises in sex ratio at birth was first made more than two centuries ago. However, I have been unable to locate direct supporting sex ratio data relating to any conflict before World War One. So it would be useful if historical demographers were to search for such data relating to these earlier wars.     

Female Control of Offspring Sex Ratios Based on Male Attractiveness in the Guppy

The sex allocation hypothesis predicts that females manipulate the offspring sex ratios according to mate attractiveness. Although there is increasing evidence to support this prediction, it is possible that paternal effects may often obscure the relationship between female control of offspring sex ratios and male attractiveness. In the present study, we examined whether females played a primary role in the manipulation their offspring sex ratios based on male attractiveness, in the guppy Poecilia reticulata, a live‐bearing fish. We excluded the paternal effects by controlling the relative sexual attractiveness of the male by presenting them to the females along with a more attractive or less attractive stimulus male. The test male was perceived to be relatively more attractive by females when it was presented along with a less attractive stimulus male, or vice versa. Subsequently, test male was mated in two different roles (relatively more and less attractive) with two females. If females were responsible for offspring sex ratio manipulation, the sex ratio of the brood would be altered on the basis of the relative attractiveness of the test male. On the other hand, if males play a primary role in offspring sex ratio manipulation, the sex ratios would not differ with the relative attractiveness of the test male. We found that females gave birth to more male‐biased broods when they mated with test males in the attractive role than when they mated with males in the less attractive role. This finding suggests that females are responsible for the manipulation of offspring sex ratios based on the attractiveness of their mates.     

Trends in Population Sex Ratios May be Explained by Changes in the Frequencies of Polymorphic Alleles of a Sex Ratio Gene

A test for heritability of the sex ratio in human genealogical data is reported here, with the finding that there is significant heritability of the parental sex ratio by male, but not female offspring. A population genetic model was used to examine the hypothesis that this is the result of an autosomal gene with polymorphic alleles, which affects the sex ratio of offspring through the male reproductive system. The model simulations show that an equilibrium sex ratio may be maintained by frequency dependent selection acting on the heritable variation provided by the gene. It is also shown that increased mortality of pre-reproductive males causes an increase in male births in following generations, which explains why increases in the sex ratio have been seen after wars, also why higher infant and juvenile mortality of males may be the cause of the male-bias typically seen in the human primary sex ratio. It is concluded that various trends seen in population sex ratios are the result of changes in the relative frequencies of the polymorphic alleles of the proposed gene. It is argued that this occurs by common inheritance and that parental resource expenditure per sex of offspring is not a factor in the heritability of sex ratio variation.     

Sex ratio manipulation within broods of house wrens, Troglodytes aedon

Trivers & Willard (1973, Science, 179, 90-92) developed an economic theory of parental investment to explain how the relative profitability of sons and daughters varies under specific ecological conditions. In their maternal condition hypothesis they proposed that in polygynous species, the sex of an offspring should be associated with the amount of parental care likely to be made available to it. In these species, the amount of parental investment directed towards offspring may differentially influence the fitness of male and female offspring because males in better than average condition as adults may enjoy larger fitness gains than a female would if she were in better than average condition, while the reverse may be true when conditions are poor. I tested this hypothesis by determining the sex of specific offspring within house wren broods. Because hatching is asynchronous and fledging is synchronous in this polygynous species, last-hatched young fledge having received less parental care than their broodmates. I predicted that last-hatched offspring would be more likely to be female. I found that these young were indeed more likely to be females, were more likely to have hatched from last-laid eggs and were fledging in poor condition relative to their broodmates. I propose that female house wrens behave in a manner consistent with the predictions of the Trivers & Willard hypothesis by producing female offspring last in the laying sequence of their clutches. Copyright 2000 The Association for the Study of Animal Behaviour.