Studies Of Sex Allocation Research Articles

Condition‐dependent maternal sex allocation in horses can be demonstrated using a biologically relevant, multivariable condition measurement

AbstractMaternal condition is influenced by multiple variables that individuals experience at seasonal and local levels, and thus condition‐dependent sex allocation is likely also multifactorial. Here, we test the Trivers‐Willard Hypothesis (TWH) using a multivariable approach on a dataset of thoroughbred mare breeding records. There is no sex ratio variation when examined at univariable level, mirroring the usual approach to test condition‐dependent sex allocation. Conversely, the multivariate model shows multiple variables interact to influence the likelihood of producing a male. Mare and management variables that represent better body condition is associated with an increase in likelihood of a male offspring. The magnitude and direction of sex ratio skew correspond closely with predicted mare energy balance, consistent with TWH predictions. Our findings therefore support the TWH and show that, while sex allocation is multifactorial, maternal energy status emerges as the dominant driver. The additive and agonistic interactions of different variables demonstrate that a multifactorial approach should be a key consideration in sex allocation studies.

The rarer-sex effect.

The study of sex allocation-that is, the investment of resources into male versus female reproductive effort-yields among the best quantitative evidence for Darwinian adaptation, and has long enjoyed a tight and productive interplay of theoretical and empirical research. The fitness consequences of an individual's sex allocation decisions depend crucially upon the sex allocation behaviour of others and, accordingly, sex allocation is readily conceptualized in terms of an evolutionary game. Here, I investigate the historical development of understanding of a fundamental driver of the evolution of sex allocation-the rarer-sex effect-from its inception in the writing of Charles Darwin in 1871 through to its explicit framing in terms of consanguinity and reproductive value by William D. Hamilton in 1972. I show that step-wise development of theory proceeded through refinements in the conceptualization of the strategy set, the payoff function and the unbeatable strategy. This article is part of the theme issue 'Half a century of evolutionary games: a synthesis of theory, application and future directions'.

Effect of maternal age on primary and secondary sex ratios in the ectoparasitoid wasp Pachycrepoideus vindemmiae

Sex allocation is defined as the allocation of resources to produce male and female offspring during reproduction, and it is an important topic in evolutionary biology. As organisms with special haplo‐diploid sex determination, parasitoid wasps are particularly suited for the study of sex allocation. However, most studies focused on the secondary sex ratio (i.e., the eclosion sex ratio) because the oviposition ratio (the primary sex ratio) is difficult to study, especially in parasitoid species. The primary sex ratio may differ from the secondary sex ratio due to larval mortality and self‐superparasitism. The present study used microsatellites to explore the effects of female age on the primary and secondary sex ratio (male proportion) of the solitary ectoparasitoid Pachycrepoideus vindemmiae (Rondani) (Hymenoptera: Pteromalidae). The primary sex ratio showed a significant decreasing trend as the oviposition days increased, and the secondary sex ratio significantly increased. Self‐superparasitism, i.e., laying more than one egg in a host, was the cause of the variation in the secondary sex ratio in P. vindemmiae. When females practiced self‐superparasitism, they tended to lay female eggs. The application of microsatellites helped explore and improve the understanding of the primary sex ratio and self‐superparasitism in this ectoparasitoid species.

Males can adjust offspring sex ratio in an adaptive fashion through different mechanisms.

Sex allocation research has primarily focused on offspring sex-ratio adjustment by mothers. Yet, fathers also benefit from producing more of the sex with greater fitness returns. Here, we review the state-of-the art in the study of male-driven sex allocation and, counter to the current paradigm, we propose that males can adaptively influence offspring sex ratio through a wide variety of mechanisms. This includes differential production and motility of X- versus Y-bearing sperms in mammals, variation in seminal fluid composition in haplo-diploid invertebrates, and epigenetic mechanisms in some fish and lizards exhibiting environmental sex determination. Conflicts of interest between mothers and fathers over offspring sex ratios can emerge, although many more studies are needed in this area. While many studies of sex allocation have focused on adaptive explanations with little attention to mechanisms, and vice versa, the integration of these two topics is essential for understanding male-driven sex allocation.

Offspring sex-ratio and environmental conditions in a seabird with sex-specific rearing costs: a long-term experimental approach

Sex allocation studies among birds and mammals are notoriously inconsistent with theoretical predictions. One explanation is the difficulty of collecting data on costs and benefits of sex-ratio adjustments, which prevents the investigation of underlying assumptions. Some predictions may thus have been tested in species where they should not have been expected. Here, we focus on the “cost of reproduction hypothesis”, which states that parents with low investment capacity should avoid producing the most expensive sex to minimise the decrease in their residual reproductive value. In the black-legged kittiwake (Rissa tridactyla), sons are energetically more expensive than daughters. Using 10 years of data (1172 chicks from 790 broods) from a long-term feeding experiment, we predicted a stronger decrease in the probability of producing a son with deteriorating environmental conditions among Control than among supplementally Fed parents. To test this prediction, we used three proxies of environmental conditions and a recent sliding window approach. We found no support for our prediction. Hence, we investigated between-year sex-ratio variation in relation to feeding status to detect a response to an unmeasured environmental variable. There was no interaction between year and feeding status, nor any effect of feeding status itself. However, the probability of producing a male increased with time, which could be a response to an oceanic regime shift that occurred around our colony, but that our proxies failed to capture. Our study further highlights the difficulty of explaining sex-ratio variation in long-lived species with complex life-histories where multiple selective pressures can occur simultaneously.

Sex allocation and progress in the studies on offspringsex ratio of birds

Sex allocation has caught much attention because it is related to life strategies, individual fitness and population dynamics. Birds, a class of vertebrates with extremely high species diversity and abundance, are ideal subjects for the study of sex allocation. Several classic hypotheses have been proposed, such as evolutionary stable strategy and Trivers-Willard hypothesis. Offspring sex ratio is a direct observation of sex allocation, so the factors influencing offspring sex ratio are key to the understanding of sex allocation between males and females. Currently, the field focuses on the research of environmental, parental and offspring factors. However, up to date it is still an open question which factor determines the offspring sex ratio, and much work needs to be done before we know to what extent parents can regulate offspring sexes. In this review, we summarize the progress in the factors influencing the offspring sex ratio, presenting a spectrum of offspring sex ratio studies from the classic hypotheses to empirical studies.

Daphnia females adjust sex allocation in response to current sex ratio and density.

Cyclical parthenogenesis presents an interesting challenge for the study of sex allocation, as individuals' allocation decisions involve both the choice between sexual and asexual reproduction, and the choice between sons and daughters. Male production is therefore expected to depend on ecological and evolutionary drivers of overall investment in sex, and those influencing male reproductive value during sexual periods. We manipulated experimental populations, and made repeated observations of natural populations over their growing season, to disentangle effects of population density and the timing of sex from effects of adult sex ratio on sex allocation in cyclically parthenogenetic Daphnia magna. Male production increased with population density, the major ecological driver of sexual reproduction; however, this response was dampened when the population sex ratio was more male-biased. Thus, in line with sex ratio theory, we show that D.magna adjust offspring sex allocation in response to the current population sex ratio.

Maternal condition and previous reproduction interact to affect offspring sex in a wild mammal.

Trivers and Willard proposed that offspring sex ratio should vary with maternal condition when condition, meant as maternal capacity to care, has different fitness consequences for sons and daughters. In polygynous and dimorphic species, mothers in good condition should preferentially produce sons, whereas mothers in poor condition should produce more daughters. Despite its logical appeal, support for this hypothesis has been inconsistent. Sex-ratio variation may be influenced by additional factors, such as environmental conditions and previous reproduction, which are often ignored in empirical studies. We analysed 39 years of data on bighorn sheep (Ovis canadensis) that fit all the assumptions of the Trivers-Willard hypothesis. Production of sons increased with maternal condition only for mothers that weaned a son the previous year. This relationship likely reflects a mother's ability to bear the higher reproductive costs of sons. The interaction between maternal condition and previous weaning success on the probability of producing a son was independent of the positive effect of paternal reproductive success. Maternal and paternal effects accounted for similar proportions of the variance in offspring sex. Maternal reproductive history should be considered in addition to current condition in studies of sex allocation.

Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica).

Parents should differentially invest in sons or daughters depending on the sex-specific fitness returns from male and female offspring. In species with sexually selected heritable male characters, highly ornamented fathers should overproduce sons, which will be more sexually attractive than sons of less ornamented fathers. Because of genetic correlations between the sexes, females that express traits which are under selection in males should also overproduce sons. However, sex allocation strategies may consist in reaction norms leading to spatiotemporal variation in the association between offspring sex ratio (SR) and parental phenotype. We analysed offspring SR in barn swallows (Hirundo rustica) over 8 years in relation to two sexually dimorphic traits: tail length and melanin-based ventral plumage coloration. The proportion of sons increased with maternal plumage darkness and paternal tail length, consistently with sexual dimorphism in these traits. The size of the effect of these parental traits on SR was large compared to other studies of offspring SR in birds. Barn swallows thus manipulate offspring SR to overproduce 'sexy sons' and potentially to mitigate the costs of intralocus sexually antagonistic selection. Interannual variation in the relationships between offspring SR and parental traits was observed which may suggest phenotypic plasticity in sex allocation and provides a proximate explanation for inconsistent results of studies of sex allocation in relation to sexual ornamentation in birds.

Allocation to pollen competitive ability versus seed production inViola tricoloras an effect of plant size, soil nutrients and presence of a root competitor

In hermaphroditic plants, the effect of a social environment on sex allocation has not been studied to our knowledge, while in hermaphroditic animals such effects are known to be common. In recent years, studies on root competition beyond the effects of nutrients have shown that plants can respond to their conspecific root competitors (social environment), making it interesting to ask if these effects could also influence sex allocation in addition to more commonly studied factors, such as plant size or resources. In this study on hermaphroditicViola tricolor, we investigated how plant size, soil nutrients and presence of a root competitor influenced allocation to pollen competitive ability versus seed production, i.e. male and female reproductive functions. We allowed plants to grow in pairs with partly intermingled or separate roots in the same amount of soil. In additional treatments with intermingled roots (as part of the same experiment) one of the two competitors was given combinations of nitrogen (N), phosphorous (P) and micro nutrients. We found that pollen performance but not seed production increased when plants were in contact in the soil. Additionally, pollen performance was negatively correlated to plant size across fertilisation treatments. For seed production, the opposite relation to plant size was seen, indicating that large, fertilized plants invest relatively more in the female function. In conclusion, in violets, sex allocation appears to be size‐dependent and influenced by both the presence of a root competitor and by nutrients. These results suggest that social environment can influence sex allocation in plants as well as in animals, indicating that such effects are important to consider in sex allocation studies across taxa.

Emerging sex allocation research in mammals: marsupials and the pouch advantage

ABSTRACT Adaptive adjustments in offspring sex ratios in mammals have long been reported, but the conditions and mechanisms that prompt shifts in the proportion of sons and daughters born are still unclear. Empirical evidence indicates that offspring sex in mammals can be related to a diversity of environmental and maternal traits. However, the underlying assumptions regarding offspring and maternal fitness are rarely tested. Physiological mechanisms of maternal selection of offspring sex may occur at many stages during the prolonged maternal investment stage, and a pluralistic approach to studying mechanisms might prove fruitful. This review highlights the apparent frequency, in marsupial mammals, of sex ratio bias, which has largely been recorded as conforming to one of a few hypotheses. Marsupials are ideally suited to experiments involving cross‐fostering of offspring, which can allow rigorous tests of the fitness consequences of rearing one sex vs. the other. The reproductive biology of marsupials lends the group to detailed studies of the timing and physiological correlates of offspring sex biases. Many components of metatherian biology may prove advantageous in experimental studies of sex allocation in mammals, and together may provide a prosperous avenue for examining adaptive and mechanistic hypotheses in mammalian sex allocation.

PATERNAL CONDITION DRIVES PROGENY SEX-RATIO BIAS IN A LIZARD THAT LACKS PARENTAL CARE

Sex-allocation theory predicts that females in good condition should preferentially produce offspring of the sex that benefits the most from an increase in maternal investment. However, it is generally assumed that the condition of the sire has little effect on progeny sex ratio, particularly in species that lack parental care. We used a controlled breeding experiment and molecular paternity analyses to examine the effects of both maternal and paternal condition on progeny sex ratio and progeny fitness in the brown anole (Anolis sagrei), a polygynous lizard that lacks parental care. Contrary to the predictions of sex-allocation theory, we found no relationship between maternal condition and progeny sex ratio. By contrast, progeny sex ratio shifted dramatically from female-biased to male-biased as paternal condition increased. This pattern was driven entirely by an increase in the production of sons as paternal condition improved. Despite strong natural selection favoring large size and high condition in both sons and daughters, we found no evidence that progeny survival was related to paternal condition. Our results emphasize the importance of considering the paternal phenotype in studies of sex allocation and highlight the need for further research into the pathways that link paternal condition to progeny fitness.

Extremely female-biased primary sex ratio and precisely constant male production in a parasitoid wasp Melittobia

The study of sex allocation is one of the most productive areas in evolutionary biology, with considerable interplay between theoretical and empirical work. However, observed sex ratios are often measured after developmental periods and they may not reflect primary sex investment ratios, which is what theory predicts. We examined with the sex ratio behaviour of the parasitoid wasp Melittobia, in which males do not disperse from their natal patch. In contrast with the well-supported predictions of local mate competition (LMC) theory, the extremely female-biased sex ratio observed at emergence changes little in response to ovipositing female number. We examined (1) the primary sex ratio at oviposition and (2) the pattern of male production over time, to test whether the inconsistency with LMC theory can be explained by differential developmental mortality between the sexes. We found that the sex ratio at oviposition measured with a microsatellite DNA marker did not differ from the sex ratio at emergence, indicating that differential developmental mortality is absent or weak. We also found that males were constantly produced throughout the period of oviposition after a single male was produced initially.

Within-clutch egg size asymmetry covaries with embryo sex in the yellow-legged gull Larus michahellis

Non-random sex allocation may occur whenever the expected reproductive value of sons and daughters differs, as is the case when the sexes differ in susceptibility to environmental conditions or maternal effects (e.g. egg size and hatch order). Under such circumstances, covariation between egg and clutch characteristics and egg sex may be expected, and this covariation should vary with maternal state or ecological conditions. In this 2-year study (2007–2008), we examined sex allocation in relation to egg and clutch traits in the yellow-legged gull Larus michahellis, a species where male chicks are larger and more susceptible to harsh rearing conditions than female ones. In 2008, eggs were more likely male early in the season in two- but not three-egg clutches, and large eggs were more likely males late in the season. No egg/clutch traits predicted egg sex in 2007. Within-clutch egg mass asymmetry (the difference in egg mass between the first- and last-laid eggs) predicted sex in both years. In 2007, clutches with smaller egg mass variation were more likely to contain males, while in 2008 this relationship held for the last-laid egg and was reversed for the preceding egg(s). Laying order and sex of the previous egg did not predict egg sex, providing no evidence of sex-specific oocyte clustering. Thus, the relationships between egg sex and egg/clutch traits differed among years, suggesting a phenotypically plastic response of females to extrinsic conditions, and involved within-clutch egg mass asymmetry, a trait likely reflecting variation in maternal quality and/or reproductive tactics, which has been largely neglected in previous studies of sex allocation.

ADAPTIVE PLASTICITY OF THE PENIS IN A SIMULTANEOUS HERMAPHRODITE

Acorn barnacles are important model organisms for the study of sex allocation. They are sessile, nonselfing hermaphrodites that copulate with penises that have been suggested to be phenotypically plastic. On wave-exposed shores, Semibalanus balanoides develop penises with relatively greater diameter whereas in wave-protected sites they are thinner. A reciprocal transplant experiment between wave-exposed and protected sites tested whether these exposure-specific morphologies have adaptive value. Mating success was compared over a range of distances to compare the ability of barnacles to reach mates. Barnacles that grew in the wave-protected site and mated in the wave-protected site fertilized more broods at increasing distances than those transplanted to the wave-exposed site. For barnacles that developed in the wave-exposed site, there was no difference in the ability to fertilize neighbors between sites of differing exposure. This study demonstrates the adaptive value of plasticity in penis morphology. The results suggest a trade-off between development of a penis adapted to wave exposure and the ability to fertilize distant mates. Barnacles in different physical environments are limited by different factors, which may limit numbers of potential mates, constrain optimal sex allocation strategies and alter reproductive behavior.

Evolutionary Biology: Parasite, Know Thyself

Studies of sex allocation provide some of the best evidence for Darwinian adaptation in nature. A new study of malaria parasites provides striking support for this cornerstone of evolutionary biology, with important implications for both evolutionary and medical biology.

Split sex ratios in the social Hymenoptera: a meta-analysis

The study of sex allocation in social Hymenoptera (ants, bees, and wasps) provides an excellent opportunity for testing kin-selection theory and studying conflict resolution. A queen–worker conflict over sex allocation is expected because workers are more related to sisters than to brothers, whereas queens are equally related to daughters and sons. If workers fully control sex allocation, split sex ratio theory predicts that colonies with relatively high or low relatedness asymmetry (the relatedness of workers to females divided by the relatedness of workers to males) should specialize in females or males, respectively. We performed a meta-analysis to assess the magnitude of adaptive sex allocation biasing by workers and degree of support for split sex ratio theory in the social Hymenoptera. Overall, variation in relatedness asymmetry (due to mate number or queen replacement) and variation in queen number (which also affects relatedness asymmetry in some conditions) explained 20.9% and 5% of the variance in sex allocation among colonies, respectively. These results show that workers often bias colony sex allocation in their favor as predicted by split sex ratio theory, even if their control is incomplete and a large part of the variation among colonies has other causes. The explanatory power of split sex ratio theory was close to that of local mate competition and local resource competition in the few species of social Hymenoptera where these factors apply. Hence, three of the most successful theories explaining quantitative variation in sex allocation are based on kin selection.

Sex ratio schedules in a dynamic game: the effect of competitive asymmetry by male emergence order

Studies of sex allocation have provided some of the most successful tests of theory in behavioral and evolutionary ecology. For instance, local mate competition (LMC) theory has explained variation in sex allocation across numerous species. However, some patterns of sex ratio variation remain unexplained by existing theory. Most existing models have ignored variation in male competitive ability and assumed all males have equal opportunities to mate within a patch. However, in some species experiencing LMC, males often fight fiercely for mates, such that male mating success varies with male fighting ability. Here, we examine the effect of competitive ability on optimal sex allocation schedules using a dynamic programming approach. This model assumes an asymmetric competitive ability derived from different mortalities according to the timing of male emergence. If the mortality of newly emerging males is larger than that of already emerged males, our model predicts a more female-biased sex ratio than expected under traditional LMC models. In addition, females are predicted to produce new males constantly at a low rate over the offspring emergence period. We show that our model successfully predicts the sex ratios produced by females of the parasitoid wasp Melittobia, a genus renowned for its vigorously fighting males and lower than expected sex ratios. Key words: dynamic game model, lethal male combat, local mate competition, Melittobia, parasitoid wasps, sex allocation. [Behav Ecol]

Disentangling the complexities of vertebrate sex allocation: a role for squamate reptiles?

Sex allocation is an important field in evolutionary biology, both historically and currently. However, while sex allocation theory has successfully predicted sex ratio bias in some taxa, most notably parasitic wasps, vertebrates are notorious for their poor fit to theoretical models. We argue that this arises from the use of very complex model systems to test relatively simple theoretical models. We further argue that squamate reptiles lizards and snakes have unduly been neglected in sex allocation studies and in fact may conform more readily to the underlying assumptions of existing theoretical models than many other vertebrates. We provide a five-point argument in favor of the use of squamates as model systems in sex allocation based on their diversity in sex determining mechanisms, life history biology, and ease of experimental manipulations.

Disentangling the complexities of vertebrate sex allocation: a role for squamate reptiles?

Sex allocation is an important field in evolutionary biology, both historically and currently. However, while sex allocation theory has successfully predicted sex ratio bias in some taxa, most notably parasitic wasps, vertebrates are notorious for their poor fit to theoretical models. We argue that this arises from the use of very complex model systems to test relatively simple theoretical models. We further argue that squamate reptiles – lizards and snakes – have unduly been neglected in sex allocation studies and in fact may conform more readily to the underlying assumptions of existing theoretical models than many other vertebrates. We provide a five‐point argument in favor of the use of squamates as model systems in sex allocation based on their diversity in sex determining mechanisms, life history biology, and ease of experimental manipulations.