Biased Sex Ratios Research Articles

Sex Ratio Bias Leads to the Evolution of Sex Role Reversal in Honey Locust Beetles

The reversal of conventional sex roles was enigmatic to Darwin, who suggested that it may evolve when sex ratios are female biased [1]. Here we present direct evidence confirming Darwin's hypothesis. We investigated mating system evolution in a sex-role-reversed beetle (Megabruchidius dorsalis) using experimental evolution under manipulated sex ratios and food regimes. In female-biased populations, where reproductive competition among females was intensified, females evolved to be more attractive and the sex roles became more reversed. Interestingly, female-specific mating behavior evolved more rapidly than male-specific mating behavior. We show that sexual selection due to reproductive competition can be strong in females and can target much the same traits as in males of species with conventional mating systems. Our study highlights two central points: the role of ecology in directing sexual selection and the role that females play in mating system evolution.

Thermosensitive period of sex determination in the coral-reef damselfish Acanthochromis polyacanthus and the implications of projected ocean warming

Higher temperatures associated with climate change have the potential to significantly alter the population sex ratio of species with temperature-dependent sex determination. Whether or not elevated temperature affects sex determination depends on both the absolute temperature experienced and the stage of development at which the thermal conditions occur. We explored the importance of exposure timing during early development in the coral reef fish, Acanthochromis polyacanthus, by increasing water temperature 1.5 or 3 °C above the summer average (28.5 °C) at different stages of development. We also measured the effect of treatment temperature on fish size and condition, in order to gauge how the thermal threshold for sex-ratio bias may compare with other commonly considered physiological metrics. Increasing grow-out temperature from 28.5 to 30 °C had no effect on the sex ratio of offspring, whereas an increase to 31.5 °C (+3 °C) produced a strong male bias (average ~90%). The thermosensitive period for this species lasted between 25 and 60 d post hatching, with the bias in sex ratio greater the earlier that fish experienced warm conditions. Temperatures high enough to bias the sex ratio are likely to be seen first during late summer (January and February) and would affect clutches produced late in the breeding season. There was no change to fish condition in response to temperature; however, the two higher temperature treatments produced significantly smaller fish at sampling. Clutches produced early in the season could buffer the population from a skewed sex ratio, as their development will remain below the thermal threshold; however, continued ocean warming could mean that clutches produced earlier in the breeding season would also be affected in the longer term. A skewed sex ratio could be detrimental to population viability by reducing the number of females in the breeding population.

Evolutionary implications for the determination of gametocyte sex ratios under fecundity variation for the malaria parasite

We investigate sex ratio determination strategies for the Malaria parasite based on putative changes in its male fecundity over the lifetime of an infection, and how such strategies might have evolved. We model fitness using the incomplete fertilization limit developed in Teboh-Ewungkem and Yuster (2010). We divide the infection lifetime of a strain into two periods, assume each human is infected by two different strains, and assume that there are two different strategies present among the many strains in the general malaria parasite population. A unique parameter dependent ESS exists for all parameter values in both of our main models, with many such strategies unbeatable. These strategies produce both male and female biased population sex ratios with female bias predominating over most of the parameter space. The first model (SKM) suggests that strains without the ability to detect characteristics of other strains present could still have evolved strategies to vary sex ratio over their lifetimes, and the second model (DKM) suggests strains with detection abilities might have evolved after that. Our analysis suggests that once the ability to detect the population sizes and fecundities of other strains has developed, detection of their sex ratio choices confers no additional selective advantage in that a DKM ESS is still an ESS among sex ratio detecting strategies. The sex ratio choices for each DKM ESS are given by the equilibrium values of the parameter equivalent sex ratio detecting strategy described in Teboh-Ewungkem and Wang (2012), in the case where two strains employing that strategy encounter each other.

Alternative Growth and Defensive Strategies Reveal Potential and Gender Specific Trade-Offs in Dioecious Plants Salix paraplesia to Nutrient Availability.

Population sex ratios of many dioecious plants in nature are biased. This may be attributed to sexually different resource demands and adaptive capacity. In male-biasedPopulus, males often display stronger physiological adaptation than females. Interestingly, Populus and Salix, belonging to Salicaceae, display an opposite biased sex ratio, especially in nutrient-poor environmental conditions. Do female willows have a greater tolerance to nutrient deficiency than males? In this study, we investigated the growth and defensive strategies of Salix paraplesia cuttings, which were grown with high and low soil fertility for about 140 days over one growing season. Results suggest that different strategies for biomass allocation may result in sexually different defense capacities and trade-offs between growth and defense. Females are likely to adopt radical strategies, overdrawing on available resources to satisfy both growth and defense, which seems to be more like a gamble compared with males. It is also suggested that females may have an extra mechanism to compensate for the investment in growth under nutrient-poor conditions. In summary, the results may help focus restoration efforts on sex selection such that a moderate increase in female willow quantity could increase the resistance and resilience of willow populations to early sporadic desertification.

More daughters in a less favourable world: Breeding in intensively-managed orchards affects tertiary sex-ratio in the great tit

Offspring sex-ratio is a key life-history trait that shows considerable variation among many bird species. Habitat quality is one of the numerous environmental factors acting on bias in sex-ratios in passerines. For the great tit Parus major, southern French apple orchards constitute both feeding and breeding habitats of considerably varying quality depending on the annual amount of chemical pesticides used for pest control, which have both direct (toxicity) and indirect (lower prey availability) effects on bird populations. In a two-year study, we specifically assessed the effect of three pest management strategies involving high (conventional), moderate (IPM) and no (organic) chemical pesticide inputs on fledgling sex-ratio using molecular sexing techniques. We found that great tit populations had significant variations in fledgling sex-ratio across our range of habitat quality, with conventional apple orchards producing a more biased sex-ratio towards daughters than IPM and organic orchards. Estimates of maternal traits (female body condition, first egg-laying date, clutch size and hatching rate) were also analysed but they were not significant predictors of brood sex-ratio. This study supports the sensitivity of bird tertiary sex-ratio to habitat quality. It also suggests that highly pesticide-treated agro-ecosystems may be poorer habitats for temperate insectivorous bird species. We provide further evidence that reducing chemical pressure might mitigate anthropogenic impacts on bird life-histories and population dynamics.

Methyltestosterone alters sex determination in the American alligator (Alligator mississippiensis)

Effects of xenobiotics can be organizational, permanently affecting anatomy during embryonic development, and/or activational, influencing transitory actions during adulthood. The organizational influence of endocrine-disrupting contaminants (EDC’s) produces a wide variety of reproductive abnormalities among vertebrates that exhibit temperature-dependent sex determination (TSD). Typically, such influences result in subsequent activational malfunction, some of which are beneficial in aquaculture. For example, 17-αmethyltestosterone (MT), a synthetic androgen, is utilized in tilapia farming to bias sex ratio towards males because they are more profitable. A heavily male-biased hatchling sex ratio is reported from a crocodile population near one such tilapia operation in Guanacaste, Costa Rica. In this study we test the effects of MT on sexual differentiation in American alligators, which we used as a surrogate for all crocodilians. Experimentally, alligators were exposed to MT in ovo at standard ecotoxicological concentrations. Sexual differentiation was determined by examination of primary and secondary sex organs post hatching. We find that MT is capable of producing male embryos at temperatures known to produce females and demonstrate a dose-dependent gradient of masculinization. Embryonic exposure to MT results in hermaphroditic primary sex organs, delayed renal development and masculinization of the clitero-penis (CTP).

Causes and consequences of spatial variation in sex ratios in a declining bird species.

Summary Male‐biased sex ratios occur in many bird species, particularly in those with small or declining populations, but the causes of these skews and their consequences for local population demography are rarely known. Within‐species variation in sex ratios can help to identify the demographic and behavioural processes associated with such biases.Small populations may be more likely to have skewed sex ratios if sex differences in survival, recruitment or dispersal vary with local abundance. Analyses of species with highly variable local abundances can help to identify these mechanisms and the implications for spatial variation in demography. Many migratory bird species are currently undergoing rapid and severe declines in abundance in parts of their breeding ranges and thus have sufficient spatial variation in abundance to explore the extent of sex ratio biases, their causes and implications.Using national‐scale bird ringing data for one such species (willow warbler, Phylloscopus trochilus), we show that sex ratios vary greatly across Britain and that male‐biased sites are more frequent in areas of low abundance, which are now widespread across much of south and east England. These sex ratio biases are sufficient to impact local productivity, as the relative number of juveniles caught at survey sites declines significantly with increasing sex ratio skew.Sex differences in survival could influence this sex ratio variation, but we find little evidence for sex differences in survival increasing with sex ratio skew. In addition, sex ratios have become male‐biased over the last two decades, but there are no such trends in adult survival rates for males or females. This suggests that lower female recruitment into low abundance sites is contributing to these skews.These findings suggest that male‐biased sex ratios in small and declining populations can arise through local‐scale sex differences in survival and dispersal, with females recruiting disproportionately into larger populations. Given the high level of spatial variation in population declines and abundance of many migratory bird species across Europe at present, male‐biased small populations may be increasingly common. As singing males are the primary records used in surveys of these species, and as unpaired males often sing throughout the breeding season, local sex ratio biases could also be masking the true extent of these population declines.

Historical background of the population biology of the swimming crab Arenaeus cribrarius (Crustacea: Portunidae) in the Ubatuba coast, southeast Brazil

This study presents results obtained 25 years ago on the population structure, sex ratio, and handedness of Arenaeus cribrarius in Ubatuba, North coast of São Paulo State, Brazil. Sampling studies were conducted during two different periods (from November 1988 to October 1989, and from May 1991 to April 1993), one of them performed for pooled data, and other exclusively for Fortaleza Bay (monthly samples from November 1988 to October 1989). Males were larger (CW, average ± SD: 73.38 ± 15.78 mm) than females (68.45 ± 12.20 mm). The size between juvenile and adult stages has an overlap, for males (40-70mm CW) e fêmeas (45-75 mm CW). A prevalence of females was registered for pooled data (1:1.42; P < 0.01), but it was not recorded in Fortaleza Bay (1:1.25; P > 0.05). The sex ratio was close to 1:1 in the smaller size classes, with females dominating in the intermediate classes, and males in larger ones. In Fortaleza Bay, a female biased sex ratio was only noted in transect I (1:3.88; P < 0.05) and in the autumn (1:1.67; P < 0.05), with 73% of the specimens measured were right-handed.

No evidence for female discrimination against male house mice carrying a selfish genetic element.

Meiotic drivers distort transmission to the next generation in their favor, with detrimental effects on the fitness of their homologues and the rest of the genome. Male carriers of meiotic drivers commonly inflict costs on their mates through genetic incompatibility, reduced fecundity, or biased brood sex ratios. Given these costs, evidence for female discrimination against male carriers is surprisingly rare. One of few examples is the t haplotype in house mice, a meiotic driver that shows strong transmission distortion in males and is typically homozygote lethal. As a consequence, mating between 2 t heterozygous (+/t) mice leads to high embryo mortality. Previous experiments showing that +/t females avoid this incompatibility cost by preferring +/+ versus +/t males have inferred preference based on olfactory cues or brief social interactions. Evidence from mating contexts in laboratory settings and semi-natural populations has been inconclusive. Here, we investigated female choice from a large number of no-choice mating trials. We found no evidence for discrimination against +/t males based on mating, remating, and copulatory behavior. Further, we found no evidence for avoidance of incompatibility through selective interactions between gametes. The likelihood of mating showed significant effects of female weight and genotype, suggesting that our test paradigm enabled females to exhibit mate choice. We discuss the strengths and limitations of our approach. By explicitly considering selection at both the individual and gene level, we argue why precopulatory female discrimination by +/t females may be less evolutionarily stable than discrimination by all females based on postcopulatory mechanisms.

Sex-different response in growth traits to resource heterogeneity explains male-biased sex ratio

In dioecious plants, differences in growth traits between sexes in a response to micro-environmental heterogeneity may affect sex ratio bias and spatial distributions. Here, we examined sex ratios, stem growth traits and spatial distribution patterns in the dioecious clonal shrub Aucuba japonica var. borealis, in stands with varying light intensities. We found that male stems were significantly more decumbent (lower height/length ratio) but female stems were upright (higher height/length ratio). Moreover, we found sex-different response in stem density (no. of stems per unit area) along a light intensity gradient; in males the stem density increased with increases in canopy openness, but not in females. The higher sensitivity of males in increasing stem density to light intensity correlated with male-biased sex ratio; fine-scale sex ratio was strongly male-biased as canopy openness increased. There were also differences between sexes in spatial distributions of stems. Spatial segregation of sexes and male patches occupying larger areas than female patches might result from vigorous growth of males under well-lit environments. In summary, females and males showed different growth responses to environmental variation, and this seemed to be one of possible causes for the sex-differential spatial distributions and locally biased sex ratios.

Superparasitism Drives Heritable Symbiont Epidemiology and Host Sex Ratio in a Wasp.

Heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts. Whilst our current understanding of the dynamics of these symbionts is typically cast within a framework of vertical transmission only, horizontal transmission has been observed in a number of cases. For instance, several symbionts can transmit horizontally when their parasitoid hosts share oviposition patches with uninfected conspecifics, a phenomenon called superparasitism. Despite this, horizontal transmission, and the host contact structures that facilitates it, have not been considered in heritable symbiont epidemiology. Here, we tested for the importance of host contact, and resulting horizontal transmission, for the epidemiology of a male-killing heritable symbiont (Arsenophonus nasoniae) in parasitoid wasp hosts. We observed that host contact through superparasitism is necessary for this symbiont’s spread in populations of its primary host Nasonia vitripennis, such that when superparasitism rates are high, A. nasoniae almost reaches fixation, causes highly female biased population sex ratios and consequently causes local host extinction. We further tested if natural interspecific variation in superparasitism behaviours predicted symbiont dynamics among parasitoid species. We found that A. nasoniae was maintained in laboratory populations of a closely related set of Nasonia species, but declined in other, more distantly related pteromalid hosts. The natural proclivity of a species to superparasitise was the primary factor determining symbiont persistence. Our results thus indicate that host contact behaviour is a key factor for heritable microbe dynamics when horizontal transmission is possible, and that ‘reproductive parasite’ phenotypes, such as male-killing, may be of secondary importance in the dynamics of such symbiont infections.

Male Reproductive Morphology Across Latitudinal Clines and Under Long-Term Female Sex-Ratio Bias.

SynopsisRecent work in evolutionary ecology has capitalized on the species-specific, rapidly evolving nature of male reproductive traits, but it is unclear how the strength of sexual selection mechanisms, such as female choice and intersexual conflict, changes with ecological factors-shifts in latitude, elevation, and sex-ratio. Marginal habitats, such as those found at high elevation or latitude, might be expected to exert energetic hardships on males such that they do not invest heavily in reproductive structures. Conversely, males in these habitats may adapt to limited breeding opportunities, evolving morphologies with efficacy in antagonistic mating. Sex-ratio biases elicited by facultative parthenogenesis may also signal increasing selective pressure for reproductive organs that improve coercion ability, as males must capitalize on mating opportunities when females have alternate reproductive options. We studied the reproductive organs of males of five species of a group of polygynandrous Japanese harvestmen, collected from populations that varied in their elevation, latitude, and observed male: female ratio. Morphological data were analyzed with modern comparative methods, using a phylogenomic framework built with molecular data from double-digest restriction associated DNA sequencing. Although no features with hypothesized utility in coercive mating significantly covaried with elevational change, penis length was found to decrease with increasing latitude, supporting the existence of physiological constraints in marginal habitats. We also found males of parthenogenetic species, with primarily female-biased populations, had potentially greater precopulatory clasping ability, as compared to males of non-parthenogenetic species with more even sex-ratios. Ultimately, our findings suggest long-term sex-ratio biases are one of many factors with the potential to influence evolution of primary and secondary reproductive morphology.

The ghost sex-life of the paedogenetic beetle Micromalthus debilis.

Genetic and sexual systems can be evolutionarily dynamic within and among clades. However, identifying the processes responsible for switches between, for instance, sexual and asexual reproduction, or cyclic and non-cyclic life histories remains challenging. When animals evolve parthenogenetic reproduction, information about the sexual mating system becomes lost. Here we report an extraordinary case where we have been able to resurrect sexual adults in a species of beetle that reproduces by parthenogenetic paedogenesis, without the production of adults. Via heat treatment, we were able to artificially induce adult beetles of Micromalthus debilis in order to describe its pre-paedogenetic mating system. Adults showed a highly female biased sex ratio, out-breeding behaviour, and sex-role reversal. Paedogenetic larvae of Micromalthus are infected with the endosymbiotic bacteria Rickettsia and Wolbachia. Clear signs of vestigialization in adults are concurrent with the loss of adults. Our data suggest an ancient female sex ratio bias that predates the loss of adults, perhaps associated with endosymbionts. We propose a model for the transition from a haplodiploid cyclical parthenogenetic life history to parthenogenetic paedogenesis. Paedogenetic development induces a new mechanism of sex ratio bias in midges, wasps and beetles.

Geographic Variation in Sex Determination Patterns in the River TurtlePodocnemis lewyana: Implications for Global Warming

Abstract Species with temperature-dependent sex determination (TSD) are more vulnerable to climate change than species with genetically based sex determination because an increase in average environmental temperature could lead to biased offspring sex ratios. In TSD species, the relationship between sex ratio and constant incubation temperature is characterized by two parameters: the pivotal temperature (Tpiv) and the transitional range of temperature (TRT) that produces both sexes. Species with variation in either of these parameters should have more potential to adapt to new climatic conditions, therefore putting them at lower risk to global warming. In this study, we incubated eggs of the turtle Podocnemis lewyana (Testudines: Podocnemididae) from two geographically isolated populations (Magdalena and Sinu rivers) under controlled microclimatic conditions to corroborate the TSD pattern previously reported for this species and to estimate the degree of inter- and intrapopulation variation in Tpiv and TR...

Sex allocation and secondary sex ratio in Cuban boa (Chilabothrus angulifer): mother’s body size affects the ratio between sons and daughters

Secondary sex ratios of animals with genetically determined sex may considerably deviate from equality. These deviations may be attributed to several proximate and ultimate factors. Sex ratio theory explains some of them as strategic decisions of mothers improving their fitness by selective investment in sons or daughters, e.g. local resource competition hypothesis (LRC) suggests that philopatric females tend to produce litters with male-biased sex ratios to avoid future competition with their daughters. Until now, only little attention has been paid to examine predictions of sex ratio theory in snakes possessing genetic sex determination and exhibiting large variance in allocation of maternal investment. Cuban boa is an endemic viviparous snake producing large-bodied newborns (∼200g). Extremely high maternal investment in each offspring increases importance of sex allocation. In a captive colony, we collected breeding records of 42 mothers, 62 litters and 306 newborns and examined secondary sex ratios (SR) and sexual size dimorphism (SSD) of newborns. None of the examined morphometric traits of neonates appeared sexually dimorphic. The sex ratio was slightly male biased (174 males versus 132 females) and litter sex ratio significantly decreased with female snout-vent length. We interpret this relationship as an additional support for LRC as competition between mothers and daughters increases with similarity of body sizes between competing snakes.

To Cull or Not To Cull? Considerations for Studies of Endocrine-Disrupting Chemicals

The power of animal models is derived from the ability to control experimental variables so that observed effects may be unequivocally attributed to the factor that was changed. One variable that is difficult to control in animal experiments is the number and composition of offspring in a litter. To account for this variability, artificial equalization of the number of offspring in a litter (culling) is often used. The rationale for culling, however, has always been controversial. The Developmental Origins of Health and Disease concept provides a new context to evaluate the pros and cons of culling in laboratory animal studies, especially in the context of endocrine-disrupting chemicals. Emerging evidence indicates that culling, especially of large litters, can drastically change the feeding status of a pup, which can result in compensatory growth with long-term consequences for the animal, including increased risk of cardio-metabolic diseases. Similarly, culling of litters to intentionally bias sex ratios can alter the animal's behavior and physiology, with effects observed on a wide range of outcomes. Thus, in an attempt to control for variability in developmental rates, culling introduces an uncontrolled or confounding variable, which itself may affect a broad spectrum of health-related consequences. Variabilities in culling protocols could be responsible for differences in responses to endocrine-disrupting chemicals reported across studies. Because litter sex composition and size are vectors that can influence both prenatal and postnatal growth, they are essential considerations for the interpretation of results from laboratory animal studies.

Condition and reproductive investment in the western mosquitofish (Gambusia affinis): little evidence for condition-dependent sex-biased investment

In sexually reproducing species, resources may theoretically be distributed with bias to the production of male or female offspring in response to the condition of the mother, commonly recognized as sex allocation. Using a recently characterized sex-specific molecular marker, we tested for maternal sex allocation (i.e. maternal primary sex ratio bias and sex-specific offspring investment) in captive laboratory-bred western mosquitofish (Gambusia affinis) at early stages of offspring development. We found no statistical evidence to support sex allocation in G. affinis, based on maternal condition. In addition, we found little evidence for correlations between maternal condition and investment in the condition (mass) of individual offspring (of one sex or the other), although we did find that larger mothers tended to have higher fecundity.

PARTIALLY CONSTRAINED SEX ALLOCATION AND THE INDIRECT EFFECTS OF ASSISTED REPRODUCTIVE TECHNOLOGIES ON THE HUMAN SEX RATIO.

Infertility affects around 15% of human couples and in many countries approximately 1-4% of babies are born following Assisted Reproductive Technologies (ART). Several ART techniques are used and these differentially affect the sex ratio of offspring successfully produced. These direct effects on sex ratio also have the potential to influence, indirectly, the sex ratios of offspring born to untreated couples. This is of concern because human sex ratio bias may adversely affect public health. Here the extent of indirect effects of ART that could operate, via Fisherian frequency-dependent natural selection, on the progeny sex ratio of unassisted members of a population is heuristically modelled. Given the degrees to which ART techniques bias sex ratios directly, it is predicted that well over 20% of couples would have to reproduce via ART for there to be any discernible effect on the sex ratios produced, in response, by the remainder of the population. This value is greater than the estimated prevalence of infertility problems among human couples. It is concluded that providing ART to couples with fertility problems does not currently generate significant ethical issues or public health concern in terms of indirect effects on the offspring sex ratios of untreated couples.

Population growth of three mirid predatory bugs feeding on eggs and larvae of Tuta absoluta on tomato

Tuta absoluta Meyrick quickly developed into a significant pest of tomatoes worldwide. While the mirid bugs Macrolophus basicornis (Stal), Engytatus varians (Distant) and Campyloneuropsis infumatus (Carvalho) prey on this tomato borer, their biology have not been well characterized. Using a mixture of T. absoluta eggs and larvae as food on tomato, mirid life histories were studied. Nymphs and adults successfully used T. absoluta as prey, although significant differences in biology of the species were observed. Campyloneuropsis infumatus and M. basicornis were quickest and slowest to become adult at 16 and 19 days, respectively. Nymphal survival was high and varied from 70 to 75 %. Female biased sex ratios were observed for C. infumatus (0.80) and M. basicornis (0.71), but not for E. varians (0.56). Intrinsic rates of increase for C. infumatus, E. varians and M. basicornis were 0.11, 0.10 and 0.11 respectively. Our results indicate rapid development and population increase of these three mirids, making them interesting candidates for biological control of T. absoluta on tomato.

Better-surviving barn swallow mothers produce more and better-surviving sons.

Sex allocation theory predicts that parents are selected to bias their progeny sex ratio (SR) toward the sex that will benefit the most from parental quality. Because parental quality may differentially affect survival of sons and daughters, a pivotal test of the adaptive value of SR adjustment is whether parents overproduce offspring of the sex that accrues larger fitness advantages from high parental quality. However, this crucial test of the long-term fitness consequences of sex allocation decisions has seldom been performed. In this study of the barn swallow (Hirundo rustica), we showed a positive correlation between the proportion of sons and maternal annual survival. We then experimentally demonstrated that this association did not depend on the differential costs of rearing offspring of either sex. Finally, we showed that maternal lifespan positively predicted lifespan of sons but not of daughters. Because in barn swallows lifespan is a strong determinant of lifetime reproductive success, the results suggest that mothers overproduce offspring of the sex that benefits the most from maternal quality. Hence, irrespective of mechanisms causing the SR bias and mother-son covariation in lifespan, we provide strong evidence that sex allocation decisions of mothers can highly impact on their lifetime fitness.