Population structure leads to male‐biased population sex ratios under environmental sex determination

Spatial structure has been shown to favor female‐biased sex allocation, but current theory fails to explain male biases seen in many taxa, particularly those with environmental sex determination (ESD). We present a theory and accompanying individual‐based simulation model that demonstrates how population structure leads to male‐biased population sex ratios under ESD. Our simulations agree with earlier work showing that the high productivity of female‐producing habitats creates a net influx of sex‐determining alleles into male‐producing habitats, causing larger sex ratio biases, and lower productivity in male‐producing environments (Harts et al. 2014). In contrast to previous findings, we show that male‐biasing habitats disproportionately impact the global sex ratio, resulting in stable male‐biased population sex ratios under ESD. The failure to detect a male bias in earlier work can be attributed to small subpopulation sizes leading to local mate competition, a condition unlikely to be met in most ESD systems. Simulations revealed that consistent male biases are expected over a wide range of population structures, environmental conditions, and genetic architectures of sex determination, with male excesses as large as 30 percent under some conditions. Given the ubiquity of genetic structure in natural populations, we predict that modest, enduring male biased allocation should be common in ESD species, a pattern consistent with reviews of ESD sex ratios.     

Weakened purifying selection leads to elevated mutation load under environmental sex determination

In many gonochoristic taxa, sex is influenced by developmental environment, a system that can lead to temporal fluctuations in offspring sex ratio. Demographic models suggest that only short‐lived species with environmental sex determination (ESD) are negatively impacted by sex‐ratio fluctuations, yet these models fail to account for the potential mutation load associated with reductions in genetically effective population sizes. In this study, we developed a series of individual‐based simulation models that explore the fixation rates of mildly deleterious alleles under different sex‐determining systems and examine the impacts of variation in lifespan and offspring sex ratio. Populations with ESD exhibited increases in fixation rates in both short‐ and long‐lived populations, but substantial increases were limited to populations characterized by a combination of high sex‐ratio variation and short lifespan. Fixation rates were negatively associated with effective population size, indicating that purifying selection operates less efficiently under ESD relative to genotypic sex determination. Reductions in effective population size could be attributed to both intragenerational forces (unequal sex ratio) and intergenerational forces (variable census population sizes). Levels of temporal sex‐ratio variation calculated from wild populations of ESD species were capable of yielding large increases in fixation rates, although this relationship was strongly mediated by lifespan. Our results may help to explain the limited phylogenetic distribution of ESD in short‐lived taxa.     

Hidden suppression of sex ratio distortion suggests Red queen dynamics between Wolbachia and its dwarf spider host

Genetic conflict theory predicts strong selection for host nuclear factors suppressing endosymbiont effects on reproduction; however, evidence of these suppressors is currently scarce. This can either be caused by a low suppressor evolution rate, or if suppressors originate frequently, by rapid spread and concurrent masking of their activity by silencing the endosymbiont effect. To explore this, we use two populations of a dwarf spider with a similar female bias, caused by a Wolbachia infection. Using inter‐ and intrapopulation crosses, we determine that one of these populations demonstrates a higher suppressing capability towards Wolbachia despite having a similar population sex ratio. This suggests that spider and endosymbiont are locked in so‐called red queen dynamics where, despite continuous coevolution, average fitness remains the same, hence hiding the presence of the suppressor. Finding different suppressor activity in populations that even lack phenotypic differentiation (i.e. similar sex ratio) further supports the hypothesis that suppressors originate often, but are often hidden by their own mode of action by countering endosymbiont effects.     

Genetic conflict and changes in heterogametic mechanisms of sex determination

The consequences of cytoplasmic sex‐ratio distortion and host repression for the evolution of host sex‐determining mechanisms are examined. Analytical models and simulations are developed to investigate whether the interplay between sex‐ratio distorters and host masculinizers or resistance genes can cause heterogamety switching (changes between male and female heterogamety). Switches from female heterogamety to a system analogous to male heterogamety can occur when selection favours the spread of autosomal masculinizers. However, the evolutionary outcome depends on the type of repressor and costs associated with repression, and also on aspects of population structure. Under most conditions, systems evolved to a polymorphic sex‐determining state although many systems were characterized by numerical dominance of male heterogamety.     

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.     

Does polyandry control population sex ratio via regulation of a selfish gene?

The extent of female multiple mating (polyandry) can strongly impact on the intensity of sexual selection, sexual conflict, and the evolution of cooperation and sociality. More subtly, polyandry may protect populations against intragenomic conflicts that result from the invasion of deleterious selfish genetic elements (SGEs). SGEs commonly impair sperm production, and so are likely to be unsuccessful in sperm competition, potentially reducing their transmission in polyandrous populations. Here, we test this prediction in nature. We demonstrate a heritable latitudinal cline in the degree of polyandry in the fruitfly Drosophila pseudoobscura across the USA, with northern population females remating more frequently in both the field and the laboratory. High remating was associated with low frequency of a sex-ratio-distorting meiotic driver in natural populations. In the laboratory, polyandry directly controls the frequency of the driver by undermining its transmission. Hence we suggest that the cline in polyandry represents an important contributor to the cline in sex ratio in nature. Furthermore, as the meiotic driver causes sex ratio bias, variation in polyandry may ultimately determine population sex ratio across the USA, a dramatic impact of female mating decisions. As SGEs are ubiquitous it is likely that the reduction of intragenomic conflict by polyandry is widespread.     

Evolutionary consequences of cytoplasmic sex ratio distorters

Summary Computer simulations of diploid genetic models were used to examine the consequences of the spread of a cytoplasmic sex ratio distorter on the frequencies of nuclear sex-determination alleles and the spread of nuclear resistance alleles in female biased populations. The cytoplsmic elements considered here override the expression of the nuclear sex-determination genes, turning genetic males into females. When homozygous male genotypes are viable, a cytoplasmic sex ratio historter spreads in a population if the proportion of daughters produced by infected females exceeds the proportion of daughters produced by uninfected females. The equilibrium frequency of male phenotypes is the proportion of uninfected progeny produced by infected females. When homozygous male genotypes are lethal, the conditions for the spread of the cytoplasmic element are more stringent. The spread of a cytoplasmic sex ratio distorter causes an increase in the frequency of nuclear male sex-determination alleles as a result of the unusual combinations of genotypes which mate in infected populations. Eventually, a cytoplasmic element may replace the nuclear gene as the sex-determination mechanism. This occurs without selection. Nuclear genes conferring resistance to cytoplasmic sex ratio distorters generally increase in female biased populations and often restore a 11 sex ratio despite continual selection on the cytoplasmic element to increase its transmission efficiency.     

Female common lizards (Lacerta vivipara) do not adjust their sex-biased investment in relation to the adult sex ratio

Sex allocation theory predicts that facultative maternal investment in the rare sex should be favoured by natural selection when breeders experience predictable variation in adult sex ratios (ASRs). We found significant spatial and predictable interannual changes in local ASRs within a natural population of the common lizard where the mean ASR is female-biased, thus validating the key assumptions of adaptive sex ratio models. We tested for facultative maternal investment in the rare sex during and after an experimental perturbation of the ASR by creating populations with female-biased or male-biased ASR. Mothers did not adjust their clutch sex ratio during or after the ASR perturbation, but produced sons with a higher body condition in male-biased populations. However, this differential sex allocation did not result in growth or survival differences in offspring. Our results thus contradict the predictions of adaptive models and challenge the idea that facultative investment in the rare sex might be a mechanism regulating the population sex ratio.     

Environmental sex reversal,Trojan sex genes,and sex ratio adjustment: conditions and population consequences

The great diversity of sex determination mechanisms in animals and plants ranges from genetic sex determination (GSD, e.g. mammals, birds, and most dioecious plants) to environmental sex determination (ESD, e.g. many reptiles) and includes a mixture of both, for example when an individual’s genetically determined sex is environmentally reversed during ontogeny (ESR, environmental sex reversal, e.g. many fish and amphibia). ESD and ESR can lead to widely varying and unstable population sex ratios. Populations exposed to conditions such as endocrine‐active substances or temperature shifts may decline over time due to skewed sex ratios, a scenario that may become increasingly relevant with greater anthropogenic interference on watercourses. Continuous exposure of populations to factors causing ESR could lead to the extinction of genetic sex factors and may render a population dependent on the environmental factors that induce the sex change. However, ESR also presents opportunities for population management, especially if the Y or W chromosome is not, or not severely, degenerated. This seems to be the case in many amphibians and fish. Population growth or decline in such species can potentially be controlled through the introduction of so‐called Trojan sex genes carriers, individuals that possess sex chromosomes or genes opposite from what their phenotype predicts. Here, we review the conditions for ESR, its prevalence in natural populations, the resulting physiological and reproductive consequences, and how these may become instrumental for population management.     

GENETICS OF SEX RATIO VARIATION AMONG NATURAL POPULATIONS OF A DIOECIOUS PLANT

The female-biased sex ratio in the genus Silene is the most widely documented example of sex ratio bias in plants. It has recently been shown that the genetic basis of sex ratio in this species involves a system of sex ratio distorters and restorers, but it is not known if these genetic elements are of fundamental importance in natural populations. I crossed plants from natural populations with known testers to examine the frequencies of sex ratio distorters and restorers in eight populations of S. alba, and to determine the extent that these elements are responsible for the sex ratio variation in nature. The genetic basis of sex ratio varied from one population to another, suggesting that sex ratio evolution occurs over a relatively small spatial scale and is asynchronous among local demes. The resulting variation in the frequency of sex ratio alleles among populations explained most of the sex ratio variation seen in nature, which suggests that the ecology and evolution of this trait in natural populations is governed primarily by underlying dynamics of selfish genetic elements. The possible causes and the evolutionary consequences of population structure at genes controlling sex ratio are discussed, as are the implications of these results for the overall importance of selfish genetic elements in natural populations.     

Sex ratio variance and the maintenance of environmental sex determination

Although variation in population sex ratios is predicted to increase the extinction rate of clades with environmental sex determination (ESD), ESD is still seen in a wide array of natural systems. It is unclear how this common sex-determining system has persisted despite this inherent disadvantage associated with ESD. We use simulation modelling to examine the effect of the sex ratio variance caused by ESD on population colonization and establishment. We find that an accelerating function of establishment success on initial population sex ratio favours a system that produces variance in sex ratios over one that consistently produces even sex ratios. This sex ratio variance causes ESD to be favoured over genetic sex determination, even when the mean global sex ratio under both sex-determining systems is the same. Data from ESD populations suggest that the increase in population establishment can more than offset the increased risk of extinction associated with temporal fluctuations in the sex ratio. These findings demonstrate that selection in natural systems can favour increased variance in a trait, irrespective of the mean trait value. Our results indicate that sex ratio variation may provide an advantage to species with ESD, and may help explain the widespread existence of this sex-determining system.     

Sex allocation by a mite parasitic on insects: local mate competition,host quality and operational sex ratio

The aim of this study was to test the predictions of local mate competition (LMC), host quality (HQ) and operational sex ratio (OSR) models, using a non-arrhenotokous parasitic mite, Hemisarcoptes coccophagus (Astigmata: Hemisarcoptidae). The life-history pattern of this mite meets the assumptions of these sex allocation models. Mating group size (LMC model), HQ and OSR affected the sex allocation of H. coccophagus females. Only young mite females adjusted the sex ratio of their progenies according to the predictions of LMC and HQ models; the sex allocation of old females was contrary to these predictions. We explain these patterns by the dynamic nature of the mite's population structure. When parents are young, their population distribution is patchy and progeny matings are local; hence sex allocation is in accordance with LMC theory. When parents become older, their populations shift towards panmixis; factors which had operated previously no longer exist. Consequently, females adjust the sex ratio of late progenies so that it can compensate for the earlier sex allocation, in order to make their total sex ratio unbiased, as expected in panmictic populations. Our data, expressed as the cumulative sex ratio, support this hypothesis.     

Sexual conflict in action: An antagonistic relationship between maternal and paternal sex allocation in the tammar wallaby,Notamacropus eugenii

Sex ratio biases are often inconsistent, both among and within species and populations. While some of these inconsistencies may be due to experimental design, much of the variation remains inexplicable. Recent research suggests that an exclusive focus on mothers may account for some of the inconsistency, with an increasing number of studies showing variation in sperm sex ratios and seminal fluids. Using fluorescent in‐situ hybridization, we show a significant population‐level Y‐chromosome bias in the spermatozoa of wild tammar wallabies, but with significant intraindividual variation between males. We also show a population‐level birth sex ratio trend in the same direction toward male offspring, but a weaning sex ratio that is significantly female‐biased, indicating that males are disproportionately lost during lactation. We hypothesize that sexual conflict between parents may cause mothers to adjust offspring sex ratios after birth, through abandonment of male pouch young and reactivation of diapaused embryos. Further research is required in a captive, controlled setting to understand what is driving and mechanistically controlling sperm sex ratio and offspring sex ratio biases and to understand the sexually antagonistic relationship between mothers and fathers over offspring sex. These results extend beyond sex allocation, as they question studies of population processes that assume equal input of sex chromosomes from fathers, and will also assist with future reproduction studies for management and conservation of marsupials.     

A method for estimating population sex ratio for sage‐grouse using noninvasive genetic samples

Population sex ratio is an important metric for wildlife management and conservation, but estimates can be difficult to obtain, particularly for sexually monomorphic species or for species that differ in detection probability between the sexes. Noninvasive genetic sampling (NGS) using polymerase chain reaction (PCR) has become a common method for identifying sex from sources such as hair, feathers or faeces, and is a potential source for estimating sex ratio. If, however, PCR success is sex‐biased, naively using NGS could lead to a biased sex ratio estimator. We measured PCR success rates and error rates for amplifying the W and Z chromosomes from greater sage‐grouse (Centrocercus urophasianus) faecal samples, examined how success and error rates for sex identification changed in response to faecal sample exposure time, and used simulation models to evaluate precision and bias of three sex assignment criteria for estimating population sex ratio with variable sample sizes and levels of PCR replication. We found PCR success rates were higher for females than males and that choice of sex assignment criteria influenced the bias and precision of corresponding sex ratio estimates. Our simulations demonstrate the importance of considering the interplay between the sex bias of PCR success, number of genotyping replicates, sample size, true population sex ratio and accuracy of assignment rules for designing future studies. Our results suggest that using faecal DNA for estimating the sex ratio of sage‐grouse populations has great potential and, with minor adaptations and similar marker evaluations, should be applicable to numerous species.     

Frequency‐dependent two‐sex models: a new approach to sex ratio evolution with multiple maternal conditions

Mothers that experience different individual or environmental conditions may produce different proportions of male to female offspring. The Trivers‐Willard hypothesis, for instance, suggests that mothers with different qualities (size, health, etc.) will use different sex ratios if maternal quality differentially affects sex‐specific reproductive success. Condition‐dependent, or facultative, sex ratio strategies like these allow multiple sex ratios to coexist within a population. They also create complex population structure due to the presence of multiple maternal conditions. As a result, modeling facultative sex ratio evolution requires not only sex ratio strategies with multiple components, but also two‐sex population models with explicit stage structure. To this end, we combine nonlinear, frequency‐dependent matrix models and multidimensional adaptive dynamics to create a new framework for studying sex ratio evolution. We illustrate the applications of this framework with two case studies where the sex ratios depend one of two possible maternal conditions (age or quality). In these cases, we identify evolutionarily singular sex ratio strategies, find instances where one maternal condition produces exclusively male or female offspring, and show that sex ratio biases depend on the relative reproductive value ratios for each sex.     

The effect of size and sex ratio experiences on reproductive competition in Nicrophorus vespilloides burying beetles in the wild

Male parents face a choice: should they invest more in caring for offspring or in attempting to mate with other females? The most profitable course depends on the intensity of competition for mates, which is likely to vary with the population sex ratio. However, the balance of pay‐offs may vary among individual males depending on their competitive prowess or attractiveness. We tested the prediction that sex ratio and size of the resource holding male provide cues regarding the level of mating competition prior to breeding and therefore influence the duration of a male's biparental caring in association with a female. Male burying beetles, Nicrophorus vespilloides were reared, post‐eclosion, in groups that differed in sex ratio. Experimental males were subsequently translocated to the wild, provided with a breeding resource (carcass) and filmed. We found no evidence that sex ratio cues prior to breeding affected future parental care behaviour but males that experienced male‐biased sex ratios took longer to attract wild mating partners. Smaller males attracted a higher proportion of females than did larger males, securing significantly more monogamous breeding associations as a result. Smaller males thus avoided competitive male–male encounters more often than larger males. This has potential benefits for their female partners who avoid both intrasexual competition and direct costs of higher mating frequency associated with competing males.     

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.     

Natural variation of the Y chromosome suppresses sex ratio distortion and modulates testis-specific gene expression in Drosophila simulans

X-linked sex-ratio distorters that disrupt spermatogenesis can cause a deficiency in functional Y-bearing sperm and a female-biased sex ratio. Y-linked modifiers that restore a normal sex ratio might be abundant and favored when a X-linked distorter is present. Here we investigated natural variation of Y-linked suppressors of sex-ratio in the Winters systems and the ability of these chromosomes to modulate gene expression in Drosophila simulans. Seventy-eight Y chromosomes of worldwide origin were assayed for their resistance to the X-linked sex-ratio distorter gene Dox. Y chromosome diversity caused males to sire ∼63% to ∼98% female progeny. Genome-wide gene expression analysis revealed hundreds of genes differentially expressed between isogenic males with sensitive (high sex ratio) and resistant (low sex ratio) Y chromosomes from the same population. Although the expression of about 75% of all testis-specific genes remained unchanged across Y chromosomes, a subset of post-meiotic genes was upregulated by resistant Y chromosomes. Conversely, a set of accessory gland-specific genes and mitochondrial genes were downregulated in males with resistant Y chromosomes. The D. simulans Y chromosome also modulated gene expression in XXY females in which the Y-linked protein-coding genes are not transcribed. The data suggest that the Y chromosome might exert its regulatory functions through epigenetic mechanisms that do not require the expression of protein-coding genes. The gene network that modulates sex ratio distortion by the Y chromosome is poorly understood, other than that it might include interactions with mitochondria and enriched for genes expressed in post-meiotic stages of spermatogenesis.     

A demographic model for sex ratio evolution and the effects of sex‐biased offspring costs

The evolution of the primary sex ratio, the proportion of male births in an individual's offspring production strategy, is a frequency‐dependent process that selects against the more common sex. Because reproduction is shaped by the entire life cycle, sex ratio theory would benefit from explicitly two‐sex models that include some form of life cycle structure. We present a demographic approach to sex ratio evolution that combines adaptive dynamics with nonlinear matrix population models. We also determine the evolutionary and convergence stability of singular strategies using matrix calculus. These methods allow the incorporation of any population structure, including multiple sexes and stages, into evolutionary projections. Using this framework, we compare how four different interpretations of sex‐biased offspring costs affect sex ratio evolution. We find that demographic differences affect evolutionary outcomes and that, contrary to prior belief, sex‐biased mortality after parental investment can bias the primary sex ratio (but not the corresponding reproductive value ratio). These results differ qualitatively from the widely held conclusions of previous models that neglect demographic structure.     

Male‐skewed adult sex ratio,survival, mating opportunity and annual productivity in the Snowy Plover Charadrius alexandrinus

Sex differences in adult mortality may be responsible for male‐skewed adult sex ratios and male‐skewed parental care in some birds. Because a surplus of breeding males has been reported in serially polyandrous populations of Snowy Plover Charadrius alexandrinus, we examined sex ratio, early‐season nesting opportunities, adult survival and annual reproductive success of a Snowy Plover population at Monterey Bay, California. We tested the hypotheses that male adult survival was greater than female survival and that a sex difference in adult survival led to a skewed adult sex ratio, different mating opportunities and different annual productivity between the sexes. Virtually all females left chicks from their first broods to the care of the male and re‐nested with a new mate. As a result, females had time to parent three successful nesting attempts during the lengthy breeding season, whereas males had time for only two successful attempts. Among years, the median population of nesting Plovers was 96 males and 84 females (median difference = 9), resulting in one extra male per eight pairs. The number of potential breeders without mates during the early nesting period each year was higher in males than in females. Adult male survival (0.734 ± 0.028 se) was higher than female survival (0.693 ± 0.030 se) in top‐ranked models. Annually, females parented more successful clutches and fledged more chicks than their first mates of the season. Our results suggest that in C. alexandrinus a sex difference in adult survival results in a male‐skewed sex ratio, which creates more nesting opportunities and greater annual productivity for females than for males.