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.     

Climate effects on offspring sex ratio in a viviparous lizard

1. Understanding individual and population responses to climate change is emerging as an important challenge. Because many phenotypic traits are sensitive to environmental conditions, directional climate change could significantly alter trait distribution within populations and may generate an evolutionary response. 2. In species with environment-dependent sex determination, climate change may lead to skewed sex ratios at hatching or birth. However, there are virtually no empirical data on the putative link between climatic parameters and sex ratios from natural populations. 3. We monitored a natural population of viviparous lizards with temperature-dependent sex determination (Niveoscincus ocellatus) over seven field seasons. Sex ratios at birth fluctuated significantly among years and closely tracked thermal conditions in the field, with the proportion of male offspring increasing in colder years. 4. This is the first study to demonstrate the effect of local climatic conditions (e.g. temperature) on offspring sex ratio fluctuations in a free-living population of a viviparous ectotherm. A succession of warmer-than-usual years (as predicted under many climate-change scenarios) likely would generate female-biased sex ratios at birth, while an increase in interannual variation (as also predicted under climate change scenarios) could lead to significant fluctuations in cohort sex ratios. If cohort sex ratio bias at birth leads to adult sex ratio bias, long-term directional changes in thermal conditions may have important effects on population dynamics in this species.     

Mutual information reveals variation in temperature-dependent sex determination in response to environmental fluctuation, lifespan and selection

Quantifying the degree to which sex determination depends on the environment can yield insight into the evolution, ecological dynamics, and functional aspects of sex determination. In temperature-dependent sex determination (TSD), theory often predicts a complete dependence of sex on temperature, with a switch-like reaction norm. However, empirical data suggest more shallow relationships between sex and temperature. Here, we demonstrate the usefulness of an index, mutual information (MI), to reflect the degree of temperature dependence in sex. MI depends on both the shape of a reaction norm and the natural temperature variation, thus providing a measure of TSD that is ecologically dependent. We demonstrate that increased lifespan and decreased environmental fluctuation predict reaction norms with high MI (switch-like). However, mutation and weaker selection on sex-specific performance reduce average MI in a population, suggesting that mutation-selection balance can resolve some of the conflict between theoretical predictions of individual-based optimality and population-based empirical results. The MI index allows clear comparison of TSD across life histories and habitats and reveals functional similarities between reaction norms that may appear different. The model provides testable predictions for TSD across populations, namely that MI should increase with lifespan and decrease with historical environmental fluctuations.     

Early-life food stress hits females harder than males in insects: A meta-analysis of sex differences in environmental sensitivity

Fitness consequences of early-life environmental conditions are often sex-specific, but corresponding evidence for invertebrates remains inconclusive. Here, we use meta-analysis to evaluate sex-specific sensitivity to larval nutritional conditions in insects. Using literature-derived data for 85 species with broad phylogenetic and ecological coverage, we show that females are generally more sensitive to food stress than males. Stressful nutritional conditions during larval development typically lead to female-biased mortality and thus increasingly male-biased sex ratios of emerging adults. We further demonstrate that the general trend of higher sensitivity to food stress in females can primarily be attributed to their typically larger body size in insects and hence higher energy needs during development. By contrast, there is no consistent evidence of sex-biased sensitivity in sexually size-monomorphic species. Drawing conclusions regarding sex-biased sensitivity in species with male-biased size dimorphism remains to wait for the accumulation of relevant data. Our results suggest that environmental conditions leading to elevated juvenile mortality may potentially affect the performance of insect populations further by reducing the proportion of females among individuals reaching reproductive age. Accounting for sex-biased mortality is therefore essential to understanding the dynamics and demography of insect populations, not least importantly in the context of ongoing insect declines.     

Developmental mortality increases sex‐ratio bias of a size‐dimorphic bark beetle

1. Given sexual size dimorphism, differential mortality owing to body size can lead to sex‐biased mortality, proximately biasing sex ratios. This mechanism may apply to mountain pine beetles, Dendroctonus ponderosae Hopkins, which typically have female‐biased adult populations (2 : 1) with females larger than males. Smaller males could be more susceptible to stresses than larger females as developing beetles overwinter and populations experience high mortality. 2. Survival of naturally‐established mountain pine beetles during the juvenile stage and the resulting adult sex ratios and body sizes (volume) were studied. Three treatments were applied to vary survival in logs cut from trees containing broods of mountain pine beetles. Logs were removed from the forest either in early winter, or in spring after overwintering below snow or after overwintering above snow. Upon removal, logs were placed at room temperature to allow beetles to complete development under similar conditions. 3. Compared with beetles from logs removed in early winter, mortality was higher and the sex ratio was more female‐biased in overwintering logs. The bias increased with overwinter mortality. However, sex ratios were female‐biased even in early winter, so additional mechanisms, other than overwintering mortality, contributed to the sex‐ratio bias. Body volume varied little relative to sex‐biased mortality, suggesting other size‐independent causes of male‐biased mortality. 4. Overwintering mortality is considered a major determinant of mountain pine beetle population dynamics. The disproportionate survival of females, who initiate colonisation of live pine trees, may affect population dynamics in ways that have not been previously considered.     

Sex ratio variation in gynodioecious Lobelia siphilitica: effects of population size and geographic location

Variation in population sex ratio can be influenced by natural selection on alternate sex phenotypes as well as nonselective mechanisms, such as genetic drift and founder effects. If natural selection contributes to variation in population sex ratio, then sex ratio should covary with resource availability or herbivory. With nonselective mechanisms, sex ratio should covary with population size. We estimated sex ratio, resource availability, herbivory and size of 53 populations of gynodioecious Lobelia siphilitica. Females were more common in populations with higher annual temperatures, lower soil moisture and lower predation on female fruits, consistent with sex-specific selection. Females were also more common in small populations, consistent with drift, inbreeding or founder effects. However, small populations occurred in areas with higher temperatures than large populations, suggesting that female frequencies in small populations could be caused by sex-specific selection. Both selective and nonselective mechanisms likely affect sex ratio variation in this gynodioecious species.     

Demographic effects of temperature‐dependent sex determination: will tuatara survive global warming?

Global climate change is of particular concern for small and isolated populations of reptiles with temperature-dependent sex determination because low genetic variation can limit adaptive response in pivotal temperatures, leading to skewed sex ratios. We explore the demographic consequences of skewed sex ratios on the viability of a tuatara population characterized by low genetic diversity. We studied the rare species of tuatara ( Sphenodon guntheri ) on the 4 ha North Brother Island in New Zealand over two nesting seasons and captured 477 individuals, with a 60% male bias in the adult population. Females first breed at 15 years and have extremely low rates of gravidity, producing clutches of three to eight eggs every 9 years. Simulations of the population using population viability analysis showed that the current population is expected to persist for at least 2000 years at hatchling sex ratios of up to 75% male, but populations with 85% male hatchlings are expected to become extinct within approximately 300 years (some eight generations). Incorporation of inbreeding depression increased the probability of extinction under male biased sex ratios, with no simulated populations surviving at hatchling sex ratios >75% male. Because recent models have predicted that climate change could lead to the production of all male S. guntheri hatchlings by 2085, we examined whether periodic intervention to produce mixed or female biased sex ratios would allow the population to survive if only males were produced in natural nests. We show that intervention every 2–3 years could buffer the effects of climate change on population sex ratios, but translocation to cooler environs might be more cost-effective. Climate change threatens tuatara populations because neither modified nesting behaviour nor adaptive response of the pivotal temperature can modify hatchling sex ratios fast enough in species with long generation intervals.     

Low temperature has opposite effects on sex determination in a marine fish at the larval/postlarval and juvenile stages

Temperature‐dependent sex determination (TSD) can be observed in multiple reptile and fish species. It is adaptive when varying environmental conditions advantage either males or females. A good knowledge of the thermosensitive period is key to understand how environmental changes may lead to changes in population sex ratio. Here, by manipulating temperature during development, we confirm that cold temperature (16°C) increases the proportion of fish that develop as females in European sea bass (Dicentrarchus labrax) until 56 days posthatching, but show that it has an opposite effect at later stages, with the proportion of males reaching ~90% after 230 days at 16°C. This is the first observation of opposite effects of temperature at different time periods on the sex ratio of a vertebrate. Our results highlight the potential complexity of environmental effects on sex determination.     

SEX RATIO SELECTION AND THE EVOLUTION OF ENVIRONMENTAL SEX DETERMINATION IN LABORATORY POPULATIONS OF MENIDIA MENIDIA

What happens when a population with environmental sex determination (ESD) experiences a change to an extreme environment that causes a highly unbalanced sex ratio? Theory predicts that frequency-dependent selection would increase the proportion of the minority sex and decrease the level of ESD in subsequent generations. We empirically modeled this process by maintaining five laboratory populations of a fish with temperature-dependent sex determination (the Atlantic silverside, Menidia menidia) in extreme constant temperature environments that caused highly skewed sex ratios to occur initially. Increases in the minority sex consistently occurred from one generation to the next across all five populations, first establishing and then maintaining a balanced sex ratio until termination of the experiment at 8 to 10 generations. The extent to which the level of ESD changed as balanced sex ratios evolved, however, was not consistent. Two populations that experienced high temperatures each generation displayed a loss of ESD, and in one of these ESD was virtually eliminated. This suggests that temperature-insensitive, sex-determining genes were being selected. In populations maintained in low temperature environments, however, the level of ESD did not decline. Instead, the response of sex ratio to temperature was adjusted upward or downward, perhaps by selection of sex-determining genes sensitive to higher (or lower) temperatures. The two different outcomes at low versus high temperatures occurred independent of the geographic origin of the founding population. Our results demonstrate that ESD is capable of evolving in response to selection.     

Sex-ratio distortion driven by migration loads

The significance of migration load in driving the evolution of recipient populations has long been documented in population genetics, but its effects have not been linked to the formation of biased sex ratios in natural populations. In this study, we develop a single-locus model to demonstrate how the migration load can shape the primary and secondary sex ratios in dioecious plants where sexual dimorphism is determined by the sex chromosomes (the XX-XY or similar systems). Our results show that migration load can generate an array of sex ratios (from the female- to male-biased primary/secondary sex ratios), depending on the selection systems at the gametophyte and sporophyte stages and on the sex ratio in the migrating seeds. Ovule abortion and the purging of maladaptive genes from the immigrating pollen at the gametophyte stage can alter the primary sex ratio and indirectly alter the secondary sex ratio. The presence of maladaptive sex-linked genes from the migrating pollen and seeds of males facilitates the outcome of the female-biased secondary sex ratios, while the presence of maladaptive sex-linked genes from the migrating seeds of females can lead to the male-biased secondary sex ratios. The detrimental effects of the Y-chromosome from the migrating pollen and seeds can enhance the formation of female-biased primary and secondary sex ratios. These theoretical predictions highlight an alternative approach to the existing sex-ratio theories for interpreting the formation of biased sex ratios in the populations that are subject to the impacts of maladaptive genes from immigrants.     

Sex-specific sibling interactions and offspring fitness in vertebrates: patterns and implications for maternal sex ratios

Vertebrate sex ratios are notorious for their lack of fit to theoretical models, both with respect to the direction and the magnitude of the sex ratio adjustment. The reasons for this are likely to be linked to simplifying assumptions regarding vertebrate life histories. More specifically, if the sex ratio adjustment itself influences offspring fitness, due to sex-specific interactions among offspring, this could affect optimal sex ratios. A review of the literature suggests that sex-specific sibling interactions in vertebrates result from three major causes: (i) sex asymmetries in competitive ability, for example due to sexual dimorphism, (ii) sex-specific cooperation or helping, and (iii) sex asymmetries in non-competitive interactions, for example steroid leakage between fetuses. Incorporating sex-specific sibling interactions into a sex ratio model shows that they will affect maternal sex ratio strategies and, under some conditions, can repress other selection pressures for sex ratio adjustment. Furthermore, sex-specific interactions could also explain patterns of within-brood sex ratio (e.g. in relation to laying order). Failure to take sex-specific sibling interactions into account could partly explain the lack of sex ratio adjustment in accordance with theoretical expectations in vertebrates, and differences among taxa in sex-specific sibling interactions generate predictions for comparative and experimental studies.     

TEMPERATURE‐DEPENDENT TURNOVERS IN SEX‐DETERMINATION MECHANISMS: A QUANTITATIVE MODEL

Sex determination is often seen as a dichotomous process: individual sex is assumed to be determined either by genetic (genotypic sex determination, GSD) or by environmental factors (environmental sex determination, ESD), most often temperature (temperature sex determination, TSD). We endorse an alternative view, which sees GSD and TSD as the ends of a continuum. Both effects interact a priori, because temperature can affect gene expression at any step along the sex‐determination cascade. We propose to define sex‐determination systems at the population‐ (rather than individual) level, via the proportion of variance in phenotypic sex stemming from genetic versus environmental factors, and we formalize this concept in a quantitative‐genetics framework. Sex is seen as a threshold trait underlain by a liability factor, and reaction norms allow modeling interactions between genotypic and temperature effects (seen as the necessary consequences of thermodynamic constraints on the underlying physiological processes). As this formalization shows, temperature changes (due to e.g., climatic changes or range expansions) are expected to provoke turnovers in sex‐ determination mechanisms, by inducing large‐scale sex reversal and thereby sex‐ratio selection for alternative sex‐determining genes. The frequency of turnovers and prevalence of homomorphic sex chromosomes in cold‐blooded vertebrates might thus directly relate to the temperature dependence in sex‐determination mechanisms.     

Sex Determination in Freshwater Eels and Management Options for Manipulation of Sex

Catadromous eels enter fresh water as sexually undifferentiated glass eels and develop into males and females before migrating back to sea as silver eels. Females develop ovaries directly from the ambiguous primordial gonad whereas males pass through a transitional intersexual stage before developing testes. Eels have sex-specific life-history strategies. Males may grow faster than females initially, but this difference is soon reversed and females attain a greater age- and size-at-metamorphosis than males. Male fitness is maximized by maturing at the smallest size that allows a successful spawning migration (a time-minimizing strategy) whereas females adopt a more flexible size-maximizing strategy that trades off pre-reproductive mortality against fecundity. Although heteromorphic sex chromosomes have been identified in some species, the sex of developing gonads is labile and gender is determined principally by environmental factors. Individuals experiencing rapid growth prior to gonad differentiation tend to develop as males, whereas eels that grow slowly initially are more likely to develop as females. Paradoxically, males tend to predominate under conditions of high density, which may be because a male “grow quickly, mature early” strategy increases an individual’s chances of survival during periods of intraspecific competition. High temperatures and saline conditions have also been proposed to favor development as males but experimental studies have failed to demonstrate a clear effect of either on sex determination. High proportions of female silver eels migrating from some upstream areas, lakes and large rivers may be due to low population density or poor conditions for growth in these habitats. Manipulating sex ratios in favor of females has the potential to increase eel production in aquaculture and to buffer natural populations against fishing pressure. Sex steroids (oestrogens and phytoestrogens) have a strong feminizing effect on undifferentiated individuals and are most effective when targeted at younger eels and administered at high doses for prolonged periods. Modifying local environmental conditions, in particular reducing eel density and limiting interference and social stress, may also promote the development of females. Further research into the timing and mechanisms of sex determination in eels is required to effectively and efficiently manipulate sex for conservation and/or economic benefit.     

X-linked meiotic drive can boost population size and persistence

X-linked meiotic drivers cause X-bearing sperm to be produced in excess by male carriers, leading to female-biased sex ratios. Here, we find general conditions for the spread and fixation of X-linked alleles. Our conditions show that the spread of X-linked alleles depends on sex-specific selection and transmission rather than the time spent in each sex. Applying this logic to meiotic drive, we show that polymorphism is heavily dependent on sperm competition induced both by female and male mating behavior and the degree of compensation to gamete loss in the ejaculate size of drive males. We extend these evolutionary models to investigate the demographic consequences of biased sex ratios. Our results suggest driving X-alleles that invade and reach polymorphism (or fix and do not bias segregation excessively) will boost population size and persistence time by increasing population productivity, demonstrating the potential for selfish genetic elements to move sex ratios closer to the population-level optimum. However, when the spread of drive causes strong sex-ratio bias, it can lead to populations with so few males that females remain unmated, cannot produce offspring, and go extinct. This outcome is exacerbated when the male mating rate is low. We suggest that researchers should consider the potential for ecologically beneficial side effects of selfish genetic elements, especially in light of proposals to use meiotic drive for biological control.     

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.     

Prenatal environmental influences on the production of sex-specific traits in mammals

The determination of offspring sex represents a delicate balancing act during which offspring must pass through several developmental levels in the presence of influential environmental factors. Successful expression of sex-specific traits requires genetic and hormone-based effects on several organizational and activational levels. Environmental factors can exert controls and disruptions at each of these levels. This review addresses the developmental stages at which environmental factors may influence the processes of sex determination, with an in depth focus on the prenatal stages, including the production of the primary and secondary sex ratios and the differentiation of functional secondary sexual characters.     

Do operational sex ratios influence sex allocation in viviparous lizards with temperature‐dependent sex determination?

Under certain environmental situations, selection may favour the ability of females to adjust the sex ratio of their offspring. Two recent studies have suggested that viviparous scincid lizards can modify the sex ratio of the offspring they produce in response to the operational sex ratio (OSR). Both of the species in question belong to genera that have also recently been shown to exhibit temperature-dependent sex determination (TSD). Here we test whether pregnant montane water skinks (Eulamprus tympanum) utilise TSD to select offspring sex in response to population wide imbalances in the OSR, by means of active thermoregulation. We use a combination of laboratory and field-based experiments, and conduct the first field-based test of this hypothesis by maintaining females in outdoor enclosures of varying OSR treatments throughout pregnancy. Although maternal body temperature during pregnancy was influenced by OSR, the variation in temperature was not great enough to affect litter sex ratios or any other phenotypic traits of the offspring.     

The ecology and evolution of temperature‐dependent reaction norms for sex determination in reptiles: a mechanistic conceptual model

Sex‐determining mechanisms are broadly categorised as being based on either genetic or environmental factors. Vertebrate sex determination exhibits remarkable diversity but displays distinct phylogenetic patterns. While all eutherian mammals possess XY male heterogamety and female heterogamety (ZW) is ubiquitous in birds, poikilothermic vertebrates (fish, amphibians and reptiles) exhibit multiple genetic sex‐determination (GSD) systems as well as environmental sex determination (ESD). Temperature is the factor controlling ESD in reptiles and temperature‐dependent sex determination (TSD) in reptiles has become a focal point in the study of this phenomenon. Current patterns of climate change may cause detrimental skews in the population sex ratios of reptiles exhibiting TSD. Understanding the patterns of variation, both within and among populations and linking such patterns with the selection processes they are associated with, is the central challenge of research aimed at predicting the capacity of populations to adapt to novel conditions. Here we present a conceptual model that innovates by defining an individual reaction norm for sex determination as a range of incubation temperatures. By deconstructing individual reaction norms for TSD and revealing their underlying interacting elements, we offer a conceptual solution that explains how variation among individual reaction norms can be inferred from the pattern of population reaction norms. The model also links environmental variation with the different patterns of TSD and describes the processes from which they may arise. Specific climate scenarios are singled out as eco‐evolutionary traps that may lead to demographic extinction or a transition to either male or female heterogametic GSD. We describe how the conceptual principles can be applied to interpret TSD data and to explain the adaptive capacity of TSD to climate change as well as its limits and the potential applications for conservation and management programs.     

The effect of temperature on sex ratio in the isopod Porcellionides pruinosus: Environmental sex determination or a by-product of cytoplasmic sex determination?

The sex ratios of the progenies of woodlice Porcellionides pruinosus (Crustacea, Isopoda) raised at different temperatures were studied. Females from three French populations sampled in the wild produced highly female-biased broods at 20°C and male-biased broods above 30°C. The effect of high temperature was not due to selective mortality of females. Sex determination was thus sensitive to temperature in P. pruinosus. We also found an interpopulation variability of sex ratio thermosensitivity and a weak inheritance of male-biased sex ratios at high temperatures. Samples taken from a wild population throughout the year showed that while the thermal conditions required for changes in the sex ratio occurred, there was no significant variation in the sex ratio. On the other hand, almost all the females and many males in the four populations studied harboured intracytoplasmic bacteria. These maternally inherited symbionts belong to the genus Wolbachia and are known to possess a feminizing effect. While in other arthropods Wolbachia are destroyed at high temperatures, the symbionts of P. pruinosus were detected by a PCR procedure whatever the rearing temperatures. In light of these results, we propose that the thermosensitivity of sex determination in P. pruinosus could reflect the removal of the cytoplasmic effect on sex determination rather than environmental sex determination sensu stricto. The reduction in the amount of bacteria (but not their entire elimination), or the inhibition of bacterial metabolism, may be responsible for sex ratio variations relating to temperature. The incomplete inheritance of male-biased sex ratios at high temperatures might reflect a selection of thermo-tolerant bacterial strains.     

Pleistocene divergence in the absence of gene flow among populations of a viviparous reptile with intraspecific variation in sex determination

Polymorphisms can lead to genetic isolation if there is differential mating success among conspecifics divergent for a trait. Polymorphism for sex‐determining system may fall into this category, given strong selection for the production of viable males and females and the low success of heterogametic hybrids when sex chromosomes differ (Haldane''s rule). Here we investigated whether populations exhibiting polymorphism for sex determination are genetically isolated, using the viviparous snow skink Carinascincus ocellatus. While a comparatively high elevation population has genotypic sex determination, in a lower elevation population there is an additional temperature component to sex determination. Based on 11,107 SNP markers, these populations appear genetically isolated. “Isolation with Migration” analysis also suggests these populations diverged in the absence of gene flow, across a period encompassing multiple Pleistocene glaciations and likely greater geographic proximity of populations. However, further experiments are required to establish whether genetic isolation may be a cause or consequence of differences in sex determination. Given the influence of temperature on sex in one lineage, we also discuss the implications for the persistence of this polymorphism under climate change.