The decapod researcher’s guide to the galaxy of sex determination

The objective of this study was to assess the frequency of use of marine resources in recruitment of Southern Hemisphere native riverine fish Galaxias maculatus from rivers across a latitudinal gradient. To do this, we analysed the concentrations of δ³⁴S in vertebral column tissues from fish collected in ten Chilean river systems across latitudes 36°–47°S. The analyses of δ³⁴S signatures in these rivers suggest that the use of marine resources by riverine populations of G. maculatus in large river systems in Chile is variable, with marine resources playing a limited role in more northern large rivers, characterised by warmer temperatures and predictable flow regimes and floodplain inundations. This is in contrast to life histories described for G. maculatus in rivers from New Zealand and Australia, where riverine populations are believed to be characterised by an obligatory recruitment phase in marine environments. Recruitment of G. maculatus in Chilean large rivers appears to depend on their freshwater productivity driven by climate as well as both longitudinal (headwaters lakes-estuary) and lateral (main channel-floodplains) hydrologic connectivities.     

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.     

Cellular calcium and redox regulation: the mediator of vertebrate environmental sex determination?

Many reptiles and some fish determine offspring sex by environmental cues such as incubation temperature. The mechanism by which environmental signals are captured and transduced into specific sexual phenotypes has remained unexplained for over 50 years. Indeed, environmental sex determination (ESD) has been viewed as an intractable problem because sex determination is influenced by a myriad of genes that may be subject to environmental influence. Recent demonstrations of ancient, conserved epigenetic processes in the regulatory response to environmental cues suggest that the mechanisms of ESD have a previously unsuspected level of commonality, but the proximal sensor of temperature that ultimately gives rise to one sexual phenotype or the other remains unidentified. Here, we propose that in ESD species, environmental cues are sensed by the cell through highly conserved ancestral elements of calcium and redox (CaRe) status, then transduced to activate ubiquitous signal transduction pathways, or influence epigenetic processes, ultimately to drive the differential expression of sex genes. The early evolutionary origins of CaRe regulation, and its essential role in eukaryotic cell function, gives CaRe a propensity to be independently recruited for diverse roles as a ‘cellular sensor’ of environmental conditions. Our synthesis provides the first cohesive mechanistic model connecting environmental signals and sex determination pathways in vertebrates, providing direction and a framework for developing targeted experimentation.     

Is regulation of aromatase expression in reptiles the key to understanding temperature-dependent sex determination?

A brief review of our current understanding (or lack of understanding) of the molecular basis of temperature-dependent sex determination (TSD) in reptiles is presented. Current theories are discussed: yolk steroids as sex determinants, the brain as the driver for TSD and the enzyme aromatase and estrogen production as the possible determinants of sex. There is little evidence to support the first two theories, but enough evidence to keep the third theory in play. As yet, however, we have no molecular understanding of how a two-degree difference in temperature during the temperature-sensitive phase of egg incubation can initiate the molecular cascade that determines whether the indifferent gonad develops as an ovary or a testis.     

Avian sex determination: what, when and where?

Sex is determined genetically in all birds, but the underlying mechanism remains unknown. All species have a ZZ/ZW sex chromosome system characterised by female (ZW) heterogamety, but the chromosomes themselves can be heteromorphic (in most birds) or homomorphic (in the flightless ratites). Sex in birds might be determined by the dosage of a Z-linked gene (two in males, one in females) or by a dominant ovary-determining gene carried on the W sex chromosome, or both. Sex chromosome aneuploidy has not been conclusively documented in birds to differentiate between these possibilities. By definition, the sex chromosomes of birds must carry one or more sex-determining genes. In this review of avian sex determination, we ask what, when and where? What is the nature of the avian sex determinant? When should it be expressed in the developing embryo, and where is it expressed? The last two questions arise due to evidence suggesting that sex-determining genes in birds might be operating prior to overt sexual differentiation of the gonads into testes or ovaries, and in tissues other than the urogenital system.     

Climate change and temperature-dependent sex determination: can individual plasticity in nesting phenology prevent extreme sex ratios?

Under temperature-dependent sex determination (TSD), temperatures experienced by embryos during development determine the sex of the offspring. Consequently, populations of organisms with TSD have the potential to be strongly impacted by climatic warming that could bias offspring sex ratio, a fundamental demographic parameter involved in population dynamics. Moreover, many taxa with TSD are imperiled, so research on this phenomenon, particularly long-term field study, has assumed great urgency. Recently, turtles with TSD have joined the diverse list of taxa that have demonstrated population-level changes in breeding phenology in response to recent climate change. This raises the possibility that any adverse impacts of climate change on populations may be alleviated by individual plasticity in nesting phenology. Here, we examine data from a long-term study on a population of painted turtles (Chrysemys picta) to determine whether changes in phenology are due to individual plasticity and whether individual plasticity in the timing of nesting has the capacity to offset the sex ratio effects of a rise in climatic temperature. We find that individual females show plasticity in the date of first nesting each year, and that this plasticity depends on the climate from the previous winter. First nesting date is not repeatable within individuals, suggesting that it would not respond to selection. Sex ratios of hatchlings within a nest declined nonsignificantly over the nesting season. However, small increases in summer temperature had a much stronger effect on nest sex ratios than did laying nests earlier in the season. For this and other reasons, it seems unlikely that individual plasticity in the timing of nesting will offset the effects of climate change on sex ratios in this population, and we hypothesize that this conclusion applies to other populations with TSD.     

How rapidly can maternal behavior affecting primary sex ratio evolve in a reptile with environmental sex determination?

Theoretical models identify maternal behavior as critical for the maintenance and evolution of sex ratios in organisms with environmental sex determination (ESD). Maternal choice of nest site is generally thought to respond more rapidly to sex ratio selection than environmental sensitivity of offspring sex (threshold temperatures) in reptiles with temperature-dependent sex determination (TSD, a form of ESD). However, knowledge of the evolutionary potential for either of these traits in a field setting is limited. I developed a simulation model using local climate data and observed levels of phenotypic variation for nest-site choice and threshold temperatures in painted turtles (Chrysemys picta) with TSD. Both nest-site choice and threshold temperatures, and hence sex ratios, evolved slowly to simulated climate change scenarios. In contrast to expectations from previous models, nest-site choice evolved more slowly than threshold temperatures because of large climatic effects on nest temperatures and indirect selection on maternally expressed traits. A variant of the model, assuming inheritance of nest-site choice through natal imprinting, demonstrated that natal imprinting inhibited adaptive responses in female nest-site choice to climate change. These results predict that females have relatively low potential to adaptively adjust sex ratios through nest-site choice.     

Bird-nest puzzle: can the study of unisexual flowers such as cucumber solve the problem of plant sex determination?

Unisexual flower development has long been used as a model system to understand the mechanism of plant sex determination. However, based on our investigation of the mechanisms regulating the development of unisexual cucumber flowers, we have realized that understanding how organ development is inhibited may not necessarily reveal how an organ is formed. We refer to this problem as a "bird-nest puzzle," meaning one cannot understand how a bird lays and hatches its eggs by understanding how its nest is ruined. To understand the biological significance of unisexual flowers, we reexamine the original meaning of sex and its application in plants. Additionally, we propose that the fundamental biological advantage for the selection and maintenance of unisexual flowers during evolution is to promote cross pollination.     

Plasticity of gene‐regulatory networks controlling sex determination: of masters,slaves, usual suspects,newcomers, and usurpators

Sexual dimorphism is one of the most pervasive and diverse features of animal morphology, physiology, and behavior. Despite the generality of the phenomenon itself, the mechanisms controlling how sex is determined differ considerably among various organismic groups, have evolved repeatedly and independently, and the underlying molecular pathways can change quickly during evolution. Even within closely related groups of organisms for which the development of gonads on the morphological, histological, and cell biological level is undistinguishable, the molecular control and the regulation of the factors involved in sex determination and gonad differentiation can be substantially different. The biological meaning of the high molecular plasticity of an otherwise common developmental program is unknown. While comparative studies suggest that the downstream effectors of sex‐determining pathways tend to be more stable than the triggering mechanisms at the top, it is still unclear how conserved the downstream networks are and how all components work together. After many years of stasis, when the molecular basis of sex determination was amenable only in the few classical model organisms (fly, worm, mouse), recently, sex‐determining genes from several animal species have been identified and new studies have elucidated some novel regulatory interactions and biological functions of the downstream network, particularly in vertebrates. These data have considerably changed our classical perception of a simple linear developmental cascade that makes the decision for the embryo to develop as male or female, and how it evolves.     

Is there a relationship between sex of cystic fibrosis carriers and sex ratio of their offspring?

Summary Data on the offspring of 198 aunts and 179 uncles of 100 cystic fibrosis index cases were analyzed. Aunts showed higher average number of liveborn sons than uncles. No significant difference was observed in the number of liveborn female offspring. When the sample was subdivided with respect to family size, the proportion of liveborn sons of aunts appeared higher than that of uncles in all classes.The present observations suggest that a female carrier may have a higher probability of male offspring than a male carrier and that she may be mainly responsible for the sex ratio deviations previously reported in sibships of cystic fibrosis patients.     

Predicting the fate of a living fossil: how will global warming affect sex determination and hatching phenology in tuatara?

How will climate change affect species'' reproduction and subsequent survival? In many egg-laying reptiles, the sex of offspring is determined by the temperature experienced during a critical period of embryonic development (temperature-dependent sex determination, TSD). Increasing air temperatures are likely to skew offspring sex ratios in the absence of evolutionary or plastic adaptation, hence we urgently require means for predicting the future distributions of species with TSD. Here we develop a mechanistic model that demonstrates how climate, soil and topography interact with physiology and nesting behaviour to determine sex ratios of tuatara, cold-climate reptiles from New Zealand with an unusual developmental biology. Under extreme regional climate change, all-male clutches would hatch at 100% of current nest sites of the rarest species, Sphenodon guntheri, by the mid-2080s. We show that tuatara could behaviourally compensate for the male-biasing effects of warmer air temperatures by nesting later in the season or selecting shaded nest sites. Later nesting is, however, an unlikely response to global warming, as many oviparous species are nesting earlier as the climate warms. Our approach allows the assessment of the thermal suitability of current reserves and future translocation sites for tuatara, and can be readily modified to predict climatic impacts on any species with TSD.     

Are homologies in vertebrate sex determination due to shared ancestry or to limited options?

The same candidate genes and the same autosomes are repeatedly used as sex chromosomes in vertebrates. Are these systems identical by descent, or are some genes or chromosomes intrinsically better at triggering the first steps of sex determination?     

Experimental evidence of masculinization by continuous illumination in a temperature sex determination teleost (Atherinopsidae) model: is oxidative stress involved?

The present study evaluates the influence of continuous light on phenotypic sex ratios in Chirostoma estor, a temperature sex determination animal model. Relative gene expression levels of 5 day old larvae were performed on two early gonad differentiation genes (sox9 and foxl2), two stress axis activation genes (gcr1 and crf) and four reactive oxygen species (ROS) antagonist effector genes (sod2, ucp2, gsr and cat). Two light treatments were applied from fertilization; control (12L:12D) simulated natural photoperiod and a continuous illumination photoperiod. By the end of the trial (12 weeks after hatching), differentiated and normal gonads were clearly identifiable in both treatments by histological observations. Regarding sex ratio, 73% of phenotypic males were found in continuous illumination compared with 40% in controls. Consistently, the sox9 gene (involved in early testis differentiation) showed an over expression in 64% of the individual larvae analysed compared with foxl2 (ovarian differentiation) suggesting a masculinization tendency in continuous illumination. On the other hand, only 36% of individuals showed the same tendency in the control treatment consistent with phenotypic sex ratios found under normal culture conditions. Relative gene expression results did not show significant difference in sod2, ucp2 and gcr1 levels, but cat, gsr and crf showed significantly higher expression levels in the continuous illumination treatment suggesting that both, the stress axis and ROS response mechanisms were activated at this time. This study suggests, a link between continuous light, oxidative stress and environmental sex determination in vertebrates. However, further research is necessary to describe this possible upstream mechanism that may drive some aspects of sexual plasticity in vertebrates.