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International audience; Species that have sex determined by environmental conditions during development (i.e., environmental sex determination [ESD]) are especially vulnerable to environmental change, including altered stress levels, habitat loss, and species translocations. These factors can produce multigenerational trends in population size and eco-evolutionary dynamics not captured by existing theory based on lifetime reproductive success (R0). Here, we extend ESD theory to use per capita growth rate r as a more appropriate measure of evolutionary success (fitness), and we demonstrate the importance of this change when males and females can differ in maturation times and when maturation times vary with local conditions (plasticity). In these cases, we show that primary and secondary sex ratios may be strongly biased; that optimal maturation times, when locally plastic, depend on the balance between mortality and growth effects; and that plasticity of maturation times can ameliorate fitness costs of increasing environmental stress

Four decades ago, it was proposed that environmental sex determination (ESD) evolves when individual fitness depends on the environment in a sex-specific fashion--a form of condition-dependent sex allocation. Many biological processes have been hypothesized to drive this sex asymmetry, yet a general explanation for the evolution of sex-determining mechanisms remains elusive. Here, we develop a mathematical model for a novel hypothesis of the evolution of ESD, and provide a first empirical test using data across turtles. ESD is favored when the sex-determining environment affects annual survival rates equivalently in males and females, and males and females mature at different ages. We compare this hypothesis to alternative hypotheses, and demonstrate how it captures a crucially different process. This maturation process arises naturally from common life histories and applies more broadly to condition-dependent sex allocation. Therefore, it has widespread implications for animal taxa. Across turtle species, ESD is associated with greater sex differences in the age at maturity compared to species without ESD, as predicted by our hypothesis. However, the effect is not statistically significant and will require expanded empirical investigation. Given variation among taxa in sex-specific age at maturity, our survival-to-maturity hypothesis may capture common selective forces on sex-determining mechanisms.

The Atlantic silverside, Menidia menidia (Pisces: Atherinidae), exhibits an exceptionally high level of clinal variation in sex determination across its geographic range. Previous work suggested linear changes in the level of temperature-dependent sex determination (TSD) with increasing latitude. Based on comparisons at 31 sites encompassing the entire species' range, we find that the change in level of TSD with latitude is instead highly nonlinear. The level of TSD is uniformly high in the south (Florida to New Jersey), then declines rapidly into the northern Gulf of Maine where genotypic sex determination (GSD) predominates and then rebounds to moderate levels of TSD in the northern-most populations of the Gulf of St. Lawrence. Major latitudinal breakpoints occur in central New Jersey (40(o)N) and the northern Gulf of Maine (44(o)N). No populations display pure TSD or GSD. Length of the growing season is the likely agent of selection driving variation in TSD with a threshold at 210 days. Because gene flow among populations is high, such distinct patterns of geographic variation in TSD/GSD are likely maintained by contemporary selection thereby demonstrating the adaptive fine tuning of sex determining mechanisms.

Why is the sex of many reptiles determined by the temperatures that these animals experience during embryogenesis, rather than by their genes? The Charnov-Bull model suggests that temperature-dependent sex determination (TSD) can enhance maternal fitness relative to genotypic sex determination (GSD) if offspring traits affect fitness differently for sons versus daughters and nest temperatures either determine or predict those offspring traits. Although potential pathways for such effects have attracted much speculation, empirical tests largely have been precluded by logistical constraints (i.e., long life spans and late maturation of most TSD reptiles). We experimentally tested four differential fitness models within the Charnov-Bull framework, using a short-lived, early-maturing Australian lizard (Amphibolurus muricatus) with TSD. Eggs from wild-caught females were incubated at a range of thermal regimes, and the resultant hatchlings raised in large outdoor enclosures. We applied an aromatase inhibitor to half the eggs to override thermal effects on sex determination, thus decoupling sex and incubation temperature. Based on relationships between incubation temperatures, hatching dates, morphology, growth, and survival of hatchlings in their first season, we were able to reject three of the four differential fitness models. First, matching offspring sex to egg size was not plausible because the relationship between egg (offspring) size and fitness was similar in the two sexes. Second, sex differences in optimal incubation temperatures were not evident, because (1) although incubation temperature influenced offspring phenotypes and growth, it did so in similar ways in sons versus daughters, and (2) the relationship between phenotypic traits and fitness was similar in the two sexes, at least during preadult life. We were unable to reject a fourth model, in which TSD enhances offspring fitness by generating seasonal shifts in offspring sex ratio: that is, TSD allows overproduction of daughters (the sex likely to benefit most from early hatching) early in the nesting season. In keeping with this model, hatching early in the season massively enhanced body size at the beginning of the first winter, albeit with a significant decline in probability of survival. Thus, the timing of hatching is likely to influence reproductive success in this short-lived, early maturing species; and this effect may well differ between the sexes.

Twenty years ago, Bulmer and Bull suggested that disruptive selection, produced by environmental fluctuations, can result in an evolutionary transition from environmental sex determination (ESD) to genetic sex determination (GSD). We investigated the feasibility of such a process, using mutation-limited adaptive dynamics and individual-based computer simulations. Our model describes the evolution of a reaction norm for sex determination in a metapopulation setting with partial migration and variation in an environmental variable both within and between local patches. The reaction norm represents the probability of becoming a female as a function of environmental state and was modeled as a sigmoid function with two parameters, one giving the location (i.e., the value of the environmental variable for which an individual has equal chance of becoming either sex) and the other giving the slope of the reaction norm for that environment. The slope can be interpreted as being set by the level of developmental noise in morph determination, with less noise giving a steeper slope and a more switchlike reaction norm. We found convergence stable reaction norms with intermediate to large amounts of developmental noise for conditions characterized by low migration rates, small differential competitive advantages between the sexes over environments, and little variation between individual environments within patches compared to variation between patches. We also considered reaction norms with the slope parameter constrained to a high value, corresponding to little developmental noise. For these we found evolutionary branching in the location parameter and a transition from ESD toward GSD, analogous to the original analysis by Bulmer and Bull. Further evolutionary change, including dominance evolution, produced a polymorphism acting as a GSD system with heterogamety. Our results point to the role of developmental noise in the evolution of sex determination.

Unlike birds and mammals, in many reptiles the temperature experienced by a developing embryo determines its gonadal sex. To understand how temperature-dependent sex determination (TSD) evolves, we must first determine the nature of genetic variation for sex ratio. Here, we analyze among-family variation for sex ratio in three TSD species: the American alligator (Alligator mississipiensis), the common snapping turtle (Chelydra serpentina) and the painted turtle (Chrysemys picta). Significant family effects and significant temperature effects were detected in all three species. In addition, family-by-temperature interactions were evident in the alligator and the snapping turtle, but not in the painted turtle. Overall, the among-family variation detected in this study indicates potential for sex-ratio evolution in at least three reptiles with TSD. Consequently, climate change scenarios that are posited on the presumption that sex-ratio evolution in TSD reptiles is genetically constrained may require reevaluation.

Models of environmental sex determination (ESD) usually assume that genetic influences on sex are polygenic, but the validity of this (or any other) form of genotype-environment interaction is virtually unknown. In the Atlantic silverside, Menidia menidia, sex is determined by an interaction between temperature and genotype and the response of sex ratio to temperature differs among populations from different latitudes. We examined the genetic basis of this pattern by measuring among family variation in the proportion of females, F/(F + M), within and among high (21°C) and low (15°C) temperatures for two populations: one from Nova Scotia (NS) where the level of ESD is low, and another from South Carolina (SC) where the level of ESD is high. In NS fish, temperature had a significant influence on sex ratio in only 1 of 23 families. The distribution of the fraction of females within temperatures for families from NS was highly heterogeneous and tended to fall into distinct classes (0.0, 0.25, 0.5, 1.0) like that expected from Mendelian segregation of a major sex factor(s). In contrast, temperature had a highly significant influence on sex ratio in all SC families examined (N = 24). Family sex ratios within temperatures were highly heterogeneous and, at least at 15°C, did not conform to simple Mendelian ratios. At 21°C, the proportion of females in most SC families was near zero and so the underlying sex tendencies of different families could not be discerned. Based on a previous study, mid-latitude fish appear to have an intermediate form of sex determination: simple Mendelian sex-ratio patterns exist and there is a moderate thermal influence on sex ratio in most but not all families. We suggest that sex determination in M. menidia is controlled by an interaction between major genetic factors, polygenic factors, and temperature and that the relative importance of each component differs with latitude. High latitude populations appear to have evolved a major sex-determining factor(s) that overrides the effect of temperature, and this factor(s) is lacking in low latitude populations.

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.

Although natural populations of most species exhibit a 1:1 sex ratio, biased sex ratios are known to be associated with non-Mendelian inheritance, as in sex-linked meiotic drive and cytoplasmic inheritance (Charnov 1982; Hurst 1993). We show how cultural inheritance, another type of non-Mendelian inheritance, can favor skewed primary sex ratios and propose that it may explain the female-biased sex ratios commonly observed in reptiles with environ- mental sex determination (ESD). Like cytoplasmic elements, cultural traits can be inherited through one sex. This, in turn, favors skewing the primary sex allocation in favor of the transmitting sex. Female nest-site philopatry is a sex- specific, culturally inherited trait in many reptiles with ESD and highly female-biased sex ratios. We propose that the association of nest-site selection with ESD facilitates the maternal manipulation of offspring sex ratios toward females.

In many species of plants, gender expression is correlated with size. Usually large plants are "more female" than small plants (Policansky 1981, 1987; Bierzychudek 1982, 1984a,b; Lovett Doust and Cavers 1982; Schlessman 1987, 1988, 1991; Pickering and Ash 1993), but the reverse is sometimes seen in wind pollinated species (see Burd and Allen 1988; de Jong and Klinkhamer 1994; Lundholm and Aarssen 1994). Models that predict evolutionarily stable sex ratios have been developed to explain this phenomenon (Freeman et al. 1980; Charnov 1982, ch. 4, 16; Lloyd 1983; Lloyd and Bawa 1984; Charnov and Bull 1985; Schlessman 1988; de Jong and Klinkhamer 1989, 1994; Bulmer 1994, ch. 10), and the majority of these are derived from Ghiselin's (1969) size-advantage hypothesis for sequential hermaphroditism in animals. This hypothesis postulates that the sexes each have different reproductive successes (RS) at different sizes, and that the sex whose relative rate of gain of RS with size is greatest should be expressed by large individuals. For example, if females gain RS more quickly with size than males, then large individuals should be female. Many of these models predict an abrupt transition from all male to all female allocation at a threshold size (i.e., diphasy; e.g., see Charnov 1982, ch. 4, and Schlessman 1988 for a review). When applying this hypothesis to flowering plants it is usually suggested that females have a higher energetic cost of reproduction relative to males as a result of the resource requirements for seed and fruit development (Bierzychudek 1984b; Lloyd and Bawa 1984; Schlessman 1988, 1991; de Jong and Klinkhamer 1994). Larger plants are believed to have greater resources or resource gathering potential and consequently, the increase in RS with size is greatest for females. Here we discuss a simple alternative evolutionary explanation that is frequently overlooked. Much available evidence suggests that mortality rate (per unit time) in plants is strongly correlated with size (Harper 1977; Gross 1981; Mithen et al. 1984; Silvertown and Lovett Doust 1993). The smallest plants in a population inevitably sustain the highest mortality rates, with mortality often declining substantially as size increases. Additionally, the female function of plants usually requires a longer reproductive time commitment relative to the male function as a result of the time required for fruit production. These two factors combine to create a selective regime promoting the evolution of a positive correlation between femaleness and size. The reasoning is simple. Suppose the smallest plants have the highest mortality rate. Then because the probability of dying early in the season is high when small, often there will not be sufficient time for female reproduction. The likelihood of reproductive success when small will be greater for males than females because pollen production and dispersal occur relatively fast. Thus, the female function will gain the most from an increase in size. Under this time-commitment hypothesis one would expect natural selection to favor the gender allocation rule, if small be male, if large be female. Although this prediction is the same qualitative one made by models based on energetic costs, it is not widely appreciated that this alternative explanation exists. Given that it is based on demographic and reproductive characteristics that appear to be quite common, we suggest that it deserves further attention. Additionally, we suggest that this time-commitment hypothesis can also explain instances of environmental sex determination (Charnov and Bull 1977), whereby plants in good quality sites are more female than plants in poor quality sites. From the above verbal argument however, it is difficult to determine whether diphasy or a graded gender transition is expected. Consequently, we present a simple mathematical model to address this question, and to clarify the conditions under which our verbal argument is valid. The model also allows a more detailed prediction of the expected pattern of gender expression and therefore suggests potential ways in which this hypothesis might be tested empirically.

Skewed sex ratios are common among several species of Poeciliopsis, a viviparous fish from northwestern Mexico. Since previous, unrelated studies from this laboratory (Angus and Schultz, 1983) suggested that deviation from a 1:1 sex ratio might be influenced by temperature, two inbred strains of P. lucida were tested for temperature-dependent sex determination by comparing sex ratios of offspring from pregnant females held at different water temperatures. Different sex ratios were produced by the two strains at the same temperature: one strain produced almost all-male offspring at 30°C and female-biased sex ratios at 24°C, while the other strain produced a 1:1 sex ratio at both temperatures. At intermediate temperatures, the labile strain produced sequentially fewer males with decreasing temperatures. The other strain produced a consistent sex ratio regardless of temperature. Poeciliopsis lucida apparently has a genetic polymorphism for temperature-influenced sex determination. An hypothesis is offered for the evolutionary origin of environmental sex determination.