Sex-determining mechanisms in reptiles can be divided into two convenient classifications: genotypic (GSD) and environmental (ESD). While a number of types of GSD have been identified in a wide variety of reptilian taxa, the expression of ESD in the form of temperature-dependent sex determination (TSD) in three of the five major reptilian lineages has drawn considerable attention to this area of research. Increasing interest in sex-determining mechanisms in reptiles has resulted in many data, but much of this information is scattered throughout the literature and consequently difficult to interpret. It is known, however, that distinct sex chromosomes are absent in the tuatara and crocodilians, rare in amphisbaenians (worm lizards) and turtles, and common in lizards and snakes (but less than 20% of all species of living reptiles have been karyotyped). With less than 2 percent of all reptilian species examined, TSD apparently is absent in the tuatara, amphisbaenians and snakes; rare in lizards, frequent in turtles, and ubiquitous in crocodilians. Despite considerable inter- and intraspecific variation in the threshold temperature (temperature producing a 1:1 sex ratio) of gonadal sex determination, this variation cannot confidently be assigned a genetic basis owing to uncontrolled environmental factors or to differences in experimental protocol among studies. Laboratory studies have identified the critical period of development during which gonadal sex determination occurs for at least a dozen species. There are striking similarities in this period among the major taxa with TSD. Examination of TSD in the field indicates that sex ratios of hatchlings are affected by location of the nests, because some nests produce both sexes whereas the majority produce only one sex. Still, more information is needed on how TSD operates under natural conditions in order to fully understand its ecological and conservation implications. TSD may be the ancestral sex-determining condition in reptiles, but this result remains tentative. Physiological investigations of TSD have clarified the roles of steroid hormones, various enzymes, and H-Y antigen in sexual differentiation, whereas molecular studies have identified several plausible candidates for sex-determining genes in species with TSD. This area of research promises to elucidate the mechanism of TSD in reptiles and will have obvious implications for understanding the basis of sex determination in other vertebrates. Experimental and comparative investigations of the potential adaptive significance of TSD appear equally promising, although much work remains to be performed. The distribution of TSD within and among the major reptilian lineages may be related to the life span of individuals of a species and to the biogeography of these species.(ABSTRACT TRUNCATED AT 400 WORDS)

Environmental sex determination in reptiles: ecology, evolution, and experimental design

New data on the genders of young turtles from eggs incubated at controlled temperatures demonstrate temperature-dependent sex determination (TSD) in 17 species surveyed for the first time and corroborate TSD in another 11 species. The well-known pattern of males from cool temperatures and females from warm ones (=Pattern Ia) occurs in eight species and may occur in seven more. A pattern of cool females, intermediate males, and warm females (=Pattern II) occurs in ten species. Data on three species surveyed for the first time are compatible with genetic sex determination (GSD). Within Clemmys, C. guttata has TSD; C. insculpta, GSD. Comparisons among phylogenetic sister groups suggest at least four independent losses of TSD in turtles. Large variation in extent of sexual differentiation at hatching among TSD species vs GSD species obscures any evidence that either system provides earlier or more complete differentiation. Pattern Ia occurs mainly in species in which adult females average larger than adult males; Pattern II occurs mainly in species with females smaller than males or in which body size is not dimorphic. Among TSD reptiles generally, the smaller gender typically arises at the coolest incubation temperatures. The new data, together with a literature survey, invite four possible explanations for various aspects of sex determination in reptiles: phylogenetic inertia, temperature-dependent differential fitness, sib-avoidance, and group-structured adaptation in sex ratios. Key demographic features from the literature include a high incidence of unisexuality within clutches and a predominance of female biases in sex ratios of hatchlings but not in those of adults. Each of these explanations remains partly but not fully plausible. Explanations for the patterns of sex determination may ultimately require a combination of hypotheses.

Sex Determination in Turtles: Diverse Patterns and Some Possible Adaptive Values

Half of the 22 extant crocodilians show evidence of temperature-dependent sex determination (TSD). We examine evidence for TSD in 11 species by reviewing reports on five and presenting new data for six. The female-male pattern (FM; females at low temperature, males at high temperature) attributed to Alligator mississippiensis and Caiman crocodilus are here revised to be female-male-female (FMF; males at intermediate temperature, females at low and high temperatures). A similar pattern characterizes Crocodylus palustris, C. moreletii, C. siamensis, and Gavialis gangeticus based on new data; published accounts establish a FMF pattern in Crocodylus porosus, C. johnstoni, and C. niloticus. TSD apparently occurs in Paleosuchus trigonatus and Alligator sinensis, but patterns are not yet documented. In the well-studied species, the incubation temperatures for FM transitions are congruent, but MF transition temperatures differ among species. In A. mississippiensis, 100% males are produced over a range of constant incubation temperatures, whereas in C. johnstoni, only low proportions of males are produced at any constant temperature.

The thermosensitive period (TSP) for A. mississippiensis occurs during stages 21 to 24 (days 30–45 at intermediate temperatures) and coincides with gonadal differentiation. A similar scenario is suggested in other species. The TSP in A. mississippiensis (and possibly other crocodilians) encompasses the third quarter of development and occurs later than in turtles and a lizard. In A. mississippiensis as in turtles, the duration (cumulative effect) and/or the magnitude (potency effect) of incubation temperatures during the TSP predictably alter sex ratios. TSP chronologies and features which are shared among TSD reptiles suggest common, underlying mechanisms; A. mississippiensis is an appropriate model for further study. In crocodilians, clutch effects are a significant source of variation in TSD response. Hatchling sex ratios previously reported for A. mississippiensis are reconsidered in light of our new data. © 1994 Wiley-Liss, Inc.

Temperature-dependent sex determination in crocodilians

Incubation temperature influences hatchling phenotypes such as sex, size, shape, color, behavior, and locomotor performance in many reptiles, and there is growing concern that global warming might adversely affect reptile populations by altering frequencies of hatchling phenotypes. Here I overview a recent theoretical model used to predict hatchling sex of reptiles with temperature-dependent sex determination. This model predicts that sex ratios will be fairly robust to moderate global warming as long as eggs experience substantial daily cyclic fluctuations in incubation temperatures so that embryos are exposed to temperatures that inhibit embryonic development for part of the day. I also review studies that examine the influence of incubation temperature on posthatch locomotion performance and growth because these are the traits that are likely to have the greatest effect on hatchling fitness. The majority of these studies used artificial constant-temperature incubation, but some have addressed fluctuating incubation temperature regimes. Although the number of studies is small, it appears that fluctuating temperatures may enhance hatchling locomotor performance. This finding should not be surprising, given that the majority of natural reptile nests are relatively shallow and therefore experience daily fluctuations in incubation temperature.

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Influence of Incubation Temperature on Hatchling Phenotype in Reptiles

Early environments can profoundly influence an organism in ways that persist over its life. In reptiles, early thermal environments (nest temperatures) can impact offspring phenotype and survival in important ways, yet we still lack an understanding of whether general trends exist and the magnitude of impact. Understanding these patterns is important in predicting how climate change will affect reptile populations and the role of phenotypic plasticity in buffering populations. We compiled data from 175 reptile studies to examine, and quantify, the effect of incubation temperature on phenotype and survival. Using meta-analytic approaches (standardized mean difference between incubation treatments, Hedges' g), we show that across all trait types examined there is, on average, a moderate to large magnitude of effect of incubation temperatures (absolute effect: |g| = 0.75). Unsurprisingly, this influence was extremely large for incubation duration, as predicted, with warmer temperatures decreasing incubation time overall (g = -8.42). Other trait types, including behaviour, physiology, morphology, performance, and survival experienced reduced, but still mostly moderate to large effects, with particularly strong effects on survival. Moreover, the impact of incubation temperature persisted at least one-year post-hatching, suggesting that these effects have the potential to impact fitness in the long term. The magnitude of effect increased as the change in temperature increased (e.g. 6°C versus 2°C) in almost all cases, and tended to decrease when temperatures of the treatments fluctuated around a mean temperature compared to when they were constant. The effect also depended on the mid-temperature of the comparison, but not in consistent ways, with some traits experiencing the greatest effects at extreme temperatures, while others did not. The highly heterogeneous nature of the effects we observe, along with a large amount of unexplained variability, indicates that the shape of reaction norms between phenotype and temperature, along with ecological and/or experimental factors, are important when considering general patterns. Our analyses provide new insights into the effects of incubation environments on reptile phenotype and survival and allow general, albeit coarse, predictions for taxa experiencing warming nest temperatures under climatic change.

Developmental temperatures and phenotypic plasticity in reptiles: a systematic review and meta-analysis.

A demographic study of the Nile crocodile Crocodylus niloticus at Lake Ngezi, Zimbabwe, revealed that females predominated in all size classes and among embryos. The sex of C. niloticus was shown to be determined by the temperature of egg incubation in constant temperature laboratory experiments. At 31 °C and below only females were produced. The threshold temperature for maleness was between 31 ° and 34 °C, but appeared to vary between clutches. The duration of the incubation period varied with temperature and was 110 days at 28 °C, falling to 85 days at 34 °C. Incubation temperature affected hatchling length, but not mass. Hatchlings from incubation at 34 °C were shorter on average than those from incubation at 28 °C and 31 °C, but by three months had outgrown them. There was no sex-related difference in length in a random sample of 200 two-year-old C. niloticus on a crocodile farm. Mean temperatures in wild nests were consistently lower than 31 °C and therefore the male threshold as determined in the laboratory. Embryonic development was slow and hatching success poor. The shallowest eggs in a nest had higher mean temperatures and more advanced embryos than the deepest eggs. They also experienced daily temperature fluctuations of up to 10 °C during which the maximum occasionally rose to 35 °C. Constant temperature incubation was not a good model of field conditions, but the correlation between nest temperatures and embryonic sex is consistent with temperature-dependent sex determination in the wild.

J. M. Hutton

Papers

Incubation temperatures, sex ratios and sex determination in a population of Nile crocodiles (Crocodylus niloticus)