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

Among reptiles that show temperature-dependent sex determination, sex ratios vary across constant incubation temperatures in ways sufficiently predictable to allow classifica- tion into patterns. One common pattern shows low temperatures yielding only males and high temperatures yielding only females. Another common pattern has low as well as high tempera- tures yielding only or mostly females and some intermediate temperatures yielding mostly males. Patterns tend to be associated with the direction of sexual dimorphism in adult size, especially for species with strong dimorphism. Pivotal temperatures (those yielding 1:l sex ratios) within the best-documented species and genera tend to increase with both latitude and longitude across central and southern North America. These geographic trends probably reflect factors that affect nest temperatures (duration of grow- ing season, insolation, and prevailing amounts of shading by vegetation). Data from a population of the alligator snapping turtle (Macroclemys temminckii) suggest that some embryos are temperature-independent females because these individuals become females even when they are shifted among male-producing temperatures during development. These indi- viduals are also more frequent in clutches of small eggs. In this and several other species, no constant incubation temperatures yield more than 75% males. 0 1994 WiIey-Liss, Inc.

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Patterns of temperature‐dependent sex determination in turtles

The various patterns of environmental sex determination in squamates, chelonians and crocodilians are described. High temperatures produce males in lizards and crocodiles but females in chelonians. Original experiments on the effects of incubation at 30 degrees C (100% females) or 33 degrees C (100% males) on development in Alligator mississippiensis are described. These include an investigation of the effect of exposing embryos briefly to a different incubation temperature on the sex ratio at hatching, and a study of the effects of 30 degrees C and 33 degrees C on growth and development of alligator embryos and gonads. A 7-day pulse of one temperature on the background of another was insufficient to alter the sex ratio dramatically. Incubation at 33 degrees C increased the rate of growth and development of alligator embryos. In particular, differentiation of the gonad at 33 degrees C was enhanced compared with 30 degrees C. A hypothesis is developed to explain the mechanism of temperature-dependent sex determination (TSD) in crocodilians. The processes of primary sex differentiation are considered to involve exposure to a dose of some male-determining factor during a specific quantum of developmental time during early incubation. The gene that encodes for the male-determining factor is considered to have an optimum temperature (33 degrees C). Any change in the temperature affects the expression of this gene and affects the dose or quantum embryos are exposed to. In these cases there is production of females by default. The phylogenetic implications of TSD for crocodilians, and reptiles in particular, are related to the life history of the animal from conception to sexual maturity. Those animals that develop under optimal conditions grow fastest and largest and become male. A general association between the size of an animal and its sex is proposed for several types of vertebrate.

Environmental regulation of sex determination in reptiles.

Incubation temperature has a direct effect on sex determination of the desert tortoise. Low temperatures (26.0-30.6 C) produce males and high temperatures (32.8-35.3 C) produce females. Pivotal temperature is approximately 31.8 C. Macroscopic and microscopic anatomy of the gonads is similar to that of other turtles. Hatching success and survival is very good between 28.1 and 32.8 C in dry sand (-5000 kPa). Incubation at 35.3 C is lethal for 72% of the eggs and produces weak hatchlings that die within 45 days. Wet sand (-5 kPa) is lethal for desert tortoise eggs. Hatchling size was dependent upon egg size and incubation condition. Hatchlings from eggs incubated at 32.8 and 35.3 C were significantly smaller than hatchlings from eggs incubated at 28.1 and 30.6 C. Hatching mass had no effect on growth rate of hatchlings. Thus, large eggs produced large hatchlings that were larger than their siblings at 120 days of age. Hatchlings from

Effects of incubation conditions on sex determination, hatching success, and growth of hatchling desert tortoises, gopherus agassizii

Mean daily temperature in natural nests of freshwater turtles with temperature-dependent sex determination is known to be a poor predictor of hatchling sex ratios when nest temperatures fluctuate. To account for this, a model was developed on the assumption that females will emerge from eggs when more than half of embryonic development occurs above the threshold temperature for sex determination rather than from eggs that spend more than half their time above the threshold. The model is consistent with previously published data and in particular explains the phenomenon whereby the mean temperature that best distinguishes between male and female nests decreases with increasing variability in nest temperature. The model, if verified by controlled experiments, has important implications for our understanding of temperature-dependent sex determination in natural nests. Both mean nest temperature and “hours spent above the threshold” will be poor predictors of hatchling sex ratios. Studies designed to investigate latitudinal trends and inter-specific differences in the threshold temperature will need to consider latitudinal and inter-specific variation in the magnitude of diel fluctuations in nest temperature, and variation in factors influencing the magnitude of those fluctuations, such as nest depth. Furthermore, any factor that modifies the relationship between developmental rate and temperature can be expected to influence hatchling sex ratios in natural nests, especially when nest temperatures are close to the threshold.

Tania M. S. Danni

Papers

Temperature-Dependent Sex Determination in Podocnemis expansa (Testudinata: Pelomedusidae)