Incubation temperature affects the behavior of adult leopard geckos (Eublepharis macularius)

doi:10.1016/0031-9384(94)90389-1

Physiology & Behavior

Volume 55, Issue 6, June 1994, Pages 1067-1072

https://doi.org/10.1016/0031-9384(94)90389-1 Get rights and content

Abstract

The leopard gecko has temperature-dependent sex determination (TSD); females are predominantly produced when incubated at 26°C (100%), 30°C (70%), and 34°C (95%), whereas males are predominantly produced at 32.5°C (75%). Exogenous estradiol can override the effect of temperature on sex determination. To compare temperature-determined females with hormone-determined females, eggs from the male-biased temperature were treated with estradiol benzoate during incubation. As adults, animals from a male-biased incubation temperature were more likely to exhibit aggression than animals from female-biased incubation temperatures. Furthermore, females from a male-biased incubation temperature tended to be less attractive than females from female-biased temperatures. Hormone-determined females were both attractive and aggressive. This suggests that incubation temperature is an important developmental determinant of adult aggressiveness and attractiveness. The 26°C animals ovariectomized on the day of hatch exhibited more frequent aggression and were unreceptive to males, indicating that postnatal ovarian hormones also play a role in adult sociosexual behaviors. The parallel between incubation temperature and intrauterine position in laboratory mammals is discussed.

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Cited by (93)

The evolutionary history of an accidental model organism, the leopard gecko Eublepharis macularius (Squamata: Eublepharidae)
2022, Molecular Phylogenetics and Evolution
The leopard gecko, Eublepharis macularius, is a widely used model organism in laboratory and experimental studies. The high phenotypic diversity in the pet trade, the fact that the provenance of different breeding lines is unknown, and that distinct Eublepharis species are known to hybridize, implies that the continued use of E. macularius as a model requires clarity on the origin of the lineages in the pet trade. We combine multi-locus sequence data and the first range-wide sampling of the genus Eublepharis to reconstruct the evolutionary history of the Eublepharidae and Eublepharis, with an updated time-tree for the Eublepharidae. Our sampling includes five of the six recognized species and additional nominal taxa of uncertain status comprising 43 samples from 34 localities plus 48 pet-trade samples. The Eublepharidae began diversifying in the Cretaceous. Eublepharis split from its sister genera in Africa in the Palaeocene-Eocene, and began diversifying in the Oligocene-Miocene, with late Miocene-Pliocene cladogenesis giving rise to extant species. The current species diversity within this group is moderately underestimated. Our species delimitation suggests 10 species with four potentially unnamed divergent lineages in Iran, India and Pakistan. All 30 individuals of E. macularius that we sampled from the pet trade, which include diverse morphotypes, come from a few shallow E. macularius clades, confirming that lab and pet trade strains are part of a single taxon. One of the wild-caught haplotypes of E. macularius, from near Karachi, Pakistan, is identical to (10) pet-trade samples and all other captive populations are closely related to wild-caught animals from central/southern Pakistan (0.1–0.5 % minimum pairwise uncorrected ND2 sequence divergence).
Clinical Reptile Behavior
2021, Veterinary Clinics of North America - Exotic Animal Practice
Epigenetic regulation of gonadal and brain aromatase expression in a cichlid fish with environmental sex determination
2020, General and Comparative Endocrinology
Citation Excerpt :
Exposure to masculinizing (high) temperatures also increases brain aromatase expression in the Mozambique tilapia Oreochromis mossambicus (Tsai et al., 2003). The degree to which within-sex variation in methylation impacts phenotypic variation is unknown, but exposure to sex-biasing temperatures also produces within-sex effects on sexual and territorial behaviors in the leopard gecko Eublepharis macularius (Flores et al., 1994; Rhen and Crews, 1999; Tsai et al., 2003). Here we examine the epigenetic underpinnings of sex and male morph determination in a West African cichlid fish, Pelvicachromis pulcher, in which more acidic conditions during the first 30 days of development result in a more male-biased adult sex ratio (Heiligenberg, 1965; Reddon and Hurd, 2013).
A fit animal must develop testes or ovaries, with brain and physiology to match. In species with alternative male morphs this coordination of development across tissues operates within sexes as well as between. For Pelvicachromis pulcher, an African cichlid in which early pH exposure influences both sex and alternative male morph, we sequence both copies of aromatase (cyp19a1), a key gene for sex determination. We analyze gene expression and epigenetic state, comparing gonad and brain tissue from females, alternative male morphs, and fry. Relative to brain, we find elevated expression of the A-copy in the ovaries but not testes. Methylation analysis suggests strong epigenetic regulation, with one region specifying sex and another specifying tissue. We find elevated brain expression of the B-copy with no sex or male morph differences. B-copy methylation follows that of the A-copy rather than corresponding to B-copy expression. In 30-day old fry, we see elevated B-copy expression in the head, but we do not see the expected elevated A-copy expression in the trunk that would reflect ovarian development. Interestingly, the A-copy epialleles that distinguish ovaries from testes are among the most explanatory patterns for variation among fry, suggesting epigenetic marking of sex prior to differentiation and thus laying the groundwork for mechanistic studies of epigenetic regulation of sex and morph differentiation.
Ultraviolet reflectance and pattern properties in leopard geckos (Eublepharis macularius)
2020, Behavioural Processes
Citation Excerpt :
We defined the age categories according to Landová et al. (2013): juveniles (striped pattern) 0–90 days old, subadults (adult-like pattern) 90–450 days old, and adults (fully disruptive coloration) more than 450 days old. The studied species has temperature-dependent sex determination (Viets et al., 1993), and the incubation temperature may also affect behavioral traits of these animals (cf. Flores et al., 1994; Sakata and Crews, 2004). To avoid the possible bias towards hatching non-territorial females, we set the incubation temperature to 28.5 °C ± 0.5, which is close to the temperature (approximately 29 °C) preferred by females of E. macularius for egg laying (Bull et al., 1988; Bragg et al., 2000).
Complex visual signaling through various combinations of colors and patterns has been well documented in a number of diurnal reptiles. However, there are many nocturnal species with highly sensitive vision, being able to discriminate colors in night conditions, as was shown in geckos. Because of their sensitivity to chromatic signals, including UV (ultraviolet), they may have potential hidden features in their coloration, which may play role in intraspecific communication (e.g. mate choice) or interspecific signals (e.g. antipredatory function). We explored this hypothesis in nocturnal Leopard geckos (Eublepharis macularius), a species using visual signals in both antipredation defense and courtship, having ontogenetic color change accompanied by a shift in behavior. We used UV photography and visual modeling in order to compare various aspects of their coloration (luminance, contrast, color proportions) between sexes, age groups and populations. We found that Leopard geckos have considerable UV reflectance in white patches on their tails (and on the head in juveniles). Though, no prominent differences were detected in their coloration between various groups. We hypothesize that the limitation of UV reflectance to the head and tail, which are both actively displayed during defense, especially in juveniles, might potentially boost the effect of antipredation signaling.
Mechanisms related to sexual determination by temperature in reptiles
2019, Journal of Thermal Biology
A number of strategies have emerged that appear to relate to the evolution of mechanisms for sexual determination in vertebrates, among which are genetic sex determination caused by sex chromosomes and environmental sex determination, where environmental factors influence the phenotype of the sex of an individual. Within the reptile group, some orders such as: Chelonia, Crocodylia, Squamata and Rhynchocephalia, manifest one of the most intriguing and exciting environmental sexual determination mechanisms that exists, comprising temperature-dependent sex determination (TSD), where the temperature of incubation that the embryo experiences during its development is fundamental to establishing the sex of the individual. This makes them an excellent model for the study of sexual determination at the molecular, cellular and physiological level, as well as in terms of their implications at an evolutionary and ecological level. There are different hypotheses concerning how this process is triggered and this review aims to describe any new contributions to particular TSD hypotheses, analyzing them from the “eco-evo-devo” perspective.
Hormonal and thermal induction of sex reversal in the bearded dragon (Pogona vitticeps, Agamidae)
2017, Zoologischer Anzeiger
Citation Excerpt :
The phenotypic changes described in the thermally-induced ZZ females (Li et al., 2016) when compared with ZW females may be attributed to their male-typical genotype, i.e. to the lack of the W chromosome, but also to permanent phenotypic changes induced by high incubation temperature. Such permanent shifts in behavioural traits, including sex-specific behaviour, were reported in both GSD and ESD lizards (Flores et al., 1994; Trnik et al., 2011). To disentangle what is the effect of sex-specific genotype and what is the effect of extreme incubation temperature, a manipulation enabling sex reversal at lower temperatures enabling production of hatching of both sexes is needed.
In amniotes (mammals, reptiles and birds) we can find two major sex-determining modes: environmental sex determination (ESD), largely in the form of temperature-dependent sex determination, and genotypic sex determination (GSD). It is evident that in reptiles there were multiple transitions between these two modes, but their directions are often difficult to reconstruct. However, it seems that GSD to ESD transitions were much less frequent. Such a transition demands production of sex-reversed individuals, i.e. individuals with a mismatch between gonadal and genotypic sex, which have to be viable and fertile in spite of lacking sex-specific parts of genomes linked to Y or W chromosomes. Up to now, there is only a single well-documented transition from the ancestral GSD to ESD among amniotes: a laboratory experiment with the bearded dragon, Pogona vitticeps. The gonadal females with male-typical ZZ genotype induced by high incubation temperatures in this species possessed masculinized morphology and behaviour. However, it is not clear whether these masculinized phenotypic traits can be attributed to the lack of female-specific W chromosome, or to extreme incubation temperatures. In this contribution, we describe the results of the experiments aiming to develop a system allowing disentangling the effects of temperature and genotype by hormonal manipulations, specifically by the application of fadrozole and exogenous estradiol (E₂) to developing eggs in a captive bred population of the bearded dragon. We documented that both high incubation temperature and E₂ application at normal incubation temperature can induce development of ZZ sex-reversed females in this laboratory population and that these females are able to lay eggs. On the other hand, the application of fadrozole led either to high hatchling mortality or to development of individuals with enlarged hemipenes, but did not induce sex reversal. The developed system will be useful in future studies to fully utilize the very valuable bearded dragon model for general understanding of potential limits and constraints of GSD to ESD transitions.

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Physiology & Behavior

Abstract

References (19)

A quantitative study of serum testosterone, sex accessory organ growth, and the development of intermale aggression in the mouse

Horm. Behav.

Concentrations of sex steroid hormones in pregnant and fetal Mongolian gerbils

Physiol. Behav.

Effects of intrauterine position on rate of sexual development in female Mongolian gerbils

Physiol. Behav.

Estrogen and sex reversal in turtles: Dosages producing both sexes produce few intersexes

Gen. Comp. Endocrinol.

Role des informations olfactives et visuelles dans la discrimination du sexe chez deux éspeces de Geckos nocturnes: Eublepharis macularius et Paroedura pictus

Biol. Behav.

Behavioral endocrinology and reproduction: An evolutionary perspective

The organizational concept and vertebrates without sex chromosomes

Brain Behav. Evol.

Paradoxical effects on brain differentiation

Neuroendocrinology

Embryonic temperature determines adult sexuality in a reptile

Nature

Cited by (93)

The evolutionary history of an accidental model organism, the leopard gecko Eublepharis macularius (Squamata: Eublepharidae)

Clinical Reptile Behavior

Epigenetic regulation of gonadal and brain aromatase expression in a cichlid fish with environmental sex determination

Ultraviolet reflectance and pattern properties in leopard geckos (Eublepharis macularius)

Mechanisms related to sexual determination by temperature in reptiles

Hormonal and thermal induction of sex reversal in the bearded dragon (Pogona vitticeps, Agamidae)

ArticleIncubation temperature affects the behavior of adult leopard geckos (Eublepharis macularius)

Abstract

Horm. Behav.

Physiol. Behav.

Physiol. Behav.

Gen. Comp. Endocrinol.

Role des informations olfactives et visuelles dans la discrimination du sexe chez deux éspeces de Geckos nocturnes: Eublepharis macularius et Paroedura pictus

Biol. Behav.

Behavioral endocrinology and reproduction: An evolutionary perspective

The organizational concept and vertebrates without sex chromosomes

Brain Behav. Evol.

Paradoxical effects on brain differentiation

Neuroendocrinology

Embryonic temperature determines adult sexuality in a reptile

Nature

Article
Incubation temperature affects the behavior of adult leopard geckos (Eublepharis macularius)