Thermal regimes during incubation do not affect mean selected temperatures of hatchling lizards (Bassiana duperreyi, Scincidae)

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Abstract

Incubation temperatures profoundly affect many phenotypic traits of squamate reptiles, and mean selected body temperatures of such animals also are plastic in response to environmental factors. Plausibly, then, incubation temperatures might affect hatchling thermoregulation, either via adaptation (i.e., populations that historically experience different nest conditions, also will diverge in hatchling thermoregulatory behaviour) or phenotypic plasticity (incubation temperatures directly modify hatchling behaviours). We tested this hypothesis with a montane scincid lizard (Bassiana duperreyi), using thermal-imaging methods to quantify temperatures (of both head and body) selected by hatchling lizards. The young lizards kept their heads cooler than their bodies, but mean selected temperatures did not differ among hatchlings from three populations with differing thermal regimes in natural nests, nor were they affected by thermal conditions during incubation. The conservatism of mean selected temperatures stands in strong contrast to the lability of many other phenotypic traits in response to incubation temperatures in this species.

Introduction

Ambient thermal heterogeneity plays a central role in the life of terrestrial ectotherms. Because temperature determines the rate of many chemical reactions (and thus, physiological processes), organismal performance typically depends upon body temperature (Du et al., 2000; Angilletta et al., 2002; Zhang and Ji, 2004) and ambient thermal regimes can substantially affect developmental rates and trajectories (Johnston and Bennett, 1996; Trudgill et al., 2005). Largely lacking the metabolic capacity to regulate their own temperatures, most squamate reptiles instead use behavioural thermoregulation to maintain temperatures within a range much narrower than that available within the environment (Avery, 1982). Overall, ambient thermal regimes thus can affect ectotherms both directly (by modifying phenotypic traits like performance and development) and by inducing behavioural responses (like basking or shade-seeking). The interplay between these two types of thermal influence defines many of the key biological features of squamate reptiles.

One life-history stage of particular interest involves the eggs of oviparous species. These immobile entities have no ability to thermoregulate behaviourally, so must develop under the thermal regimes of the nest-site that was selected by their mother. Extensive experimental work has shown that even minor details of those thermal regimes can influence a wide array of phenotypic traits of the hatchlings that emerge: for example, incubation temperatures can modify a hatchling reptile’s sex, body size, body shape, colour, activity level, locomotor performance, and antipredator tactics (Deeming, 2004). Behavioural selection of body temperatures also displays immense plasticity, with mean selected temperatures being modified by factors such as feeding regimes, reproductive state, predator scent, and prior thermal experience (Brown and Griffin, 2005; Gerald and Spezzano, 2005; Goodman and Walguarnery, 2007; Lin et al., 2008). This plasticity suggests that incubation regimes also might influence thermoregulatory tactics of the offspring, and indeed such effects have been reported in reptiles. For example, neonatal snakes (Nerodia sipedon) from cool-incubated eggs selected lower body temperatures than did their warmer-incubated siblings (Blouin-Demers et al., 2000).

Ambient thermal regimes inside natural nests might influence the thermoregulatory tactics of hatchling reptiles via two discrete processes that operate over different timescales. First, optimality theory suggests that reaction norms for embryonic development should evolve to match the conditions that animals normally experience; and thus, two populations that differ in nest thermal regimes might well produce hatchlings with an evolved divergence in thermal behaviour (and hence, potentially, in mean selected temperatures). Alternatively (or additionally), nest temperatures might directly affect hatchling phenotypes for thermoregulatory behaviour (as they do for many other traits: see above), in which case we expect divergent thermoregulatory tactics as a direct (developmentally plastic) response to different incubation regimes.

To test these predictions, we need a study system with (a) multiple populations experiencing consistently different thermal regimes inside the nest; (b) phenotypic plasticity induced by incubation conditions; and (c) a method of measuring thermal characteristics selected by hatchling (and thus, small) animals. We have taken advantage of a study system that confers these benefits: a montane lizard species for which our extensive prior studies show (a) among-population divergence in field nest temperatures, and (b) high plasticity in hatchling phenotypes as a consequence of nest temperatures; and we have used thermal imaging methods to measure accurately the temperatures selected by very small (<0.4 g) hatchling lizards.

Section snippets

Study species and monitoring of field nests

The three-lined skink, Bassiana duperreyi, is a medium-sized scincid lizard (adults to 80 mm snout–vent length, SVL; hatchlings to 27 mm SVL) widely distributed through cool-climate habitats in south-eastern Australia (Cogger, 2000). Female Bassiana duperreyi produce a single clutch of three to nine eggs in communal nests under rocks or logs in open areas from late November to December. In the Brindabella Range of south-eastern Australia, we have studied populations of this species that nest in

Results

The within-individual variation of Tsel across the three readings per animal (mean variance: 8.2 for head temperature and 9.5 for body temperature) was lower than the between-individual variation (variance: 15.6 for head temperature and 19.1 for body temperature). The temperatures selected by hatchling lizards showed no significant association with population of origin, incubation treatment, or hatchling body mass. There was no trend for larger lizards to have higher or lower temperatures in

Discussion

In our study, neither adaptation (exposure to different thermal incubation regimes over evolutionary time) nor acclimation (exposure to different regimes during an individual's own egg stage) affected mean selected temperatures of these hatchling montane lizards. That conservatism – especially the lack of acclimation – stands in strong contrast to the results of previous experimental-incubation studies on this same lizard species, where the temperatures at which an egg is incubated affect the

Acknowledgements

We thank Hua Ye for assistance in the laboratory and Rory Telemeco for data and calculations on the temperatures of field nests. Ethics approval was provided by the University of Sydney Animal Ethics Committee. This work was supported by grants from the University of Sydney to W-G. Du and the Australian Research Council to R. Shine.

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