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Developmental plasticity, the changes in the phenotype induced by the environment experienced by the developing embryo, is an important source of variation for many organismal traits that can influence individual fitness (West-Eberhardt, 2003). In most species of oviparous reptiles, females abandon their eggs after laying them in nests (Reynolds et al., 2002). In the absence of parental care, the thermal and hydric conditions inside reptile nests can vary markedly throughout the incubation period. For example, nest temperatures often fluctuate widely on a daily basis (Shine and Harlow, 1996; Andrews and Warner, 2002), and can vary depending on local weather conditions (Shine, 2004). In the last few decades, a large body of experimental research has demonstrated that incubation temperatures can influence a multitude of offspring traits, including sex, morphology, behavior, performance, and cognitive abilities (Deeming and Ferguson, 1991; Deeming, 2004; Noble et al., 2018; While et al., 2018). Some of these developmental effects can be long lasting, and can influence the growth and survival of offspring (Qualls and Andrews, 1999; Andrews et al., 2000; Dayananda et al., 2016) and may influence lifetime reproductive success (Warner and Shine, 2008). Thus, an understanding of thermal developmental plasticity can provide insights into how reptiles may cope with changing environments (Mitchell et al., 2008; Angilletta, 2009; Carlo et al., 2018).

Most research on thermal developmental plasticity has focused on how incubation temperatures affect morphological traits, physiology, sex ratios and incubation duration (While et al., 2018). By contrast, few studies have investigated whether incubation temperatures can also influence the thermal preferences or thermal tolerances of hatchlings (Lang, 1987; Blumberg et al., 2002; Du et al., 2010; Dayananda et al., 2017; Abayarathna et al., 2019; Refsnider et al., 2019). Most lizards maintain their body temperature (hereafter, T_b) within a preferred range by carefully selecting suitable microhabitats, altering their behavior, or by adjusting their posture, shape, or color (Huey, 1982). In turn, selected T_bs influence the physiology, behavior, performance, activity budgets, and growth of individuals, which can influence their survival and reproduction (Huey, 1982; Angilletta, 2009). Thus, incubation-induced plasticity in preferred body temperatures (T_pref) may have important fitness consequences for hatchling lizards. More broadly, an understanding of how incubation temperatures influence the T_pref of lizards is important for predicting how species may fare under future climates (Huey et al., 2012).

Experimental studies on lizards have found that incubation temperatures may affect the thermoregulatory behavior of hatchlings of some species, but not others (Du et al., 2010; Refsnider et al., 2019). For example, incubation temperatures did not affect the selected T_bs of hatchling veiled chameleons Chamaeleo calyptratus (Andrews, 2008), three lined skinks Bassiana duperreyi (Du et al., 2010), or Cuban rock iguanas Cyclura nubila (Alberts et al., 1997). By contrast, other studies reported the opposite effect. For example, in the Madagascar ground gecko, Paroedura pictus, hatchlings from hot incubation temperatures had higher dorsal temperatures prior to crossing between the cold and hot sides of a thermal shuttle apparatus (Blumberg et al., 2002). In Sceloporus virgatus, hatchlings from cold temperature incubation (15–25°C) selected higher T_bs, and maintained T_bs more precisely than hatchlings from hot temperature (20–30°C) incubation (Qualls and Andrews, 1999). In a study on Jacky dragons (Amphibolurus muricatus) using constant temperature incubation, hatchlings from the 28.1°C treatment had lower T_bs after 2 h in a thermal gradient than hatchlings from 25 or 32°C treatments (Esquerre et al., 2014). Despite evidence that incubation temperatures can affect the T_pref of hatchlings, it is unclear whether such incubation induced shifts are ecologically relevant, particularly if the effects are short lived or are masked by interactions with the post-hatching environment (Andrews et al., 2000; Buckley et al., 2007). For example, incubation-induced differences in T_pref of hatchlings might have little effect on subsequent growth or survival if lizards shift T_pref in response to food availability. In some lizards, individuals may elevate their T_pref after feeding, or may select cooler T_pref when food is scarce (Brown and Griffin, 2005). Such thermophilic responses to feeding might mask or swamp developmental shifts in thermoregulatory behavior. Hence, to understand the ecological significance of incubation-induced shifts in T_pref, we also need to assess whether other sources of variation such as feeding influence the T_pref of hatchlings.

In this study, we carried out an experiment to test whether thermal conditions during incubation affected the thermal preferences of hatchling velvet geckos, Amalosia lesueurii. Velvet geckos lay eggs communally in nest crevices, and maximum daily nest temperatures are positively correlated with maximum daily air temperatures (Dayananda et al., 2016). Thermal data collected from 21 nests in 2018–2019 revealed that the slope of the relationship between air temperature and nest temperature was greater than one in 24% of nests (Cuartas-Villa and Webb, 2021). Because the frequency and intensity of heatwaves is predicted to increase in future (Cowan et al., 2020; Trancoso et al., 2020), it is likely that some nests will become hotter in future. To determine how such changes might affect phenotypic traits of hatchlings, we incubated eggs under a “cold” (mean = 24.3°C, range 18.4–31.1°C) and “hot” treatment (mean = 28.9°C, range 19.1–38.1°C) to mimic current vs. potential future nest temperatures. We predicted that hatchlings from hot incubation should have higher T_pref than hatchlings from cold incubation; i.e., local adaptation hypothesis (Levinton, 1983). Our null hypothesis was that incubation temperature would not influence T_pref. However, it is possible that developmental shifts in T_pref might not be detectable if T_pref is influenced by environmental conditions in the post-hatching environment. To explore these hypotheses, we measured the preferred body temperatures of hatchlings in a cost-free thermal gradient. To assess whether feeding influenced gecko body temperatures, we measured the hatchling’s body temperatures after feeding and fasting.

Lizards from both hot and cold incubation treatments showed very similar patterns of thermoregulation (Figure 3), and had similar preferred T_bs before feeding (mean T_bs = 25.9 and 25.7°C, respectively) and after feeding (mean T_bs = 30.7 and 30.4°C, respectively). Both cold-incubated and hot-incubated lizards showed similar patterns of thermoregulation, with hatchlings maintaining higher body temperatures (T_bs) after midday than during the morning (Fig. 3). Lizard body temperatures varied significantly with hour of day [F₍₃._{4, 68}.₆₎ = 20.73, P < 0.01], but there was no interaction between hour and incubation treatment [F₍₃._{4, 85}.₄₎ = 2.25, P = 0.08] nor between feeding status, incubation treatment and hour [F₍₃._{4, 85}.₄₎ = 0.99, P = 0.42]. However, lizard feeding status significantly affected body temperatures, with lizards maintaining higher T_bs after feeding than prior to feeding [F₍₁,₂₀₎ = 206.78, P = 0.0001, Figure 3]. There was also a significant interaction between feeding status and hour [F₍₄._{3, 85}.₄₎ = 3.97, P = 0.004], reflecting the fact that at 10 a.m., 1 h after being placed in the gradient, body temperatures of fed and unfed lizards were similar (Figure 3). Thereafter, body temperatures of recently-fed lizards were higher than those of fasted lizards during each hour of the day (Figure 3). Lizards selected higher body temperatures in the thermal gradient after feeding (mean T_b = 30.6°C, IQR = 29.6–32.0°C, range = 23.5–35.5°C) than before feeding (mean T_b = 25.8°C, IQR = 24.7–26.9°C, range = 20.0–32.5°C). Overall, there was no significant effect of incubation treatment on hatchling T_bs [F_{(1, 20)} = 0.13, P = 0.73] and no interaction between feeding status and incubation treatment [F₍₁,₂₀₎ = 0.04, P = 0.84].

We predicted that hatchlings from the hot incubation treatment would select higher preferred body temperatures (T_pref) than hatchlings from the cold treatment. Contrary to our prediction, we found no evidence that incubation temperatures affected the thermal preferences of 4-week old hatchlings. Indeed, mean selected T_bs of cold- and hot-incubated hatchlings were very similar, as was the precision of thermoregulation (Figure 3). Although we measured body temperatures of hatchlings at age four weeks, our findings agree with the results of previous studies, which found no effect of incubation temperatures on selected T_bs of hatchlings during the 2 months of life in veiled chameleons Chamaeleo calyptratus (Andrews, 2008), and western fence lizards Sceloporus occidentalis (Buckley et al., 2007). Other studies reported no effect of incubation on selected T_bs of 1-week old three lined skinks Bassiana duperreyi (Du et al., 2010) or 14–16 month old Cuban rock iguanas Cyclura nubila (Alberts et al., 1997). By contrast, other studies have reported that incubation temperatures can influence the thermoregulatory behavior of hatchlings. For example, in western fence lizards hatchlings from a warm-incubation treatment thermoregulated more precisely than lizards from a cool-incubation treatment, and this effect persisted for at least seven weeks post hatching (Buckley et al., 2007). In the Madagascar ground gecko, Paroedura pictus, hatchlings from a hot incubation treatment maintained higher dorsal temperatures prior to crossing between the cold and hot sides of a thermal shuttle apparatus at night, and this effect persisted for several weeks after hatching (Blumberg et al., 2002). Studies on other ectotherms suggest that as for reptiles, the effects of developmental temperatures on preferred body temperatures are mixed (Dillon et al., 2009). For example, in some Drosophila species, flies reared at 25°C had higher T_pref than those reared at 20°C (Yamamoto and Ohba, 1984). In Drosophila melanogaster, adults selected lower temperatures when reared at 28°C than when reared at 19 or 25°C (Krstevska and Hoffmann, 1994). These mixed results suggest that like other traits, reaction norms for thermal preferences may be non-linear (Noble et al., 2018). Hence, we cannot rule out the possibility that intermediate incubation temperatures might affect preferred T_bs of velvet geckos. Future studies, using intermediate temperatures, and larger sample sizes, would help resolve this issue.

Ultimately, the biological relevance of incubation-induced shifts in preferred T_bs will depend on the magnitude and duration of such effects relative to other sources of environmental variation (Booth, 2018). Notably, several studies have shown that incubation-induced shifts in T_b are transitory, so are unlikely to influence traits linked to fitness (Buckley et al., 2007; Goodman and Walguarnery, 2007). In the present study, hatchlings maintained significantly higher T_bs after feeding (fed: mean T_b = 30.6°C; fasted mean T_b = 25.8°C), demonstrating that food availability has large effects on hatchling T_bs. Thermophilic responses to feeding are widespread in snakes (Blouin-Demers and Weatherhead, 2001) but are less common in lizards (Wall and Shine, 2008; Schuler et al., 2011). Notably, the 4.8°C increase in mean T_b of hatchling geckos after feeding is similar to that reported for snakes in thermal gradients (typically, increases of 2–6°C (Lysenko and Gillis, 1980; Slip and Shine, 1988; Tsai and Tu, 2005), but is higher than the 3.1°C increase reported for adults of our study species (Dayananda and Webb, 2020), or the modest increases (typically, <2°C), reported for lizards such as Heloderma suspectum (Gienger et al., 2013) and Anolis carolinensis (Brown and Griffin, 2005). Future studies on hatchlings of other lizard species in this respect, particularly geckos, would help to evaluate the generality of our results.

Why do fasted hatchlings select lower T_bs than recently fed individuals? After feeding, selection of higher T_bs likely maximizes digestive efficiency and rates of energy assimilation (Harlow et al., 1976; Beaupre et al., 1993). However, because metabolic rates scale with T_b, maintenance of high T_bs increases energy expenditure (Angilletta, 2009). Therefore, in the absence of food, hatchlings may select lower T_bs to reduce energy expenditure. Conserving energy might be particularly important for hatchlings, as they may lack sufficient energy reserves in their tails to survive long periods in the absence of food (Greer, 1989). Ultimately, shifts in T_b in response to food availability may represent a trade-off between energy conservation vs. maintenance of other fitness related behaviors (Huey, 1982). For example, adults of Yarrow’s spiny lizard Sceloporus jarrovi that were deprived of food for five days maintained high T_bs, presumably so they could maximize important fitness related behaviors such as territory defense (Schuler et al., 2011). In the wild, hatchling velvet geckos congregate under rocks near communal nest sites, and hatchlings often share rocks with conspecifics during the first few months of life (Webb, 2006), so territory defense may be unimportant during this period.

Irrespective of feeding status, hatchling geckos displayed diel variation in preferred T_bs. Hatchlings selected low T_bs in the morning, and thereafter they raised their T_b and maintained elevated temperatures throughout the afternoon (Figure 3). Similar diel patterns of thermoregulation were reported for individuals of two gecko species, Eublepharis macularius and Oedura marmorata, that were fasted for 3 days before being placed in a thermal gradient (Angilletta et al., 1999). Similarly, individuals of the gecko Tarentola mauritanica increased their T_bs during the day (Gill, 1994). The underlying cause for this pattern of thermoregulation in geckos is not known, but we note that T_bs of hatchling A. lesueurii follow the same pattern as rock temperatures; i.e., delayed heating, reaching a peak in early afternoon (Webb and Shine, 1998). Potentially, this pattern might represent an entrained circadian rhythm for activity or thermoregulation (Refinetti and Susalka, 1997; Tawa et al., 2014). Because hatchling geckos commence foraging shortly after dusk, maintaining high T_bs around dusk would aid in prey capture and potentially, escape from predators (Christian and Tracy, 1981). As for diurnal lizards, maintenance of high T_bs during daylight hours would facilitate physiological processes such as digestion, growth and sloughing (Huey, 1982; Angilletta et al., 1999).

In conclusion, we found no effects of incubation temperature on the thermal preference of hatchling velvet geckos. However, there was a strong effect of feeding status on the hatchlings thermal preference, suggesting that food availability may influence thermoregulation by hatchlings in the wild. To evaluate the role of thermal developmental plasticity on the thermal preferences of hatchling lizards, future studies should not only estimate the duration of such effects, but also, their magnitude relative to plasticity caused by the post-hatching environment.

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author/s.

The animal study was reviewed and approved by University of Technology Animal Care and Ethics Committee.

TA and JW contributed to conception, design of the study, contributed to manuscript revision, read, and approved the submitted and revised versions. TA carried out the experiments, wrote the first draft of the manuscript, and organized the database. JW performed the statistical analysis and edited the manuscript. Both authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.