A multi-trait evaluation of patterns and fitness consequences of breeding phenology plasticity with nocturnal warming and food restriction in a lizard

Théo Bodineau, Pierre de Villemereuil, Baptiste Lemaire, Simon Agostini, Beatriz Decencière, Matéo Millet, Sandrine Meylan, Jean-François Le Galliard

<figure><img src="image_1.png" /></figure>

To cite this version:

Théo Bodineau, Pierre de Villemereuil, Baptiste Lemaire, Simon Agostini, Beatriz Decencière, et al. A multi-trait evaluation of patterns and fitness consequences of breeding phenology plasticity with nocturnal warming and food restriction in a lizard. Functional Ecology, 2025, 10.1111/1365-2435.70030. hal-05012292

HAL Id: hal-05012292

https://hal.science/hal-05012292v1

Submitted on 31 Mar 2025

HAL is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_2.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
<figure><img src="image_3.png" /></figure>

<figure><img src="image_4.png" /></figure>

BRITISH
ECOLOGICAL
SOCIETY

Functional Ecology

RESEARCH ARTICLE

Phenology–Trait Relationships Across Different Scales and Organizational Levels

# A multi-trait evaluation of patterns and fitness consequences of breeding phenology plasticity with nocturnal warming and food restriction in a lizard

Théo Bodineau<fnref n="1" /> ID

Pierre de Villemereuil<fnref n="2" />,<fnref n="3" /> ID

Baptiste Lemaire<fnref n="1" /> ID

Simon Agostini<fnref n="4" />

Beatriz Decencière<fnref n="4" /> ID

Matéo Millet<fnref n="1" /> ID

Sandrine Meylan<fnref n="1" /> ID

Jean-François Le Galliard<fnref n="1" />,<fnref n="4" /> ID

**Correspondence**

Théo Bodineau
Email: theo.bodineau@gmail.com

**Funding information**

Agence Nationale de la Recherche

**Handling Editor:** Solveig Franziska Bucher

**Abstract**

1. Faced with climate warming, ectothermic species shift their breeding phenology, which is in part attributed to an acceleration of gestation or incubation in warmer environments. Thermal acceleration of gestation may have important fitness implications for breeding females and their offspring by impacting maternal homeostasis, embryonic development and hatching date, but these benefits and costs have been poorly documented. In addition, while climate change is characterised by a stronger trend for night-time than for daytime warming and concurrent alterations of food availability, few studies have quantified phenology-trait effects of increasing nocturnal temperatures and decreasing food intake.

2. Here, we exposed female common lizards (Zootoca vivipara) to contrasted nocturnal temperatures and prey availability during gestation. We investigated multiple traits to quantify the functional impacts of nocturnal warming and food availability on breeding phenology, maternal condition, physiology and behaviour, current reproductive output and both females and offspring life-history traits.

3. Nocturnal warming advanced parturition dates, but food restriction further accelerated gestation and females' muscle catabolism under moderate nocturnal warming. Nocturnal warming and food restriction during gestation had negative effects on reproductive output and increased physiological imbalances in breeding females. Hot nocturnal temperatures down-regulated basal corticosterone levels and immunocompetence, while food restriction reduced the antioxidant capacity of females.

4. The thermal acceleration of gestation induced by nocturnal warming had positive effects on offspring life-history traits related to fitness, such as endurance at birth and body growth during the first few months of life.

5. By analysing multiple traits, our study provides an integrated understanding of the intra- and intergenerational effects of nocturnal warming and resource

This is an open access article under the terms of the [Creative Commons Attribution-NonCommercial License](https://creativecommons.org/licenses/by-nc), which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

© 2025 The Author(s). *Functional Ecology* published by John Wiley & Sons Ltd on behalf of British Ecological Society.

<footnote n="1">¹Sorbonne Université, UPEC, UPCité, CNRS, INRAE, IRD, Institut d'Ecologie et des Sciences de l'Environnement de Paris (iEES Paris—UMR 7618), Paris, France</footnote>

<footnote n="2">²Institut de Systématique, Évolution, Biodiversité (ISYEB), École Pratique des Hautes Études, PSL, MNHN, CNRS, SU, UA, Paris, France</footnote>

<footnote n="3">³Institut Universitaire de France (IUF), France</footnote>

<footnote n="4">⁴École Normale Supérieure, PSL Research University, Département de Biologie, CNRS, UAR 3194, Centre de Recherche en Ecologie Expérimentale et Prédictive (CEREEP-Ecotron IleDeFrance), Saint-Pierre-lès-Nemours, France</footnote>
availability during gestation in a viviparous ectotherm. Our results underline the importance of considering nocturnal warming and resource availability as factors causing increased physiological imbalances and negative effects on ectotherm reproduction. They also show the need to consider the benefits and costs of phenological advances for breeding females and their offspring in order to improve our understanding of the consequences of phenological changes in the context of climate change.

KEYWORDS

ectotherm, food availability, nocturnal temperatures, performance, phenology, plasticity, reproductive costs, trade-off

# 1 | INTRODUCTION

Terrestrial ectotherms are among the most affected organisms by global warming because their metabolism, behavioural activity and life history are highly dependent on the thermal conditions in the environment (Duffy et al., 2022; Kingsolver, 1995; Sinervo et al., 2010). Faced with climate change, terrestrial ectotherms show marked phenological changes with emergence and breeding dates advancing by several days to several weeks per decade due to climate warming (Cohen et al., 2018; Thackeray et al., 2016; Vitasse et al., 2021). Although genetic adaptation can explain these phenological advances, phenotypic plasticity is the favoured hypothesis for ectotherms (Ljungström et al., 2015). Indeed, temperature affects essential biochemical processes (such as reaction kinetics, enzyme inactivation or hormone regulation) and behaviours (such as activity) that influence key events in the life history, such as spring emergence (Moss & MacLeod, 2022), reproduction timing and gestation (for viviparous species) or incubation length (for oviparous species) by influencing the speed of embryonic development (Noble et al., 2018). In particular, warmer developmental temperatures lead to a thermal acceleration of embryonic development and earlier hatching dates in a wide range of insects, amphibians and reptiles (Bradford, 1990; Noble et al., 2018; Rebaudo & Rabhi, 2018). Understanding the fitness consequences of this thermal plasticity of breeding phenology is, therefore, essential to anticipate demographic changes and vulnerability of ectothermic species exposed to climate warming.

In reptiles, thermal conditions during embryonic development can significantly influence offspring phenotype, survival and ontogenic trajectories (Booth, 2006; Noble et al., 2018; While et al., 2015). Incubation temperatures affect embryonic metabolism and the degree of conversion of yolk to tissue, which may influence body condition at birth (Pettersen et al., 2024; Storm & Angilletta Jr., 2007; Sun et al., 2015). In general, the effects of developmental temperature on embryo viability, post-hatching survival and offspring performance seem to follow a concave curve with lower performance values for offspring from colder and warmer incubation temperatures (Noble et al., 2018). In addition, earlier hatching dates induced by accelerated embryonic development at

warmer temperatures can increase postnatal survival, growth and recruitment ('early is better' hypothesis; Le Henanff et al., 2013; Li et al., 2018; Pearson & Warner, 2018; Uller & Olsson, 2010; Wapstra et al., 2010). Indeed, early hatching date can give the offspring a 'head start' thanks to more favourable environmental conditions (e.g. extended period before winter for growth and production of fat bodies, warmer temperatures and longer periods of activity in early summer, greater prey abundance) and to less competition between conspecifics early in life (reviewed in Warner & Shine, 2007).

Although warmer developmental temperatures and phenological advances may be generally beneficial to the offspring, the effects of accelerated breeding phenology on performance traits and fitness of females remain largely unknown. In reptiles, reproduction entails substantial changes in the mother's behaviour (e.g. activity budget, thermoregulatory behaviour, feeding), physiology and energy balance (Bleu et al., 2012; Shine, 1980) and, therefore, represents a critical life stage for energy and water balance, especially in viviparous species (Brusch et al., 2020; Dupoué et al., 2015; Lourdais et al., 2013). In addition to the direct allocation of energy and nutrients in egg formation, viviparity induces additional reproductive costs for the mother such as reduced locomotor performance, increased risk of predation and increased metabolic rate and energy expenditure during gestation (Foucart et al., 2014; Jara et al., 2019; Le Galliard et al., 2003; Van Dyke & Beaupre, 2011). Thermal acceleration of gestation may reduce such costs by decreasing the gestation length, but it could also lead to significant energy demands in viviparous species, affecting female body condition as well as the quality and output of reproduction (Brusch et al., 2020; Brusch IV et al., 2023). In addition, warmer temperatures during gestation could alter maternal homoeostasis by affecting key physiological processes such as the immunocompetence, the regulation of basal corticosterone secretion (the major glucocorticoid in reptiles) via the hypothalamo-pituitary-adrenal (HPA) axis and the regulation of redox balance (Wang et al., 2024). For example, exposure to high temperatures or heat waves can lead to an increase in basal corticosterone levels (Dezetter et al., 2022; Racic et al., 2020), an increase in oxidative stress (Costantini, 2014; Han et al., 2020), as well as down-regulation of the immunocompetence (Butler et al., 2013; Sacchi et al., 2017; Stahlschmidt et al., 2017; Zhang et al., 2023).
These effects of temperature on maternal homoeostasis appear to be quite variable across studies of reptiles and have rarely been studied during gestation (Ballen et al., 2012; Dupoué et al., 2018, 2020; Jessop et al., 2016). In addition, these physiological changes might have a significant impact on a wide range of fitness-related traits (Burraco et al., 2020; Dupoué et al., 2020; Graham et al., 2011; Love et al., 2013; Zhang et al., 2023), calling for multivariate studies investigating the behavioural, energetic and homeostatic consequences of the thermal plasticity of breeding phenology.

While recent climate change is characterised by a more rapid increase in nocturnal temperatures than daytime temperatures in most regions of the globe (Sadok & Jagadish, 2020; Vose et al., 2005; Zhong et al., 2023), few studies have quantified the effect of nocturnal warming on breeding phenology and fitness traits in ectotherms (reviewed in Rutschmann et al., 2024; Speights et al., 2017). High nocturnal temperatures can impact morphology, physiology and life-history strategies of ectotherms, such as body mass changes (Hodgson & Schwanz, 2024), basal corticosterone levels (Dupoué et al., 2018), evaporative water loss rates (Dupoué, Rutschmann, Le Galliard, Miles, et al., 2017), heating efficiency (Rutschmann et al., 2020), body growth rates (Rutschmann et al., 2021) and too high nocturnal warming can lead to population decline (Dupoué, Rutschmann, Le Galliard, Clobert, et al., 2017). In viviparous reptiles, nocturnal warming should accelerate gestation but could also increase reliance of reproductive females on energy or water intake due to increased metabolic rates and water loss rates at high nocturnal temperatures (Brusch IV et al., 2023; Clarke & Zani, 2012; Moore et al., 2020; Wu et al., 2012; Zhao et al., 2014). Thus, the consequences of nocturnal warming on energy budget and reproductive output of ectotherms should depend on the thermoregulation strategies of pregnant females as well as on resource availability (Rutschmann et al., 2024). In diurnal, perfectly thermoregulating species, it is predicted that reduced food intake shifts the optimal nocturnal temperature for net energy gain towards lower values because declining energy intake coupled with increased energetic expenditure during resting phases makes ectotherms less energetically tolerant of heat and leads to a 'metabolic meltdown' (Huey & Kingsolver, 2019; Rutschmann et al., 2024; Thomas et al., 2017). Furthermore, numerous field studies have documented concomitant changes in climate, primary production and prey abundance for many reptiles (Hallmann et al., 2017; Laws, 2017; Lister & Garcia, 2018), making it highly relevant to investigate the thermal plasticity of breeding phenology under different food conditions during gestation in ectotherms.

Here, we studied the effects of increasing nocturnal temperatures and decreasing prey availability on breeding females and life-history traits of their offspring in the viviparous common lizard (Zootoca vivipara, Lichenstein 1823). Using an experimental design, we exposed pregnant females to contrasted nocturnal temperatures (21°C, 16°C, 13°C) and food availability (ad libitum food or moderate food restriction) during gestation. We quantified behavioural and physiological responses of females by recording their activity and thermoregulation behaviours and measuring multivariate indicators of body condition,

immunocompetence and homeostasis (i.e. baseline corticosterone levels, oxidative damage and antioxidant capacity) throughout gestation. We also quantified reproductive output, offspring morphology and performance traits at birth and released females and juveniles into semi-natural enclosures to examine delayed effects of nocturnal temperature and food availability on mother and offspring fitness. We examined the following four related hypotheses and predictions. First, we hypothesised that nocturnal warming should accelerate gestation and that highest temperatures and food restriction should additively alter maternal homeostasis and reproductive output by increasing energy imbalance, oxidative stress and baseline corticosterone levels, thus decreasing immunocompetence, body condition, reproductive investment and litter viability. Second, females should develop short-term behavioural strategies, such as reduced activity and shifts in thermoregulatory behaviours, to promote energy conservation and mitigate the negative effects of too high nocturnal warming and food restriction during gestation. Third, food restriction should negatively impact offspring body condition and performance at birth, while nocturnal warming should increase offspring performance as well as post-summer survival and growth due to earlier hatching dates. Fourth, we predict synergetic effects of food restriction and temperature during gestation on maternal traits and reproductive output due to the lower thermal optimum of performances with restricted energy intake (Huey & Kingsolver, 2019).

## 2 | MATERIALS AND METHODS

### 2.1 | Study species, sampling and rearing conditions

The European common lizard (Zootoca vivipara) is a small diurnal and terrestrial lizard widely distributed in northern Eurasia in highly seasonal, cool and humid habitats. In natural and our captive populations, the mating period begins shortly after the emergence of sexually mature females from overwintering (Bauwens & Verheyen, 1985). Mated females carry out vitellogenesis during 2-3 weeks between mid-April and May, which is followed by ovulation and egg fertilisation that mark the onset of gestation (Bauwens & Verheyen, 1985). Parturition occurs after an average gestation period of ca. 2 months and ranges between late June and early August depending on thermal conditions and individual characteristics (Rutschmann et al., 2016). Breeding females (N=138) used in this study were captured inside semi-natural populations maintained in outdoor enclosures at CEREEP-Ecotron IleDeFrance (48°17'11.5" N, 2°40'45.6" E; Figure S1) after the mating season (i.e. between 3 May and 26 May). Females were acclimated for a minimum of 1 week before the experiments in individual terrariums (25×15×15 cm) filled with sterilised peat as substrate, equipped with a shelter and installed in a temperature-controlled room (25°C during daytime from 8.30 AM to 6.00 PM, 16°C at night from 6.00 PM to 8.30 AM). Terrariums were lit and heated automatically from 9.00 AM to 12.30 PM and from 1.30 PM to 4.30 PM by a UVB-enhanced neon tube (30 W) and a halogen heating bulb (25 W) placed on one side of
the terrarium to generate a thermal gradient relevant to this species. All lizards were acclimated by providing food ad libitum (400±25 mg of crickets *Acheta domestica* three times a week), water ad libitum and a humid environment (three water sprays per day). We inferred the reproductive status of females by the presence of recent bite marks on the abdomen and determined the initial gestation stage of females (i.e. vitellogenic or ovulatory stage) and the ovulation date by ultra-sonography (SonoSite M-Turbo, Inc., Bothell, WA, USA). Ovulation is detected by the change in the appearance of follicles from spherical and echoluent during vitellogenesis to highly echogenic ovulated eggs (Gilman & Wolf, 2007; Figure S2). All females were captured during vitellogenesis or close to ovulation. Experiments were performed under the approval of Charles Darwin Animal Experimentation Ethics Committee (APAFIS 41678) in an animal breeding facility accredited with permit 17/DDPP/SPAE/57.

## 2.2 | Experimental design

Using air-conditioned breeding rooms and heaters, we exposed pregnant females during all the gestation to contrasted nocturnal temperatures from 6.00PM to 8.30AM (Figure S3; hot night (H): 21°C±1.43 SD, intermediate night (I): 16°C±0.75 SD, cold night (C): 13°C±0.46 SD) and food availability conditions (control feeding treatment (F): ad libitum feeding with 400±25 mg of crickets three times per week, moderate feeding restriction (FR): feeding with 200±20 mg of crickets three times per week). Terrariums were lit and heated automatically following the same diurnal schedule described above. Intermediate and warm nocturnal temperatures simulate moderate and strong nocturnal warming scenarios, while cold treatment nights simulate current thermal conditions encountered in cold populations of this species (Dupoué et al., 2022). As climate change can also affect prey species abundance, though food availability in natural populations is rarely known, we applied two feeding treatments that simulate either high or limited availability of prey. This should constrain trade-offs between reproduction, growth and maintenance in a mixed income-capital breeder like the common lizard (Bleu et al., 2013; Mugabo et al., 2011). On average, we started the experimental treatments at or shortly after ovulation. Ovulation date was negatively correlated with body condition at capture, such that females in better body condition at capture ovulated earlier (slope: -6.33±1.25; $F_{1,122}=26.46, p<0.0001$) but it was not influenced by main effects of nocturnal temperatures ($F_{2,122}=1.56, p=0.21$) and food availability ($F_{1,122}=0.36, p=0.55$), or their interaction ($F_{2,120}=0.70, p=0.50$). Throughout the experiment, the females were maintained individually under the same daytime lighting and heating conditions as during acclimatisation. We randomly and equally distributed pregnant females of similar size, condition and vitellogenic stage into six experimental groups (N=23 per group) formed by the factorial combination of the nocturnal temperature and food treatments and randomly arranged them in rearing rooms. In addition, due to the important sample size and the time required for measurements, we formed three

experimental lots of 46 females composed of a balanced number of females from each experimental group. Measurements of morphological, physiological and behavioural traits were carried out over three consecutive days, with females from the same lot being measured on the same day.

## 2.3 | Morphological changes during gestation

Before the start of experimental treatments and 2 days after parturition, we quantified the tail width and limb thickness of females, which are reliable proxies of energetic condition. In reptiles, a decrease in tail width and limb thickness indicates muscle catabolism and mobilisation of caudal energy reserves (Brusch et al., 2020; Brusch IV et al., 2023). We took digital pictures of the females ventrally using a flatbed scanner (CanoScan LiDE 700F, Canon) and measured tail width at the 7th subcaudal scale rows with ImageJ software (Schneider et al., 2012). At the same time, left hind limb thickness was measured using a spessimeter (ID-C1012BS, Mitutoyo, Japan). We then calculated intra-individual changes in limb thickness and tail width between the beginning of the experiment and the parturition day.

## 2.4 | Physiological changes during gestation

We monitored baseline corticosterone levels, oxidative stress and immunocompetence throughout gestation by taking three repeated individual measurements at the beginning of gestation before the start of treatments, during gestation approximately in mid to two-thirds of gestation as detected by regular ultrasound monitoring of some females (see below) and after parturition day. At each measurement session, females were bled using a standard protocol within 3 min of restraining the animal to avoid handling-induced stress effects (Meylan et al., 2003). Approximately 50 µL of whole blood was collected from the post-orbital sinus, and plasma was obtained by centrifugation at 11000 rpm for 6 min of the blood samples, divided in two sub-samples and stored at -25°C until assay. Corticosterone level was measured on one sub-sample with a competitive enzymeimmunoassay method using corticosterone EIA (IDS Corticosterone EIA kit, ref. AC-14F1, lot J54692, IDS EURL Paris, France) after 1:10 dilution (see details in Josserand et al., 2017; intra-plate repeatability: $F_{35,36}=16.62, p<0.0001, r=0.89$). Furthermore, we measured the reactive oxygen metabolites (ROMs) in plasma as an index of oxidative damage with the d-ROMs colorimetric kit (MC003, lot NST03AA, Diacron International Italy), which measures the activity of organic hyperoxides (intra-plate repeatability: $F_{65,66}=17.16, p<0.0001, r=0.89$). We further used OXY-absorbent test kits (MC435, lot NST38BA, Diacron International Italy) to measure the non-enzymatic antioxidant capacity (OXY) of diluted plasma samples (1:100) to neutralise an oxidant attack from hypochlorous acid (intra-plate repeatability: $F_{67,69}=3.86, p<0.0001, r=0.59$; see details in Dupoué et al., 2020). In addition, we estimated immunocompetence
using phytohaemagglutinin (PHA) induced skin swelling test at least 2 days after the blood sampling. Local inflammation was assessed by skin swelling in response to the injection of a mitogen (i.e. 0.04 mL of a solution of PBS containing 2.5 mg/mL of PHA (Sigma-Aldrich; reference L8754)) in the right hind limb of the lizard as described by Meylan et al. (2013). The PHA swelling response includes both innate and adaptive components of the immune system in the common lizard (Mugabo et al., 2015), which may bias repeated measurements due to adaptive immunity after the first administration. We thus administered all females with a subcutaneous injection of PHA in the right hind limb during the acclimatisation phase (ca. 7 days before our first initial measurement) in order to elicit adaptive components. Skin swelling was calculated at the beginning, during gestation and at parturition as the absolute difference in the right limb thickness measured with a spessimeter (ID-C1012BS, Mitutoyo, Japan; to the nearest 0.01 mm) before and 12 h after the PHA injection (see details in Meylan et al., 2013).

## 2.5 | Activity, surface body temperature and food consumption

We recorded once a week female behavioural activity and surface body temperature during activity with instantaneous sampling every 45 min from 9.30 AM to 11.45 AM and from 2.00 PM to 3.30 PM local time (i.e. 7 readings during the day). One observer noted if lizards were active (i.e. visible and outside the shelter) or inactive (hidden or under the shelter). If they were not hidden, surface body temperature was recorded using an infrared thermometer (Raytek, Raynger MX2). In the middle of each behavioural record, we also noted the room temperature using a digital thermometer. To estimate the food consumption of pregnant females, at the end of each week (i.e. on Friday), we counted and weighed any uneaten crickets and removed them. On average, food-restricted females consumed all the crickets (98.1% ± 0.05 SD), while adlibitum-fed females did not (84.7% ± 0.18 SD), suggesting that our feeding treatment effectively simulated environments with contrasting prey availability (see Table S1; Figure S5).

## 2.6 | Reproductive monitoring and offspring phenotype

From acclimation to parturition, we monitored the females' gestation stage using ultrasound scans (SonoSite M-Turbo, Inc., Bothell, WA, USA) at least once a week. After parturition, each female was weighed and the litter was characterised by recording the number of unfertilised eggs, undeveloped embryos, stillborn and live juveniles. Juveniles were measured for snout to vent length (SVL; with a ruler, to the nearest 0.5 mm), weighed (using a precision scale to the nearest mg) and sexed by counting ventral scales (Lecomte et al., 1992). We further calculated reproductive investment as the difference between the body mass of females before and after parturition.

All live juveniles were marked by toe-clipping. The following day, we measured their endurance capacity in a circular racetrack maintained at 30.7°C ± 0.9 SD with a heat lamp (see details in Le Galliard & Ferrière, 2008). Juveniles warmed up at 30°C before the measurement in a climatic chamber. During endurance tests, lizards were stimulated to run at a constant speed (ca. 0.66 km h⁻¹) and motivated to continue after each stop with soft brush taps behind the tail until the lizard showed signs of exhaustion, determined by the loss of its ability to right itself after strong tail stimulations (Le Galliard et al., 2003; Sorci et al., 1995). Endurance was calculated as the running time until exhaustion (to the nearest second). Juveniles from the same litter were released in the evening after endurance measurements into 1 of 15 outdoor enclosures chosen pseudo-randomly in order to standardise the density, sex ratio and treatment frequency of juveniles among enclosures. Females were released into the same enclosure as their juveniles after all the measurements had been taken (on average 4 days after parturition).

## 2.7 | Monitoring of survival, growth and condition during post-reproductive season

In September 2023, all surviving offspring and females were captured in outdoor enclosures and measured for SVL and body mass in order to assess survival and growth during the post-reproductive summer season. We measured left hind limb thickness and tail width of adult females following the same method described above to estimate long-term effects of treatments on body condition. We calculated the specific growth rate of juveniles before wintering (SGR=[Ln (SVL) – Ln (initial SVL)]/days) using established methods (Liu et al., 2022).

## 2.8 | Replication statement

<table><thead><tr><td>Manipulated factors</td><td>Scale of inference</td><td>Scale at which the factor of interest is applied</td><td>Number of replicates at the appropriate scale</td></tr></thead><tbody><tr><td>Nocturnal temperatures (cold, intermediate, hot) and food availability (ad libitum, moderate food restriction)</td><td>Individual females Individual juveniles</td><td>Individual females</td><td>23 females of each nocturnal temperature/ food availability combination</td></tr></tbody></table>

## 2.9 | Statistical analyses

Analyses were performed with R software version 4.2.0 (R Core Team, 2022) and all statistical results are reported in Tables S1-S5.
For each analysis, we built a full model including the two-way inter-
action between nocturnal temperatures and food availability, checked
its assumptions and performed a goodness-of-fit test when relevant.
Non-significant effects were then eliminated using a stepwise model
selection procedure starting from the full model. We analysed mater-
nal phenological, morphological and physiological traits during ges-
tation using mixed models including a random effect of the capture
enclosure to account for potential differences among the enclosure
from where the female was captured and a fixed effect of the experi-
mental lot since these measurements were carried out successively
for each experimental lot. We analysed the ovulation date of females
using linear mixed models (LMMs) including the body condition of fe-
males at capture (i.e. residuals of the mass-over-size regression) and
the experimental treatments as fixed effects. We analysed the par-
turition date of females with LMMs including the fixed effect of the
individual-centred ovulation date and the experimental treatments.
To study intra-individual changes in limb thickness and tail width dur-
ing gestation, we used LMMs including fixed effects of the initial limb
thickness or tail width at capture, individual-centred ovulation date
and experimental treatments. We analysed repeated measurements of
PHA swelling response, baseline corticosterone, ROMs and OXY levels
using LMMs including the fixed effect of individual-centred ovulation
date and the three-way interaction between measurement session
Usage (factor with 3 levels: at the beginning, during gestation, after parturition), nocturnal temperatures and food availability. We also added a
random effect of individual identity to control for inter-individual vari-
ability. For baseline corticosterone, ROMs and OXY levels analyses, we
corrected the inter-plate variability of the assays by adding a fixed plate
effect to the models. Female litter size and viability were analysed with
generalised linear mixed models (GLMMs) assuming Poisson and bi-
nomial distribution, respectively, and we used LMMs to study female
reproductive investment and post-partum body mass. These models
included female SVL and experimental treatments as fixed effects. In
all analyses described above (except the ovulation date analysis), we
added a fixed effect of individual-centred ovulation date because ovu-
lation date, which marks the onset of gestation, can be correlated with
parturition date and female quality (Bauwens & Verheyen, 1985) and
because the experimental treatments and physiological measurements
started or were carried out not at the same time of the reproductive
cycle for each female.

We analysed repeated measurements of maternal behaviours
during gestation using mixed models including a random effect of in-
dividual identity to control for inter-individual variability and a fixed
effect of the experimental lot. We analysed surface body temperatures
during activity throughout the gestation (which is linearly linked to in-
ternal body temperature; Figure S4) using LMMs including fixed effects
of the breeding room temperatures, the gestation stage (calculated as
the number of days between the ovulation date and the date of mea-
surement, divided by the number of days between ovulation date and
parturition date), the experimental treatments and the experimental
lot. To ensure a Gaussian distribution of the residuals, we performed
a Box-Cox transformation of raw surface body temperatures. To study
activity behaviours, we counted the number of times each day out

of seven observations where females were active and then analysed
these counts data as success-failure events with GLMMs assuming a
binomial distribution including fixed effects of the gestation stage, the
experimental treatments and the experimental lot. We calculated the
ratio of crickets consumed per week (calculated as the mass of crickets
supplied minus the mass of crickets not consumed, divided by the mass
of crickets supplied) with LMMs including the experimental treatments
and the gestation stage as fixed effects.

To analyse offspring SVL, body mass and endurance at birth, we used LMMs with the effects of experimental treatments, sex, individual-centred ovulation date of the mother and offspring SVL (except for SVL analyses) as fixed effects and a random effect of female identity. For endurance analyses, we also added the number of stimulation and the running distance as fixed effects.

We further analysed delayed effects of experimental treat-
ments on both female and offspring morphology and survival using
mixed models including the release enclosure as a random effect.
Post-summer juvenile SVL, juvenile specific growth rate and female
body condition in September were analysed with LMMs including
the experimental treatments, sex (except for female body condi-
tion analysis) and SVL (except for juvenile SVL and specific growth
rate analysis). Female intra-individual changes in limb thickness and
tail width between parturition and September were analysed with
LMMs including the fixed effect of the limb thickness or tail width
at parturition and the experimental treatments. For juvenile and fe-
male survival analyses, we fitted GLMMs assuming a binomial distri-
bution and included the experimental treatments and sex (only for
juvenile survival analyses). In all juvenile post-summer traits analy-
ses, we included a random effect of individual identity of the mother
in the models.

3 | RESULTS

3.1 | Feeding, activity and surface body temperature of females

During gestation, females exhibited significant behavioural changes, with a regular decrease in selected surface body temperatures during activity, behavioural activity and food consumption (Table S1; Figure S5). In addition, nocturnal temperatures alone or in interaction with food availability affected female behaviours during gestation (Table S1). Surface body temperatures during activity were influenced by nocturnal temperatures, with slightly higher daytime body temperatures when females were exposed to warmer nocturnal temperatures (hot: 26.56°C±3.18 SD; intermediate: 26.06°C±3.09 SD; cold: 25.16°C±2.84 SD; Figure S5a). We also found significant effects of the interaction between nocturnal temperatures and food availability on behavioural activity and the ratio of cricket consumed during gestation (Table S1). Activity patterns of ad libitum fed females did not change with nocturnal temperatures, whereas food-restricted females showed higher daytime activity when they were exposed to warm nights compared with cold nights (Figure S5b).
Food-restricted females consumed almost all crickets independently of nocturnal temperatures, while well-fed females exposed to hot nights consumed more crickets than those exposed to intermediate or cold nights (Figure S5c).

## 3.2 | Morphological and physiological changes during gestation

Female energetic condition traits (limb thickness, tail width and post-partum body condition) were all influenced by nocturnal temperatures and food availability (Table S2), but only limb thickness changes during gestation were affected by the interaction between nocturnal temperatures and food availability. Indeed, under ad libitum feeding conditions, females exposed to the warmest nights showed a decrease in limb thickness, while females from the two other treatment groups exhibited slight increases (Figure 1a). With food restriction, females from warm and intermediate night conditions lost limb thickness, whereas it remained stable in cold night conditions. In contrast, tail width changes and post-partum body condition were influenced solely by the additive effects of experimental treatments, with food-restricted females and those exposed to hot nocturnal temperatures showing a smaller increase in tail width during gestation (Figure 1b) and a lower post-partum body condition (Figure 1c).

In addition, physiological traits of gravid females were mainly affected by nocturnal temperatures, except for redox balance and we did not detect any interactive effect of food and temperature treatments (Table S3). Female skin swelling response and baseline corticosterone levels were affected by the interaction between measurement session (i.e. at the beginning, during gestation, after parturition) and nocturnal temperatures independently of food availability. On average, skin swelling response increased during gestation for females exposed to intermediate and cold nocturnal temperatures but decreased under hot nocturnal temperatures (Figure 2a). Baseline corticosterone levels rose during early gestation regardless of treatments and subsequently declined after parturition, except for females exposed to cold nocturnal temperatures that maintained high corticosterone levels after parturition (Figure 2b). Oxidative stress markers (OXY and ROMs levels) were unaffected by nocturnal temperatures, but food availability in interaction with the measurement session influenced OXY levels. OXY levels increased during gestation for well-fed females but decreased for food-restricted females (Figure 2c).

## 3.3 | Reproductive output and juvenile phenotype at birth

Reproductive traits were all correlated with ovulation date (Table S4; discussed in Supporting Information). Females that ovulated early gave birth earlier (slope: 0.64±0.05; Figure 3) and had higher litter size (slope: -0.01±0.005), reproductive investment

(slope: -0.03±0.01) and litter viability (slope: -0.33±0.01). Reproductive traits were also significantly affected by nocturnal temperatures and food availability, except for litter size (Table S4). Parturition date was affected by the interactive effects of nocturnal temperatures and food availability. Nocturnal warming shortened gestation time regardless of food, except for females exposed to intermediate nights, which gave birth earlier when food was restricted (Figure 3). We also detected significant additive effects of nocturnal temperatures and food availability on reproductive investment and litter viability. Females exposed to hot nights had a lower reproductive investment (hot: 1.74g±0.65 SD; intermediate: 2.14g±0.59 SD; cold: 2.14g±0.74 SD), as well as food-restricted females (food ad libitum: 2.16g±0.59 SD; food-restricted: 1.83g±0.74 SD). The proportion of viable offspring in the litter was higher in females exposed to intermediate nocturnal temperatures compared with hot and cold nights (hot: 0.59±0.42 SD; intermediate: 0.74±0.35 SD; cold: 0.58±0.35 SD). It was also higher in well-fed compared to food-restricted females (food ad libitum: 0.70±0.35 SD; food-restricted: 0.56±0.40 SD). Juvenile body size at birth was not influenced by treatments, whereas juvenile body condition and endurance were respectively influenced by food availability and nocturnal temperatures. Juveniles born from food-restricted females were slightly less corpulent than juveniles from well-fed females (Figure 4a) and juveniles born from females exposed to hot nights had a higher endurance capacity than juveniles from females exposed to cold nights (Figure 4a). Except for parturition dates, we did not detect any interactive effect of nocturnal temperatures and food availability on reproductive output and juvenile phenotype at birth (Table S4).

## 3.4 | Delayed effect on survival and phenotype of juveniles and females

Of 135 living females and 508 juveniles born in the laboratory and released in the field, we recaptured 119 juveniles and 97 females in September 2023 (estimated survival rates: 72% for adult females and 23% for juveniles). Overall, we detected no interactive effects of nocturnal temperatures and food availability on the survival or growth of females and juveniles in September (Table S5). Nocturnal temperatures had no delayed effects on juvenile and female survival, or on females' condition (i.e. limb thickness, tail width and post-partum body condition). However, nocturnal temperatures during gestation significantly affected post-summer juveniles SVL without impacting their specific growth rate. Juveniles from females exposed to warm nights were larger in September than juveniles from females exposed to cold nights (Figure 4c). In addition, food availability during gestation had no delayed effect on juvenile survival or growth and only affected post-summer female body condition, without influencing their survival, limb thickness and tail width changes. Food-restricted females during gestation still had a lower post-summer body condition in September (contrast=-0.27±0.08 g).
<figure><img src="image_5.png" /><figcaption>FIGURE 1 Intra-individual changes in (a) limb thickness, (b) tail width and post-parturm body condition of females (c) as a function of nocturnal temperatures (H: hot (red); I: intermediate (grey); C: cold (blue)) and food availability treatments (F: ad libitum food (solid line); FR: food-restricted (dashed line)). In (a) and (b), a negative change indicates a decrease in the limb thickness or tail width. Body condition of females after parturition are residuals of a linear regression between female body mass and SVL. Boxplots of the distribution of data are displayed and different letters indicate significant differences between groups (*p* < 0.05; Tukey's HSD post hoc test).</figcaption></figure>
<figure><img src="image_6.png" /><figcaption>FIGURE 2 Effects of nocturnal temperatures (hot (red); intermediate (grey); cold (blue)) and food availability treatments (ad libitum food (solid black line); food-restricted (dashed black line)) on (a) PHA swelling response, (b) baseline corticosterone and (c) OXY levels of breeding females throughout gestation (0: beginning of gestation; 1: mid-gestation; 2: after parturition). Points are mean values ± SE.</figcaption></figure>
<figure><img src="image_7.png" /></figure>

FIGURE 3 Relationship between parturition and ovulation dates of breeding females *Zootoca vivipara* as a function of nocturnal temperatures (H: hot (red); I: intermediate (grey); C: cold (blue)) and food availability treatments (F: ad libitum food (solid line); FR: food-restricted (dashed line)). Confidence intervals were not displayed to improve visibility. Points represent individual values.

4 | DISCUSSION

To improve our understanding of the thermal plasticity of breeding
phenology in viviparous ectotherms, we examined the combined ef-
fects of nocturnal warming and prey availability during gestation on
parturition dates and multivariate indicators of condition, reproduc-
tion, offspring phenotype at birth and maternal and juvenile fitness.
Nocturnal warming strongly shortened average gestation time in line
with several previous studies of lizards (Brusch IV et al., 2023; Clarke
& Zani, 2012; Moore et al., 2020) and the general thermal plasticity
of gestation in reptiles (reviewed in Noble et al., 2018). Furthermore,
exposure to the warmest nights and food restriction had negative
additive effects on reproduction and increased the costs of repro-
duction, as shown by changes in the immune system and energy bal-
ance of pregnant females. In contrast, moderate nocturnal warming
increased litter viability and thermal acceleration of gestation was
beneficial to the offspring by enhancing their performance at birth
and allowing for a longer growth period and size advantage through-
out early life.

4.1 | Nocturnal temperatures and prey availability interact to drive breeding phenology

As expected, exposure to hot nights (+8°C) accelerated gestation
strongly by around 39% compared to cold nights. These results are
in line with previous research in oviparous and viviparous reptiles
showing that higher nocturnal temperatures lead to earlier parturi-
tion or hatching dates (Brusch IV et al., 2023; Clarke & Zani, 2012;
Moore et al., 2020). In addition, nocturnal temperatures and prey

availability had unexpected interactive effects on parturition dates.
Under cold and hot nocturnal conditions, prey availability did not
influence breeding phenology, but food-restricted females gave
birth earlier than well-fed females under intermediate nocturnal
temperatures. While changes in breeding dates due to prey avail-
ability are well documented in insectivorous birds, where some spe-
cies adjust their breeding dates based on prey availability (reviewed
in Martin, 1987; Robb et al., 2008), the effects of prey availability
alone or in interaction with temperature on the breeding phenology
of reptiles are poorly documented (Hall et al., 2018). Given food is
unlikely to directly affect the speed of embryonic development in
utero in the common lizard, the observed interactive effects may
stem from subtle behavioural adjustments in response to resource
availability and nocturnal temperatures (discussed in *Supporting
Information*).

4.2 | Nocturnal temperatures and prey availability drive reproductive output

Nocturnal warming and food restriction strongly influenced repro-
ductive investment and litter viability but had no effect on fecundity,
probably because litter size is set before the start of the experi-
ment in this lecithotrophic species (Bauwens & Verheyen, 1985).
The common lizard uses mixed capital and income reproductive
strategies (Bleu et al., 2013), where reproductive investment and
reproductive success may depend on both stored resources and re-
sources recently acquired during vitellogenesis or gestation (Bonnet
et al., 1998). Higher energy expenditure induced by hot nights and
lower food intake due to food restriction both reduced the amount
<figure><img src="image_8.png" /></figure>

FIGURE 4 Effects of nocturnal temperatures (hot (red); intermediate (grey); cold (blue)) and food availability treatments (ad libitum food (solid line); food-restricted (dashed line)) on (a) juvenile body condition at birth, (b) juvenile endurance and (c) post-summer juvenile SVL. Juvenile body condition at birth are residuals of a linear regression between juvenile mass and juvenile SVL. Boxplots of the distribution of data are displayed and different letters indicate significant differences between groups (*p* < 0.05; Tukey's HSD post hoc test).
of energy available to fuel reproduction, thus reducing reproductive investment and embryo viability. These results are consistent with previous studies in viviparous lizards reporting negative effects of too high nocturnal warming or too low prey availability during gestation on reproductive investment (Brusch IV et al., 2023; Wang et al., 2017). Nevertheless, nocturnal temperatures had non-linear effects on litter viability such that moderate nocturnal warming increased litter viability in line with the general pattern of a concave curve between offspring viability and developmental temperatures across studies of squamate reptiles (Noble et al., 2018).

## 4.3 | High nocturnal temperatures and food restriction disrupt maternal homeostasis

High nocturnal temperatures and low prey availability increased the energetic costs of gestation, as seen with the loss of body condition and reduced limb thickness and tail width. This was most likely due to increased muscle catabolism and mobilisation of caudal lipid reserves, which are physiological responses to cover energy and amino acid requirements when energy expenditure increases or food intake is insufficient (Bodineau, Chabaud, Decencière, et al., 2024; Brusch IV et al., 2023; Price, 2017). Interestingly, muscle loss occurred at intermediate nocturnal temperatures under food restriction but only at high night-time temperatures under ad libitum food, suggesting a lower optimal nocturnal temperature with restricted prey availability. Thus, in line with theoretical studies, reduced prey availability could accentuate the metabolic costs of nocturnal warming on female condition (Huey & Kingsolver, 2019; Rutschmann et al., 2024; Thomas et al., 2017). Yet, this shift in optimal temperatures was not seen in other components of body condition and energetics, such as caudal lipid mobilisation and overall body condition. We suggest that the combined effects of nocturnal warming and food deprivation may affect differently the different metabolic pathways (e.g. lipids and amino acids regulation) underlying body condition.

Breeding phenology plasticity due to nocturnal warming was also associated with significant alterations of key physiological traits such as immunocompetence and basal corticosterone levels. High nocturnal warming led to a decrease in immunocompetence relative to cold and intermediate nocturnal conditions like in other reptile species (Butler et al., 2013; Sacchi et al., 2017; Stahlschmidt et al., 2017). Our current study cannot provide a detailed mechanistic understanding of the effects of temperature on the immune system as the PHA swelling response includes several innate and adaptive components (Demas et al., 2011; Mugabo et al., 2015). Immune suppression at high temperatures could be due to direct effects of temperature on the activity of phagocytic and cytotoxic cells of innate and adaptive immunity (Rios & Zimmerman, 2015) or to indirect effects of high temperatures on the amount of energy that can be allocated to the immune system. However, in the second case, we would have predicted a negative effect of food restriction on immunocompetence, as seen in multi-ocellated racerunners, for example (Wang

et al., 2017), which we did not observe. Furthermore, while corticosterone levels tend to increase during gestation in several viviparous squamate species (Lorioux et al., 2016; Taylor et al., 2004), this pattern was only visible in females exposed to cold nights, whereas intermediate and hot night temperatures down-regulated basal corticosterone levels late in gestation, contrary to our initial predictions. A down-regulation of circulating corticosterone levels in response to warming is consistent with the negative relationship between basal corticosterone levels and minimum daily temperatures observed in natural populations and could constitute an energy conservation mechanism in response to chronic exposure to high temperatures (Dupoué et al., 2018). Finally, nocturnal temperatures had no significant effect on the oxidative balance of females (i.e. oxidative damage and antioxidant capacity). Although environmental temperatures can modulate oxidative stress or antioxidant responses in reptiles (Dupoué et al., 2020; Han et al., 2020), previous studies on the common lizard also reported no nocturnal warming effect on oxidative balance (Brusch et al., 2020; Rutschmann et al., 2021). This could be explained by the ability of females to buffer the effects of nocturnal warming through physiological or behavioural adjustments or might be explained by the use of global instead of more specific markers of oxidative stress (Rutschmann et al., 2024). In contrast, food restriction reduced the non-enzymatic antioxidant capacity of females, probably because food provides antioxidant compounds and because the production of antioxidant molecules requires energy (reviewed in Costantini, 2014).

## 4.4 | Behavioural responses were insufficient

Behavioural adjustments were insufficient to compensate for the energetic costs induced by warm nights and low prey availability, impacting both energy balance and reproductive performance. While some reptiles may reduce their mean body temperature or activity during chronic exposure to fasting or heat waves in order to promote energy conservation (Angilletta Jr., 2009), females exposed to hot nights had slightly higher daytime surface body temperatures during activity and higher activity rates under low prey availability. Increased activity and body temperatures in energetically challenging environments could be short-term responses to promote energy intake, as higher body temperatures favour food intake and digestive efficiency (Van Damme et al., 1991). Obviously, these responses do not constitute effective energy conservation strategies against chronic exposure to high nocturnal temperatures or low prey availability. However, ad libitum-fed females increased cricket consumption under hot nights, likely due to improved digestion efficiency or to offset energy imbalances caused by hot nights (Brusch IV et al., 2023). Ultimately, changes in daily activity patterns, in selected body temperatures during activity phases and in prey consumption which drive the net energy budget in ectotherms (i.e. the balance between inputs from food intake and assimilation, and outputs from energy expenditure at rest and during activity (Dillon et al., 2010; Levy et al., 2017; Rutschmann et al., 2024)), were insufficient to
mitigate the negative impacts of high nocturnal temperatures and food restriction on energy balance. Although behavioural adjustments could be facilitated in the wild, our results suggest that diurnal reptiles may have difficulty in behaviourally buffering nocturnal warming and low prey availability (Rutschmann et al., 2024).

4.5 | Warm developmental nocturnal temperatures have beneficial effects on juveniles

Nocturnal temperatures did not influence juvenile morphology at birth, but hot nocturnal temperatures increased juvenile endurance, suggesting a positive effect of nocturnal warming on the intrinsic quality of neonates. In reptiles, developmental temperatures are important determinants of offspring fitness-related traits, but these effects often vary in magnitude and direction between species, and the underlying mechanisms are still poorly understood (reviewed in Booth, 2006; Noble et al., 2018; While et al., 2018). For example, some studies show positive effects of warmer developmental temperatures or increased maternal thermoregulatory opportunities on juvenile body condition and locomotor performance at birth (Li et al., 2018; Pearson & Warner, 2018; Zhang et al., 2013), while others show the opposite (Braña & Ji, 2000; Dayananda et al., 2017; Swain & Jones, 2000) or no effect (Beltrán et al., 2020; Brusch et al., 2020). Mechanisms underlying the effects of thermal regimes on offspring locomotor performance could include beneficial effects of warmer developmental temperatures or reduced gestation length on the development of musculoskeletal or brain function in embryos (Booth, 2017; While et al., 2009) or different thermal performance curves between juveniles from different thermal treatments, as we tested the endurance at a single temperature (Pearson & Warner, 2018). In addition, low prey availability during gestation negatively impacted juvenile body condition at birth, likely due to maternal behavioural or physiological responses rather than direct placental nutrient support during embryogenesis, as the common lizard is lecithotrophic without a placental exchange structure (Stewart et al., 2004).

In addition, nocturnal warming had no delayed effects on female post-manipulation survival or the change of condition-related traits (i.e. body condition, limb thickness and tail width) after the manipulation, but food restriction led to a long-lasting body condition decline (see also Mugabo et al., 2011). Yet, our results indicate that thermal acceleration of gestation induced by nocturnal warming had beneficial effects on the growth of the offspring since the post-summer body size of juveniles was greater when females were exposed to warmer nocturnal temperatures during gestation. These effects of developmental temperatures on post-summer growth could be explained by differences in offspring quality (e.g. foraging skills) and/or reflect the advantage of an early birth date, which generally confers growth benefits due to a longer growth period before winter (Adolph & Porter, 1993; Bodineau, de Villemereuil, Agostini, et al., 2024; Pearson & Warner, 2018; Warner & Shine, 2007). In fact, when we

replaced the effect of nocturnal thermal treatment with juvenile birth date, we found a negative correlation between birth date and post-summer SVL (slope: -0.25 ± 0.02; F₁,₄₆.₅ = 112.71, *p* < 0.0001). Thus, contrary to our predictions and some previous studies, high developmental temperatures did not improve post-summer juvenile growth rates or survival (Liu et al., 2022; Sun et al., 2018; Warner & Shine, 2007). This suggests that any advantage of warmer developmental temperatures or early birth in the common lizard was mainly a consequence of growth period extension before wintering rather than from more advantageous growing conditions early in the season (i.e. more favourable temperatures, longer days, weaker competition between conspecifics (Bodineau, de Villemereuil, Agostini, et al., 2024)).

5 | CONCLUSIONS

We examined how nocturnal warming and prey availability during gestation jointly influence breeding phenology and multiple indicators of female homeostasis, reproductive output and offspring quality in a viviparous lizard. Independently of food availability, breeding phenology advancement induced by overnight warming benefited offspring by enhancing locomotor performance and extending the time period of early-life growth, but also altered maternal homeostasis and reproductive performance. These findings highlight a potential mother-offspring conflict in the context of warming-induced phenological shifts and suggest that intense nocturnal warming may reshape reproductive strategies in viviparous ectotherms. Additionally, gravid females exhibited limited and sometimes even counterproductive, behavioural strategies to counteract the energetic costs of nocturnal warming and low prey availability further accentuated some of these costs. Since climate warming often induces concomitant changes in prey availability (Bretagnolle & Terraube, 2019; Laws, 2017), these findings challenge the assumption that phenological shifts are uniformly beneficial or detrimental, highlighting the necessity of evaluating the costs and benefits of breeding phenology plasticity taking into account the energy landscape and not only temperature changes.

AUTHOR CONTRIBUTIONS

Théo Bodineau, Jean-François Le Galliard, Sandrine Meylan and Pierre de Villemereuil conceived the ideas and designed methodology; Théo Bodineau, Jean-François Le Galliard, Sandrine Meylan, Simon Agostini and Beatriz Decencière participated in lizard captures and breeding; Matéo Millet performed the endurance assays; Théo Bodineau and Baptiste Lemaire carried out physiological assays; Théo Bodineau collected and analysed the data with the help of Jean-François Le Galliard, Sandrine Meylan and Pierre de Villemereuil; Théo Bodineau led the writing of the manuscript with the help of Jean-François Le Galliard, Sandrine Meylan and Pierre de Villemereuil. All authors contributed critically to the paper and gave final approval for publication.
<figure><img src="image_9.png" /></figure>

## ACKNOWLEDGEMENTS

The authors thank Charline Andréani, Tom Compain, Max Delpy, Fabien Fournié, Camille Hamon and Anaïs Marhuenda who contributed to data acquisition. This work was supported by an Agence Nationale de la Recherche grant (ANR-17-CE020013, 'AQUATHERM') to J.-F. Le Galliard. Théo Bodineau' PhD grant is funded by the Ministère de l'Enseignement Supérieur et de la Recherche. This work has benefited from human and technical resources provided by the CEREEP-Ecotron IleDeFrance (CNRS/ENS UAR 3194). Experiments were performed under the approval of Charles Darwin Animal Experimentation Ethics Committee (APAFIS 41678) in an animal breeding facility accredited with permit 17/ DDPP/SPAE/57.

## CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.

## DATA AVAILABILITY STATEMENT

Data and scripts are available at Zenodo with DOI: https://doi.org/10.5281/zenodo.11197883 (Bodineau, de Villemereuil, Lemaire, et al., 2024).

## STATEMENT ON INCLUSION

Our study brings together authors from the same countries, including a Senior Researcher, a Professor, a Lecturer, a PhD student, engineers and a master's student. All authors were engaged early on with the research and study design to ensure that the diverse sets of perspectives they represent were considered from the onset.

## ORCID

Théo Bodineau https://orcid.org/0000-0001-7375-1401

Pierre de Villemereuil https://orcid.org/0000-0002-8791-6104

Baptiste Lemaire https://orcid.org/0009-0004-2150-7916

Beatriz Decencière https://orcid.org/0000-0002-2847-7631

Matéo Millet https://orcid.org/0009-0008-5335-8395

Sandrine Meylan https://orcid.org/0000-0002-0865-3335

Jean-François Le Galliard https://orcid.org/0000-0002-5965-9868

## REFERENCES

Adolph, S., & Porter, W. (1993). Temperature, activity, and lizard life histories. *The American Naturalist*, 142, 273–295. https://doi.org/10.1086/285538

Angilletta, M. J., Jr. (2009). *Thermal adaptation*. Oxford University Press. https://doi.org/10.1093/acprof:oso/9780198570875.001.1

Ballen, C., Healey, M., Wilson, M., Tobler, M., Wapstra, E., & Olsson, M. (2012). Net superoxide levels: Steeper increase with activity in cooler female and hotter male lizards. *Journal of Experimental Biology*, 215(5), 731–735. https://doi.org/10.1242/jeb.062257

Bauwens, D., & Verheyen, R. F. (1985). The timing of reproduction in the lizard *Lacerata vivipara*: Differences between individual females. *Journal of Herpetology*, 19(3), 353–364. https://doi.org/10.2307/1564263

Beltrán, I., Durand, V., Loiseleur, R., & Whiting, M. J. (2020). Effect of early thermal environment on the morphology and performance of

a lizard species with bimodal reproduction. *Journal of Comparative Physiology B*, 190(6), 795–809. https://doi.org/10.1007/s00360-020-01312-2

Bleu, J., Le Galliard, J.-F., Fitze, P. S., Meylan, S., Clobert, J., & Massot, M. (2013). Reproductive allocation strategies: A long-term study on proximate factors and temporal adjustments in a viviparous lizard. *Oecologia*, 171(1), 141–151. https://doi.org/10.1007/s00442-012-2401-1

Bleu, J., Massot, M., Haussy, C., & Meylan, S. (2012). Experimental litter size reduction reveals costs of gestation and delayed effects on offspring in a viviparous lizard. *Proceedings of the Royal Society B: Biological Sciences*, 279(1728), 489–498. https://doi.org/10.1098/rspb.2011.0966

Bodineau, T., Chabaud, C., Decencière, B., Agostini, S., Lourdais, O., Meylan, S., & Le Galliard, J.-F. (2024). Microhabitat humidity rather than food availability drives thermo-hydroregulation responses to drought in a lizard. *Oikos*, 202(6), e10535. https://doi.org/10.1111/oik.10535

Bodineau, T., de Villemereuil, P., Agostini, S., Decencière, B., Le Galliard, J.-F., & Meylan, S. (2024). Breeding phenology drives variation in reproductive output, reproductive costs, and offspring fitness in a viviparous ectotherm. *Journal of Evolutionary Biology*, 37(9), 1023–1034. https://doi.org/10.1093/jeb/voae086

Bodineau, T., de Villemereuil, P., Lemaire, B., Agostini, S., Decencière, B., Millet, M., Meylan, S., & Le Galliard, J.-F. (2024). Data from: A multi-trait evaluation of patterns and fitness consequences of breeding phenology plasticity with nocturnal warming and food restriction in a lizard. *Zenodo*, https://doi.org/10.5281/zenodo.11197883

Bonnet, X., Bradshaw, D., & Shine, R. (1998). Capital versus income breeding: An ectothermic perspective. *Oikos*, 83(2), 333–342. https://doi.org/10.2307/3546846

Booth, D. T. (2006). Influence of incubation temperature on hatchling phenotype in reptiles. *Physiological and Biochemical Zoology*, 79(2), 274–281. https://doi.org/10.1086/499988

Booth, D. T. (2017). Influence of incubation temperature on sea turtle hatchling quality. *Integrative Zoology*, 12(5), 352–360. https://doi.org/10.1111/1749-4877.12255

Bradford, D. F. (1990). Incubation time and rate of embryonic development in amphibians: The influence of ovum size, temperature, and reproductive mode. *Physiological Zoology*, 63(6), 1157–1180.

Braña, F., & Ji, X. (2000). Influence of incubation temperature on morphology, locomotor performance, and early growth of hatchling wall lizards (*Podarcis muralis*). *Journal of Experimental Zoology*, 286(4), 422–433. https://doi.org/10.1002/(SICI)1097-010X(20000301)286:4<422::AID-JEZ10>3.0.CO;2-D

Bretagnolle, V., & Terraube, J. (2019). Predator-prey interactions and climate change. In P. O. Dunn & A. P. Møller (Eds.), *Effects of climate change on birds* (2nd ed., pp. 199–220). Oxford University Press. https://doi.org/10.1093/oso/9780198824268.003.0015

Brusch, G. A., Gavira, R. S. B., Viton, R., Dupoué, A., Leroux-Coyau, M., Meylan, S., Galliard, J.-F. L., & Lourdais, O. (2020). Additive effects of temperature and water availability on pregnancy in a viviparous lizard. *Journal of Experimental Biology*, 223(19), jeb228064. https://doi.org/10.1242/jeb.228064

Brusch, G. A., IV, Le Galliard, J.-F., Viton, R., Gavira, R. S. B., Clobert, J., & Lourdais, O. (2023). Reproducing in a changing world: Combined effects of thermal conditions by day and night and of water constraints during pregnancy in a cold-adapted ectotherm. *Oikos*, 2023(3), e09536. https://doi.org/10.1111/oik.09536

Burraco, P., Orizaola, G., Monaghan, P., & Metcalfe, N. B. (2020). Climate change and ageing in ectotherms. *Global Change Biology*, 26(10), 5371–5381. https://doi.org/10.1111/gcb.15305

Butler, M. W., Stahlschmidt, Z. R., Ardia, D. R., Davies, S., Davis, J., Guillette, L. J., Johnson, N., McCormick, S. D., McGraw, K. J., & DeNardo, D. F. (2013). Thermal sensitivity of immune function:
Evidence against a generalist-specialist trade-off among endother-
mic and ectothermic vertebrates. *The American Naturalist*, **181**(6),
761-774. https://doi.org/10.1086/670191

Clarke, D. N., & Zani, P. A. (2012). Effects of night-time warming on temperate ectotherm reproduction: Potential fitness benefits of climate change for side-blotched lizards. *Journal of Experimental Biology*, *215*(7), 1117-1127. https://doi.org/10.1242/jeb065359

Cohen, J. M., Lajeunesse, M. J., & Rohr, J. R. (2018). A global synthesis of animal phenological responses to climate change. *Nature Climate Change*, *8*(3), 224-228. https://doi.org/10.1038/s4155 8-018-0067-3

Costantini, D. (2014). Oxidative stress and Hormesis in evolutionary ecol-
ogy and physiology: A marriage between mechanistic and evolutionary
approaches. Springer Berlin Heidelberg. https://doi.org/10.1007/
978-3-642-54663-1

Dayananda, B., Penfold, S., & Webb, J. K. (2017). The effects of incu-
bation temperature on locomotor performance, growth and sur-
vival in hatchling velvet geckos. *Journal of Zoology*, *303*(1), 46-53.
https://doi.org/10.1111/jzo.12460

Demas, G. E., Zysling, D. A., Beechler, B. R., Muehlenbein, M. P., & French, S. S. (2011). Beyond phytohaemagglutinin: Assessing vertebrate immune function across ecological contexts. *The Journal of Animal Ecology*, *80*(4), 710-730. https://doi.org/10.1111/j.1365-2656.2011.01813.x

Dezetter, M., Le Galliard, J.-F., Leroux-Coyau, M., Brischoux, F., Angelier, F., & Lourdais, O. (2022). Two stressors are worse than one: Combined heatwave and drought affect hydration state and glucocorticoid levels in a temperate ectotherm. *Journal of Experimental Biology*, *225*(7), jeb243777. https://doi.org/10.1242/jeb.243777

Dillon, M. E., Wang, G., & Huey, R. B. (2010). Global metabolic impacts of recent climate warming. *Nature*, *467*(7316), 704-706. https://doi.org/10.1038/nature09407

Duffy, K., Gouhier, T. C., & Ganguly, A. R. (2022). Climate-mediated shifts in temperature fluctuations promote extinction risk. *Nature Climate Change*, *12*(11), 1037-1044. https://doi.org/10.1038/s41558-022-01490-7

Dupoué, A., Blaimont, P., Angelier, F., Ribout, C., Rozen-Rechels, D., Richard, M., Miles, D., de Villemereuil, P., Rutschmann, A., Badiane, A., Aubret, F., Lourdais, O., Meylan, S., Cote, J., Clobert, J., & Le Galliard, J.-F. (2022). Lizards from warm and declining populations are born with extremely short telomeres. *Proceedings of the National Academy of Sciences*, *119*(33), e220137119. https://doi.org/10.1073/pnas.2201371119

Dupoué, A., Blaimont, P., Rozen-Rechels, D., Richard, M., Meylan, S., Clobert, J., Miles, D. B., Martin, R., Decencière, B., Agostini, S., & Le Galliard, J.-F. (2020). Water availability and temperature induce changes in oxidative status during pregnancy in a viviparous lizard. *Functional Ecology*, *34*(2), 475-485. https://doi.org/10.1111/1365-2435.13481

Dupoué, A., Brischoux, F., Angelier, F., DeNardo, D. F., Wright, C. D., & Lourdais, O. (2015). Intergenerational trade-off for water may induce a mother-offspring conflict in favour of embryos in a viviparous snake. *Functional Ecology*, *29*(3), 414-422. https://doi.org/10.1111/1365-2435.12349

Dupoué, A., Rutschmann, A., Le Galliard, J. F., Clobert, J., Angelier, F., Marciau, C., Ruault, S., Miles, D., & Meylan, S. (2017). Shorter telomeres precede population extinction in wild lizards. *Scientific Reports*, *7*(1), 16976. https://doi.org/10.1038/s41598-017-17323-z

Dupoué, A., Rutschmann, A., Le Galliard, J. F., Clobert, J., Blaimont, P., Sinervo, B., Miles, D. B., Haussy, C., & Meylan, S. (2018). Reduction in baseline corticosterone secretion correlates with climate warming and drying across wild lizard populations. *Journal of Animal Ecology*, *87*(5), 1331-1341. https://doi.org/10.1111/1365-2656.12843

Dupoué, A., Rutschmann, A., Le Galliard, J. F., Miles, D. B., Clobert, J., DeNardo, D. F., Brusch, G. A., & Meylan, S. (2017). Water availability

and environmental temperature correlate with geographic vari-
ation in water balance in common lizards. *Oecologia*, **185**(4), 561-
571. https://doi.org/10.1007/s00442-017-3973-6

Foucart, T., Lourdais, O., DeNardo, D. F., & Heulin, B. (2014). Influence of reproductive mode on metabolic costs of reproduction: Insight from the bimodal lizard *Zootoca vivipara*. *Journal of Experimental Biology*, *217*(22), 4049-4056. https://doi.org/10.1242/jeb.104315

Gilman, C. A., & Wolf, B. O. (2007). Use of portable ultrasonography as a nondestructive method for estimating reproductive effort in lizards. *Journal of Experimental Biology*, *210*(11), 1859-1867. https://doi.org/10.1242/jeb.001875

Graham, A. L., Shuker, D. M., Pollitt, L. C., Auld, S. K. J. R., Wilson, A. J., & Little, T. J. (2011). Fitness consequences of immune responses: Strengthening the empirical framework for ecoimmunology. *Functional Ecology*, *25*(1), 5-17. https://doi.org/10.1111/j.1365-2435.2010.01777.x

Hall, J. M., Buckelew, A., Lovern, M., Secor, S. M., & Warner, D. A. (2018). Seasonal shifts in reproduction depend on prey availability for an income breeder. *Physiological and Biochemical Zoology*, *91*(6), 1129-1147. https://doi.org/10.1086/700341

Hallmann, C. A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., Stenmans, W., Müller, A., Sumser, H., Hörren, T., Goulson, D., & de Kroon, H. (2017). More than 75 percent decline over 27 years in total flying insect biomass in protected areas. *PLoS One*, *12*(10), e0185809. https://doi.org/10.1371/journal.pone.0185809

Han, X., Hao, X., Wang, Y., Wang, X., Teng, L., Liu, Z., Zhang, F., & Zhang, Q. (2020). Experimental warming induces oxidative stress and immunosuppression in a viviparous lizard, *Eremias multiocellata*. *Journal of Thermal Biology*, *90*, 102595. https://doi.org/10.1016/j.jtherbio.2020.102595

Hodgson, M. J., & Schwanz, L. E. (2024). Best of both worlds: Acclimation to fluctuating environments confers advantages and minimizes costs of constant environments. *Functional Ecology*, *38*(4), 724-738. https://doi.org/10.1111/1365-2435.14522

Huey, R. B., & Kingsolver, J. G. (2019). Climate warming, resource avail-
ability, and the metabolic meltdown of ectotherms. *The American
Naturalist*, *194*(6), E140–E150. https://doi.org/10.1086/705679

Jara, M., García-Roa, R., Escobar, L. E., Torres-Carvajal, O., & Pincheira-
Donoso, D. (2019). Alternative reproductive adaptations pre-
dict asymmetric responses to climate change in lizards. *Scientific
Reports*, *9*(1), 5093. https://doi.org/10.1038/s41598-019-41670-8

Jessop, T. S., Lane, M. L., Teasdale, L., Stuart-Fox, D., Wilson, R. S., Careau, V., & Moore, I. T. (2016). Multiscale evaluation of thermal dependence in the glucocorticoid response of vertebrates. *The American Naturalist*, *188*(3), 342-356. https://doi.org/10.1086/687588

Josserand, R., Dupoué, A., Agostini, S., Haussy, C., Le Galliard, J.-F., & Meylan, S. (2017). Habitat degradation increases stress-hormone levels during the breeding season, and decreases survival and reproduction in adult common lizards. *Oecologia*, *184*(1), 75-86. https://doi.org/10.1007/s00442-017-3841-4

Kingsolver, J. G. (1995). Fitness consequences of seasonal polyphenism in western white butterflies. *Evolution*, *49*(5), 942-954. https://doi.org/10.1111/j.1558-5646.1995.tb02329.x

Laws, A. N. (2017). Climate change effects on predator-prey interac-
tions. *Current Opinion in Insect Science*, *23*, 28-34. https://doi.org/
10.1016/j.cois.2017.06.010

Le Galliard, J.-F., Bris, M., & Clobert, J. (2003). Timing of locomotor impairment and shift in thermal preferences during gravidity in a viviparous lizard. *Functional Ecology*, *17*(6), 877-885. https://doi.org/10.1046/j.0269-8463.2003.00800.x

Le Galliard, J.-F., & Ferrière, R. (2008). Evolution of maximal endurance capacity: Natural and sexual selection across age classes in a lizard. *Evolutionary Ecology Research*, *10*, 157-176.

Le Henanff, M., Meylan, S., & Lourdais, O. (2013). The sooner the better: Reproductive phenology drives ontogenetic trajectories in a temperate squamate (*Podarcis muralis*). *Biological Journal of the Linnean
Society, 108(2), 384–395. https://doi.org/10.1111/j.1095-8312. 2012.02005.x

Lecomte, J., Clobert, J., & Massot, M. (1992). Sex identification in juve-
niles of *Lacerta vivipara*. *Amphibia-Reptilia*, 13(1), 21–25. https://doi.
org/10.1163/156853892X00193

Levy, O., Borchert, J. D., Rusch, T. W., Buckley, L. B., & Angilletta, M. J., Jr. (2017). Diminating returns limit energetic costs of climate change. *Ecology*, 98(5), 1217–1228. https://doi.org/10.1002/ecy.1803

Li, S.-R., Hao, X., Wang, Y., Sun, B.-J., Bi, J.-H., Zhang, Y.-P., Janzen, F. J., & Du, W.-G. (2018). Female lizards choose warm, moist nests that improve embryonic survivorship and offspring fitness. *Functional Ecology*, 32(2), 416–423. https://doi.org/10.1111/1365-2435.12995

Lister, B. C., & Garcia, A. (2018). Climate-driven declines in arthro-
pod abundance restructure a rainforest food web. *Proceedings of the
National Academy of Sciences of the United States of America*,
115(44), E10397-E10406. https://doi.org/10.1073/pnas.17224
77115

Liu, W., Liu, P., Cui, L., Meng, Y., Tao, S., Han, X., & Sun, B. (2022). Moderate climate warming scenarios during embryonic and post-embryonic stages benefit a cold-climate lizard. *Functional Ecology*, 36(5), 1137–1150. https://doi.org/10.1111/1365-2435.14032

Ljungström, G., Wapstra, E., & Olsson, M. (2015). Sand lizard (*Lacerta agi-
lis*) phenology in a warming world. *BMC Evolutionary Biology*, 15(1),
206. https://doi.org/10.1186/s12862-015-0476-0

Lorioux, S., Angelier, F., & Lourdais, O. (2016). Are glucocorticoids good indicators of pregnancy constraints in a capital breeder? *General and Comparative Endocrinology*, 232, 125–133. https://doi.org/10.1016/jygcen.2016.04.007

Lourdais, O., Lorioux, S., & DeNardo, D. F. (2013). Structural and per-
formance costs of reproduction in a pure capital breeder, the
Children's python Antaresia childreni. *Physiological and Biochemical
Zoology*, 86(2), 176–183. https://doi.org/10.1086/669127

Love, O. P., McGowan, P. O., & Sheriff, M. J. (2013). Maternal adversity and ecological stressors in natural populations: The role of stress axis programming in individuals, with implications for populations and communities. *Functional Ecology*, 27(1), 81–92. https://doi.org/10.1111/j.1365-2435.2012.02040.x

Martin, T. E. (1987). Food as a limit on breeding birds: A life-history per-
spective. *Annual Review of Ecology and Systematics*, 18, 453–487.

Meylan, S., Dufty, A. M., & Clobert, J. (2003). The effect of transdermal
corticosterone application on plasma corticosterone levels in preg-
nant Lacerta vivipara. *Comparative Biochemistry and Physiology Part
A: Molecular & Integrative Physiology*, 134(3), 497–503. https://doi.
org/10.1016/S1095-6433(02)00343-4

Meylan, S., Richard, M., Bauer, S., Haussy, C., & Miles, D. (2013). Costs of mounting an immune response during pregnancy in a lizard. *Physiological and Biochemical Zoology: PBZ*, 86(1), 127–136. https://doi.org/10.1086/668637

Moore, G., Penniket, S., & Cree, A. (2020). Greater basking opportunity and warmer nights during late pregnancy advance modal birth season in a live-bearing gecko, lowering the risk of reduced embryonic condition. *Biological Journal of the Linnean Society*, 130(1), 128–141. https://doi.org/10.1093/biolinnean/blaa017

Moss, J. B., & MacLeod, K. J. (2022). A quantitative synthesis of and pre-
dictive framework for studying winter warming effects in reptiles.
*Oecologia*, 200(1), 259–271. https://doi.org/10.1007/s00442-022- 05251-3

Mugabo, M., Marquis, O., Perret, S., & Le Galliard, J.-F. (2011). Direct and socially-mediated effects of food availability late in life on life-history variation in a short-lived lizard. *Oecologia*, 166, 949–960. https://doi.org/10.1007/s00442-011-1933-0

Mugabo, M., Perret, S., Decencière, B., Meylan, S., & Le Galliard, J.-F. (2015). Density-dependent immunity and parasitism risk in experimental populations of lizards naturally infested by ixodid ticks. *Ecology*, 96(2), 450–460. https://doi.org/10.1890/14-0524.1

Noble, D. W. A., Stenhouse, V., & Schwanz, L. E. (2018). Developmental temperatures and phenotypic plasticity in reptiles: A systematic review and meta-analysis. *Biological Reviews*, 93(1), 72–97. https://doi.org/10.1111/brv.12333

Pearson, P. R., & Warner, D. A. (2018). Early hatching enhances survival despite beneficial phenotypic effects of late season developmental environments. *Proceedings of the Royal Society B: Biological Sciences*, 285(1874), 20180256. https://doi.org/10.1098/rspb.2018.0256

Pettersen, A. K., Nord, A., While, G. M., & Uller, T. (2024). How do fluc-
tuating temperatures alter the cost of development? *Functional
Ecology*, 38(1), 114–125. https://doi.org/10.1111/1365-2435.14450

Price, E. R. (2017). The physiology of lipid storage and use in reptiles. *Biological Reviews*, 92(3), 1406–1426. https://doi.org/10.1111/brv.12288

R Core Team. (2022). R: A language and environment for statistical comput-
ing. R Foundation for Statistical Computing. https://www.R-proje-
ct.org/

Racic, A., Tylan, C., & Langkilde, T. (2020). Effects of temperature on plasma corticosterone in a native lizard. *Scientific Reports*, 10, 16315. https://doi.org/10.1038/s41598-020-73354-z

Rebaudo, F., & Rabhi, V.-B. (2018). Modeling temperature-dependent de-
velopment rate and phenology in insects: Review of major develop-
ments, challenges, and future directions. *Entomologia Experimentalis
et Applicata*, 166(8), 607–617. https://doi.org/10.1111/eea.12693

Rios, F. M., & Zimmerman, L. M. (2015). Immunology of reptiles. In *Encyclopedia of life sciences* (pp. 1–7). John Wiley & Sons, Ltd. https://doi.org/10.1002/9780470015902.a0026260

Robb, G. N., McDonald, R. A., Chamberlain, D. E., & Bearhop, S. (2008). Food for thought: Supplementary feeding as a driver of ecological change in avian populations. *Frontiers in Ecology and the Environment*, 6(9), 476–484. https://doi.org/10.1890/060152

Rutschmann, A., Dupoué, A., Miles, D. B., Megía-Palma, R., Lauden, C., Richard, M., Badiane, A., Rozen-Rechels, D., Brevet, M., Blaimont, P., Meylan, S., Clobert, J., & Le Galliard, J.-F. (2021). Intense nocturnal warming alters growth strategies, colouration and parasite load in a diurnal lizard. *Journal of Animal Ecology*, 90(8), 1864–1877. https://doi.org/10.1111/1365-2656.13502

Rutschmann, A., Miles, D. B., Le Galliard, J.-F., Richard, M., Moulherat, S., Sinervo, B., & Clobert, J. (2016). Climate and habitat interact to shape the thermal reaction norms of breeding phenology across lizard populations. *Journal of Animal Ecology*, 85(2), 457–466. https://doi.org/10.1111/1365-2656.12473

Rutschmann, A., Perry, C., Le Galliard, J.-F., Dupoué, A., Lourdais, O., Guillon, M., Brusch, G., IV, Cote, J., Richard, M., Clobert, J., & Miles, D. B. (2024). Ecological responses of squamate reptiles to nocturnal warming. *Biological Reviews*, 99(2), 598–621. https://doi.org/10.1111/brv.13037

Rutschmann, A., Rozen-Rechels, D., Dupoué, A., Blaimont, P., de Villemereuil, P., Miles, D. B., Richard, M., & Clobert, J. (2020). Climate dependent heating efficiency in the common lizard. *Ecology and Evolution*, 10(15), 8007–8017. https://doi.org/10.1002/ece3.6241

Sacchi, R., Mangiacotti, M., Scali, S., Ghitti, M., & Zuffi, M. A. L. (2017). Effects of colour morph and temperature on immunity in males and females of the Common Wall lizard. *Evolutionary Biology*, 44(4), 496–504. https://doi.org/10.1007/s11692-017-9422-y

Sadok, W., & Jagadish, S. V. K. (2020). The hidden costs of nighttime warming on yields. *Trends in Plant Science*, 25(7), 644–651. https://doi.org/10.1016/j.tplants.2020.02.003

Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. *Nature Methods*, 9(7), 671–675. https://doi.org/10.1038/nmeth.2089

Shine, R. (1980). Costs of reproduction in reptiles. *Oecologia*, 46(1),
92-100.

Sinervo, B., Mendez-de-la-Cruz, F., Miles, D. B., Heulin, B., Bastiaans, E., Villagran-Santa Cruz, M., Lara-Resendiz, R., Martinez-Mendez, N.,
Calderon-Espinosa, M. L., Meza-Lazaro, R. N., Gadsden, H., Avila, L. J., Morando, M., De la Riva, I. J., Sepulveda, P. V., Rocha, C. F. D., Ibarguengoytia, N., Puntriano, C. A., Massot, M., ... Sites, J. W. (2010). Erosion of lizard diversity by climate change and altered thermal niches. *Science*, 328(5980), 894–899. https://doi.org/10.1126/science.1184695

Sorci, G., Swallow, J. G., Garland, T., & Clobert, J. (1995). Quantitative genetics of locomotor speed and endurance in the lizard Lacerta vivipara. *Physiological Zoology*, 68(4), 698–720.

Speights, C. J., Harmon, J. P., & Barton, B. T. (2017). Contrasting the potential effects of daytime versus nighttime warming on insects. *Current Opinion in Insect Science*, 23, 1–6. https://doi.org/10.1016/j.cois.2017.06.005

Stahlschmidt, Z. R., French, S. S., Ahn, A., Webb, A., & Butler, M. W. (2017). A simulated heat wave has diverse effects on immune function and oxidative physiology in the corn Snake (*Pantherophis guttatus*). *Physiological and Biochemical Zoology*, 90(4), 434–444. https://doi.org/10.1086/691315

Stewart, J. R., Heulin, B., & Surget-Groba, Y. (2004). Extraembryonic membrane development in a reproductively bimodal lizard, *Lacerta (Zootoca) vivipara*. *Zoology*, 107(4), 289–314. https://doi.org/10.1016/j.zool.2004.07.004

Storm, M. A., & Angilletta, M. J., Jr. (2007). Rapid assimilation of yolk enhances growth and development of lizard embryos from a cold environment. *Journal of Experimental Biology*, 210(19), 3415–3421. https://doi.org/10.1242/jeb.005652

Sun, B.-J., Li, T., Gao, J., Ma, L., & Du, W.-G. (2015). High incubation temperatures enhance mitochondrial energy metabolism in reptile embryos. *Scientific Reports*, 5, 8861. https://doi.org/10.1038/srep08861

Sun, B.-J., Ma, L., Li, S.-R., Williams, C. M., Wang, Y., Hao, X., & Du, W.-G. (2018). Phenology and the physiological niche are co-adapted in a desert-dwelling lizard. *Functional Ecology*, 32(11), 2520–2530. https://doi.org/10.1111/1365-2435.13201

Swain, R., & Jones, S. M. (2000). Maternal effects associated with gestation conditions in a viviparous lizard, *Niveoscincus metallicus*. *Herpetological Monographs*, 14, 432–440. https://doi.org/10.2307/1467056

Taylor, E. N., DeNardo, D. F., & Jennings, D. H. (2004). Seasonal steroid hormone levels and their relation to reproduction in the Western diamond-backed rattlesnake, *Crotalus atrox* (Serpentes: Viperidae). *General and Comparative Endocrinology*, 136(3), 328–337. https://doi.org/10.1016/j.ygcen.2004.01.008

Thackeray, S. J., Henrys, P. A., Hemming, D., Bell, J. R., Botham, M. S., Burthe, S., Helaouet, P., Johns, D. G., Jones, I. D., Leech, D. I., Mackay, E. B., Massimino, D., Atkinson, S., Bacon, P. J., Brereton, T. M., Carvalho, L., Clutton-Brock, T. H., Duck, C., Edwards, M., ... Wanless, S. (2016). Phenological sensitivity to climate across taxa and trophic levels. *Nature*, 535(7611), 241–245. https://doi.org/10.1038/nature18608

Thomas, M. K., Aranguren-Gassis, M., Kremer, C. T., Gould, M. R., Anderson, K., Klausmeier, C. A., & Litchman, E. (2017). Temperature-nutrient interactions exacerbate sensitivity to warming in phytoplankton. *Global Change Biology*, 23(8), 3269–3280. https://doi.org/10.1111/gcb.13641

Uller, T., & Olsson, M. (2010). Offspring size and timing of hatching determine survival and reproductive output in a lizard. *Oecologia*, 162(3), 663–671. https://doi.org/10.1007/s00442-009-1503-x

Van Damme, R., Bauwens, D., & Verheyen, R. F. (1991). The thermal dependence of feeding behaviour, food consumption and gut-passage time in the lizard *Lacerta vivipara* Jacquin. *Functional Ecology*, 5(4), 507–517. https://doi.org/10.2307/2389633

Van Dyke, J. U., & Beaupre, S. J. (2011). Bioenergetic components of reproductive effort in viviparous snakes: Costs of vitellogenesis exceed costs of pregnancy. *Comparative Biochemistry and Physiology*

Part A: Molecular & Integrative Physiology, 160(4), 504–515. https://doi.org/10.1016/j.cbpa.2011.08.011

Vitasse, Y., Ursenbacher, S., Klein, G., Bohnenstengel, T., Chittaro, Y., Delestrade, A., Monnerat, C., Rebetez, M., Rixen, C., Strebel, N., Schmidt, B. R., Wipf, S., Wohlgemuth, T., Yoccoz, N. G., & Lenoir, J. (2021). Phenological and elevational shifts of plants, animals and fungi under climate change in the European Alps. *Biological Reviews*, 96(5), 1816–1835. https://doi.org/10.1111/brv.12727

Vose, R. S., Easterling, D. R., & Gleason, B. (2005). Maximum and minimum temperature trends for the globe: An update through 2004. *Geophysical Research Letters*, 32(23), L23822. https://doi.org/10.1029/2005GL024379

Wang, J.-H., Zhang, L., Zhang, P.-J., & Sun, B.-J. (2024). Physiological processes through which heatwaves threaten fauna biodiversity. *The Innovation Life*, 2(2), 100069. https://doi.org/10.59717/j.xinn-life.2024.100069

Wang, Y., Zeng, Z.-G., Ma, L., Li, S.-R., & Du, W.-G. (2017). Food restriction affects maternal investment but not neonate phenotypes in a viviparous lizard. *Zoological Research*, 38(2), 81–87. https://doi.org/10.24272/j.issn.2095-8137.2017.011

Wapstra, E., Uller, T., While, G. M., Olsson, M., & Shine, R. (2010). Giving offspring a head start in life: Field and experimental evidence for selection on maternal basking behaviour in lizards. *Journal of Evolutionary Biology*, 23(3), 651–657. https://doi.org/10.1111/j.1420-9101.2009.01924.x

Warner, D. A., & Shine, R. (2007). Fitness of juvenile lizards depends on seasonal timing of hatching, not offspring body size. *Oecologia*, 154(1), 65–73. https://doi.org/10.1007/s00442-007-0809-9

While, G. M., Noble, D. W. A., Uller, T., Warner, D. A., Riley, J. L., Du, W.-G., & Schwanz, L. E. (2018). Patterns of developmental plasticity in response to incubation temperature in reptiles. *Journal of Experimental Zoology Part A: Ecological and Integrative Physiology*, 329(4–5), 162–176. https://doi.org/10.1002/jez.2181

While, G. M., Uller, T., & Wapstra, E. (2009). Offspring performance and the adaptive benefits of prolonged pregnancy: Experimental tests in a viviparous lizard. *Functional Ecology*, 23(4), 818–825. https://doi.org/10.1111/j.1365-2435.2009.01544.x

While, G. M., Williamson, J., Prescott, G., Horváthová, T., Fresnillo, B., Beeton, N. J., Halliwell, B., Michaelides, S., & Uller, T. (2015). Adaptive responses to cool climate promotes persistence of a non-native lizard. *Proceedings of the Royal Society B: Biological Sciences*, 282(1803), 20142638. https://doi.org/10.1098/rspb.2014.2638

Wu, T., Hao, S., Sun, O. J., & Kang, L. (2012). Specificity responses of grasshoppers in temperate grasslands to diel asymmetric warming. *PLoS One*, 7(7), e41764. https://doi.org/10.1371/journal.pone.0041764

Zhang, H., Yu, G., Chen, Q., Wang, Z., & Lin, L. (2013). The effects of ambient temperature and thermoregulation on locomotor performance of newborn guide toad-headed lizards (*Phrynocephalus putjatia*). *Acta Ecologica Sinica*, 33(3), 127–131. https://doi.org/10.1016/j.chnaes.2013.03.001

Zhang, Q., Han, X.-Z., Burraco, P., Hao, X., Teng, L.-W., Liu, Z.-S., Zhang, F.-S., & Du, W.-G. (2023). Telomere length, oxidative stress and their links with growth and survival in a lizard facing climate warming. *Science of the Total Environment*, 891, 164424. https://doi.org/10.1016/j.scitotenv.2023.164424

Zhao, F., Zhang, W., Hoffmann, A. A., & Ma, C.-S. (2014). Night warming on hot days produces novel impacts on development, survival and reproduction in a small arthropod. *Journal of Animal Ecology*, 83(4), 769–778. https://doi.org/10.1111/1365-2656.12196

Zhong, Z., He, B., Chen, H. W., Chen, D., Zhou, T., Dong, W., Xiao, C., Xie, S., Song, X., Guo, L., Ding, R., Zhang, L., Huang, L., Yuan, W., Hao, X., Ji, D., & Zhao, X. (2023). Reversed asymmetric warming of sub-diurnal temperature over land during recent decades. *Nature Communications*, 14(1), 7189. https://doi.org/10.1038/s41467-023-43007-6
SUPPORTING INFORMATION

Additional supporting information can be found online in the Supporting Information section at the end of this article.

**Table S1:** Output of statistical models used to test the effects of gestation stage, experimental treatments and their interaction on female behavioural traits and food consumption during gestation in *Zootoca vivipara*.

**Table S2:** Output of statistical models used to test the effects of ovulation date, experimental treatments and their interaction on female morphological traits during gestation in *Zootoca vivipara*.

**Table S3:** Output of statistical models used to test the effects of ovulation date, two- and three-way interaction between experimental treatments and measurement session on female physiological traits during gestation in *Zootoca vivipara*.

**Table S4:** Output of statistical models used to test the effects of ovulation date, experimental treatments and their interaction on female reproductive traits and juvenile traits at birth in *Zootoca vivipara*.

**Table S5:** Output of statistical models used to test the effects of experimental treatments and their interaction on post-summer survival and morphological traits of females and juveniles in *Zootoca vivipara*.

**Figure S1:** Outdoor macrocosms in which populations of common lizards are maintained.

**Figure S2:** Examples of longitudinal ultrasound scans of the thoracoabdominal region of the same reproductive female *Zootoca vivipara* throughout the reproductive cycle.

**Figure S3:** Average daily variation of temperature in the rearing rooms during the experiment as a function of nocturnal thermal treatment.

**Figure S4:** Relationship between cloacal body temperature and surface body temperature.

**Figure S5:** Effects of nocturnal temperatures and food availability on female surface body temperature during activity, female activity rate and female crickets' consumption throughout gestation.

**How to cite this article:** Bodineau, T., de Villemereuil, P., Lemaire, B., Agostini, S., Decencière, B., Millet, M., Meylan, S., & Le Galliard, J.-F. (2025). A multi-trait evaluation of patterns and fitness consequences of breeding phenology plasticity with nocturnal warming and food restriction in a lizard. *Functional Ecology*, *00*, 1–18. https://doi.org/10.1111/1365-2435.70030