Phenotypic plasticity may help lizards cope with increasingly variable temperatures

Ma, Liang; Sun, Bao‐Jun; Li, Xing-han; Du, Wei‐Guo

doi:10.1007/s00442-018-4127-1

Cited by 14 publications

(15 citation statements)

References 65 publications

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“…Given the thermal dependence of food intake and energy budget in animals (Brown et al., 2004; Du et al., 2000; Speakman, 2005), mothers may be able to ‘programme’ the food assimilation efficiency and metabolic capacity of offspring to increase energy income and therefore the threshold of energy limitation under climate warming. For example, females exposed to increasing or highly variable temperatures produce offspring with higher metabolic rates and higher growth rates in marine sticklebacks and our study species E. multiocellata (Ma et al., 2018; Shama et al., 2014).…”

Section: Discussionmentioning

confidence: 86%

“…First, maternal behavioural thermoregulation plays an important role in responding to temperature variation or climate warming in ectothermic animals because effective thermoregulators may buffer the impact of extreme temperatures behaviourally, and thereby have time for intra‐ and inter‐generation plasticity and evolutionary adaptation before they become extinct (Huey et al., 2012; Kearney et al., 2009; Ladyman et al., 2003). For example, maternal behavioural thermoregulation may enable females to manipulate developmental temperatures of embryos that profoundly affect the preferred body temperature, metabolic rate, and probably growth of offspring in E. multiocellata and other lizards (Ma et al., 2018; Paranjpe et al., 2013). Second, maternal effect may mediate oxidative stress, a potentially widespread mechanism underlying life‐history trade‐offs, to shape offspring growth and survival (Monaghan et al., 2009; Vitikainen et al., 2016).…”

Section: Discussionmentioning

confidence: 99%

“…growth and survival) in response to temperature change in lizards. In viviparous species, offspring from females with longer access to basking grew faster than those with shorter basking periods (Cree & Hare, 2016; Wapstra, 2000); offspring from females exposed to highly variable temperatures had higher growth rates than those from females under less variable temperatures (Ma et al., 2018). Moreover, previous studies on anticipatory maternal effects have shown that offspring from parents exposed to a simulated warm climate have higher growth rates or survivorship under similar warm conditions than offspring exposed to a present climate scenario in oviparous lizards (Schwanz et al., 2020; Sun et al., 2018).…”

Section: Introductionmentioning

confidence: 99%

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Grow fast but don't die young: Maternal effects mediate life‐history trade‐offs of lizards under climate warming

Xia

Zou

Han

et al. 2021

Journal of Animal Ecology

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As postulated by life‐history theory, not all life‐history traits can be maximized simultaneously. In ectothermic animals, climate warming is predicted to increase growth rates, but at a cost to overall life span. Maternal effects are expected to mediate this life‐history trade‐off, but such effects have not yet been explicitly elucidated. To understand maternal effects on the life‐history responses to climate warming in lizard offspring, we conducted a manipulative field experiment on a desert‐dwelling viviparous lacertid lizard Eremias multiocellata, using open‐top chambers in a factorial design (maternal warm climate and maternal present climate treatments × offspring warm climate and offspring present climate treatments). We found that the maternal warm climate treatment had little impact on the physiological and life‐history traits of adult females (i.e. metabolic rate, reproductive output, growth and survival). However, the offspring warm climate treatment significantly affected offspring growth, and both maternal and offspring warm climate treatments interacted to affect offspring survival. Offspring from the warm climate treatment grew faster than those from the present climate treatment. However, the offspring warm climate treatment significantly decreased the survival rate of offspring from maternal present climate treatment, but not for those from the maternal warm climate treatment. Our study demonstrates that maternal effects mediate the trade‐off between growth and survival of offspring lizards, allowing them to grow fast without a concurrent cost of low survival rate (short life span). These findings stress the importance of adaptive maternal effects in buffering the impact of climate warming on organisms, which may help us to accurately predict the vulnerability of populations and species to future warming climates.

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Section: Discussionmentioning

confidence: 86%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Grow fast but don't die young: Maternal effects mediate life‐history trade‐offs of lizards under climate warming

Xia

Zou

Han

et al. 2021

Journal of Animal Ecology

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“…To eliminate the effects of circadian rhythms on metabolic rates, all the trials were conducted between 10:00 AM to 6:00 PM. To minimize the effects of food digestion on metabolic rates, we removed the food and enabled the lizards to fast for at least 12 h prior to the trials started (Ma et al, 2018; Sun, Ma, et al, 2018). Oxygen consumption and carbon dioxide production were used for metabolic rate calculation.…”

Section: Methodsmentioning

confidence: 99%

Higher metabolic plasticity in temperate compared to tropical lizards suggests increased resilience to climate change

Sun

Williams

et al. 2022

Ecological Monographs

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Patterns in functional diversity of organisms at large spatial scales can provide insight into possible responses to future climate change, but it remains a challenge to link large-scale patterns at the population or species level to their underlying physiological mechanisms at the individual level. The climate variability hypothesis predicts that temperate ectotherms will be less vulnerable to climate warming compared with tropical ectotherms, due to their superior acclimatization capacity.However, metabolic acclimatization occurs over multiple levels, from the enzyme and cellular level, through organ systems, to whole-organism metabolic rate (from this point forwards biological hierarchy). Previous studies have focused on one or a few levels of the biological hierarchy, leaving us without a general understanding of how metabolic acclimatization might differ between tropical and temperate species. Here, we investigated thermal acclimation of three species of Takydromus lizards distributed along a broad latitudinal gradient in China, by studying metabolic modifications at the level of the whole organism, organ, mitochondria, metabolome, and proteome. As predicted by the climate variability hypothesis, the two temperate species T. septentrionalis and T. wolteri had an enhanced acclimation response at the whole organism level compared with the tropical species T. sexlineatus, as measured by respiratory gas exchange rates. However, the mechanisms by which whole organism performance was modified was strikingly different in the two temperate species: widespread T. septentrionalis modified organ sizes, whereas the narrowly distributed T. wolteri relied on mitochondrial, proteomic and metabolomic regulation. We suggest that these two mechanisms of thermal acclimatization may represent general strategies used by ectotherms, with distinct ecological costs and benefits. Lacking either of these mechanisms of thermal acclimatization capacity, the tropical species is likely to have increased vulnerability to climate change.

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“…Empirical studies have demonstrated that experimental warming can increase reproductive frequency in oviparous squamates for 2–3 clutches (Du et al 2005b, Lu et al 2018), which also appear in some sites according to our prediction. However, reproductive frequency in viviparous species has not been shown to increase under experimental warming (Ma et al 2018b), although some viviparous species (not including Sceloporus lizards) in warmer regions tend to have a larger probability of producing two litters (or more in very few cases) rather than one per year (Mesquita et al 2016a, Schwarzkopf et al 2016). Under climate change, the reproductive frequency of viviparous species will increase at few sites (4.49% sites) only, where gravid females were estimated to not reproduce every year in recent climates (Fig.…”

Section: Discussionmentioning

confidence: 99%

Variable impacts on reproductive energetics may render oviparous squamates more vulnerable to climate warming than viviparous species

Levy

Buckley

et al. 2022

Ecography

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Squamate reptiles exhibit two reproductive modes: oviparity and viviparity. Existing large‐scale studies suggest that viviparous species are more vulnerable to climate warming based on viviparous species occupying relatively colder environments, which are predicted to decline in availability under climate warming. However, oviparous and viviparous squamates are geographically widespread and their distributions often overlap. Are oviparous or viviparous squamates more vulnerable to climate warming when they inhabit similar thermal environments? We used Sceloporus lizards in North America as a model system to predict the impact of climate warming on oviparous and viviparous species in sympatric zones. We used mechanistic models to quantify the changes in maternal energy balance (MEB) and offspring energy balance (OEB) under a climate warming scenario. We then projected the fitness impacts of future climate warming based on estimates of MEB and OEB. Under a climate warming scenario (RCP8.5), oviparous females are predicted to increase reproductive frequency more than viviparous females, which restricts time for postpartum energy accumulation before the end of the season and decreases MEB. Under climate warming, OEB of oviparous species increased more than viviparous species, but the increases were less geographically widespread. Interestingly, the developmental success and OEB of oviparous species are predicted to decline at some sites under climate warming, which is not predicted to happen for viviparous species. Our results highlight that oviparous species will respond more variably to climate warming than viviparous species. More specifically, oviparous species in hot areas with high temperature variation may be especially vulnerable under climate warming compared to sympatric viviparous species.

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Phenotypic plasticity may help lizards cope with increasingly variable temperatures

Cited by 14 publications

References 65 publications

Grow fast but don't die young: Maternal effects mediate life‐history trade‐offs of lizards under climate warming

Grow fast but don't die young: Maternal effects mediate life‐history trade‐offs of lizards under climate warming

Higher metabolic plasticity in temperate compared to tropical lizards suggests increased resilience to climate change

Variable impacts on reproductive energetics may render oviparous squamates more vulnerable to climate warming than viviparous species

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