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Effects of early thermal environment on the behavior and learning of a lizard with bimodal reproduction

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Abstract

Early developmental temperatures influence the physiology and behavior of reptiles, with important consequences for their fitness and survival. For example, many viviparous lizards are cold adapted which may restrict their activity times during the reproductive season, increasing their susceptibility to global warming. However, it is unclear if and how lizards with different reproductive modes (oviparity vs. viviparity) can respond to rising temperatures by modifying their life-history traits. We examined the effect of developmental temperatures on hatchling behavior and learning in viviparous and oviparous populations of the lizard Saiphos equalis to test whether their reproductive behavior can buffer against rising temperatures. Gravid females from both populations were subjected to current or projected end-of-century (future) thermal environments to evaluate differences in the exploratory, foraging and antipredator behavior, and spatial learning ability of their offspring. We found that viviparous lizards were more exploratory and had a less-pronounced antipredator response than oviparous lizards. Regardless of the mode of reproduction, elevated temperatures reduced the exploratory behavior of hatchling lizards. Elevated temperatures also reduced the foraging efficiency of oviparous, but not viviparous, hatchlings. Finally, future-gestated oviparous hatchlings were more likely to choose the correct refuge and made fewer mistakes in a spatial learning task; however, we found only weak evidence of spatial learning in S. equalis. Our results suggest that although global warming is likely to have a negative impact on phenotypic traits, in S. equalis, some of these effects may be ameliorated by maternal behavior and/or physiological responses during pregnancy, particularly in viviparous populations.

Significance statement

Computational modeling studies suggest that live-bearing lizards (viviparous) are more vulnerable to global warming compared with egg-laying ones (oviparous). However, there is little experimental evidence showing that viviparous species are indeed at a greater risk of extinction. Using a lizard species that has both oviparous and viviparous populations, we tested the effect of high developmental temperatures (projected for 2100) on the behavior and learning of their offspring. We found that elevated temperatures had a stronger negative effect on egg-laying lizards by producing hatchlings with lower foraging efficiency. Our results suggest that viviparous mothers can ameliorate some of the effects of global warming on their offspring. Moreover, our study suggests that if live bearers are indeed more vulnerable to global warming, it is likely not due to maladaptive behavior in offspring, but rather, to other causes that affect pregnant females.

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Acknowledgments

We thank Sergio Naretto and Cooper Van Der Waal for their assistance in the field and the laboratory, as well as Catarina Vila Pouca for her suggestions during the writing of the manuscript. We thank Camilla Whittington and Scott Parker for their advice regarding animal capture and identification. Finally, we are grateful to two anonymous reviewers for the comments which improved the manuscript.

Data availability statement

The datasets generated during the current study (raw data and R script code) are available through the Open Science Framework (OSF; https://osf.io/9zhmq/).

Funding

This work was supported by the Australasian Society for the Study of Animal Behaviour (2018 Student Grants) and the Australian Museum (2018/2019 Peter Rankin Trust Fund for Herpetology). This work was performed in the Plant Growth Facility (PGF) at Macquarie University. IB was supported by an international Research Training Program (iRTP) scholarship from the Australian Government and Macquarie University. VD and RL were supported by Le CROUS (Centre Régional des OEuvres Universitaires et Scolaires) de Strasbourg and University of Strasburg (France).

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Contributions

Conceptualization: MJW and IB. Methodology: IB, VD, and RL. Formal analysis: IB. Resources: IB and MJW. Data curation: IB. Writing—original draft: IB, VD, and RL. Writing—review and editing: IB and MJW. Visualization: IB. Supervision: IB and MJW. Funding acquisition: IB and MJW.

Corresponding author

Correspondence to Iván Beltrán.

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The authors declare that they have no conflict of interest.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures were in accordance with the ethical standards of the institution or practice at which the studies were conducted. Collection of animals was approved by the New South Wales National Parks and Wildlife Service, Office of Environment and Heritage (OEH; License No. SL101962). The experiments were approved by the Macquarie University Animal Ethics Committee (ARA 2017-029).

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Beltrán, I., Loiseleur, R., Durand, V. et al. Effects of early thermal environment on the behavior and learning of a lizard with bimodal reproduction. Behav Ecol Sociobiol 74, 73 (2020). https://doi.org/10.1007/s00265-020-02849-6

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