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Benefits of paternal thermoregulation: male midwife toads select warmer temperature to shorten embryonic development

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Abstract

Parental thermoregulation can provide an efficient way to control embryonic temperature and optimize developmental durations and timing. To date, most studies on parental thermal effects have focused on maternal influences, because of the predominant role of females for parental care in most systems. Yet, paternal thermal effects are equally expected to occur in species that display paternal care to the progeny. We studied the midwife toad, a small amphibian with exclusive male parental care and terrestrial eggs transport. We examined the variations of body temperature of egg-carrying males and non-reproductive individuals in the field, and determined their thermal preferences in a laboratory thermal gradient. We also experimentally examined the influence of temperature on embryonic development durations across five treatments (16, 18, 20, 22, 24 °C). In support of our predictions, we detected a shift in thermal preferences with reproduction, with carrying males preferring higher temperatures than non-carrying ones. Field monitoring indicated that carrying males used diurnal shelters early in the season when thermal conditions were more constraining. Meanwhile, they minimized overheating risks by avoiding shelters with high substrate temperature. Finally, we detected a marked thermal dependence of embryonic development, suggesting potential phenological benefits of paternal thermoregulation in this species.

Significance statement

Paternal thermal care is well known among birds during incubation but male thermal care and thermal effects remain virtually unstudied among terrestrial ectotherms. In ectotherms, body temperature directly depends on the thermal environment and behavioral thermoregulation can influence developmental durations and offspring traits. We studied the midwife toad, a species that display exclusive male parental care with terrestrial egg transport. Our results demonstrate that carrying males selected preferred higher temperatures than non-reproductive individuals in a thermal gradient but also avoided thermal extreme in the field. The duration of development was considerably shortened at the temperature selected by reproductive male. Our study provides evidences of active paternal thermoregulation for an amphibian species with exclusive male parental care.

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Data availability

The datasets generated during and/or analyzed during the current study are available as supplementary material.

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Acknowledgements

The authors thank Lauriane Bégué, Juliette Scheuer, and Lisa Poncet for participation in data collection. We warmly thank Pascal Marteau and the sawmill company “Marteau-Bois” for allowing to access to their site. We also thank Jean-Pierre Vacher and the two reviewers for their very constructive comments that have considerably improved the manuscript.

Funding

This study received the financial and technical support from the Centre National de la Recherche Scientifique (CNRS) and was funded by La Rochelle Université (PhD grant to LL) and by the Region Nouvelle-Aquitaine under the “Aquastress” project (2018-1R20214 to OL).

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Contributions

LL carried out the field work and lab experiments, participated in the statistical analyses, and drafted the manuscript; OL and FB conceived and coordinated the study, participated in data analysis, and critically revised the manuscript. All authors gave final approval for publication and agree to be held accountable for the work performed therein.

Corresponding author

Correspondence to Olivier Lourdais.

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Ethics approval

All applicable national, and/or institutional guidelines for the use of animals were followed. This study was performed in accordance with French laws relative to capture, transport, and experiments on Alytes obstetricans (DREAL permit #04022016) and all procedures were approved by an independent ethical committee (Apafis #14193–2018032114365130 v3).

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All authors gave final approval for publication and agree to be held accountable for the work performed therein.

Competing interests

The authors declare no competing interests.

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Communicated by C. R Gabor.

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Lange, L., Brischoux, F. & Lourdais, O. Benefits of paternal thermoregulation: male midwife toads select warmer temperature to shorten embryonic development. Behav Ecol Sociobiol 76, 48 (2022). https://doi.org/10.1007/s00265-022-03155-z

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  • DOI: https://doi.org/10.1007/s00265-022-03155-z

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