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Sibling differences in litter huddle position contribute to overall variation in weaning mass in a small mammal

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Abstract

In altricial, litter-bearing species, huddling together with siblings during early life is a vital strategy to maintain a sufficiently high and stable body temperature. In this context, individual differences in huddling behavior within litters have been emphasized, as pups regularly occupying more central positions have relatively higher body temperatures, have quicker access to the mother’s nipples during nursing, and consequently show greater growth. However, it is not known whether such positive effects of a central litter huddle position on within-litter differences in growth translate into an overall higher weaning mass, taking into account strong contributors to among-litter growth variation, such as litter size and maternal parity. We used path analysis to investigate causal relations among these variables, based on data from 150 domestic rabbit pups from 24 litters. Our results confirmed positive, indirect effects of pups’ central litter huddle position on within-litter differences in early growth. This positive effect of a central litter huddle position also contributed to explaining a significant part of the overall across-litter variance in weaning body mass, apparent even when controlling for the direct negative effect of litter size, the direct positive effects of birth mass, and the lower offspring growth in primiparous compared to multiparous mothers. Thus, the results underline the key role of individual differences in litter huddle position in shaping within-litter but also overall variation in early growth. This might constitute an important mechanism accounting for how the positive association between body mass at birth and early growth is mediated in altricial, polytocous mammals.

Significance statement

Huddling together with siblings during early life saves energy and thus can contribute to early growth in small, altricial mammals. However, this strategy can also lead to individual differences within the litter, as heavier pups typically occupy energetically more favorable positions in the center of the huddle. In our study, we show and compare the different causal pathways underlying this effect. Most importantly, our analysis shows that advantages in early growth arising from a more central position in the litter huddle are also apparent when comparing pups across all litters—even though there is typically a notable variation in growth among different litters, for example due to litter size and maternal (parity) effects. In conclusion, the results underline the key role of sibling interactions within the litter in shaping differences in early growth, with potential fitness consequences during later life.

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Data availability

The authors confirm that the data supporting the study will be made available by the corresponding authors upon reasonable request.

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Acknowledgments

For support in obtaining data and carrying out the experiments, we thank the students and lab colleagues Humberto Pérez Roldán, Yesenia Fernández Pérez, Verónica Reyes Meza, and Esmeralda García Torres. We are grateful for the helpful and constructive comments of two anonymous reviewers. We also thank Carolina Rojas for long-term administrative support.

Funding

Financial support was provided by the Mexican funding agencies Consejo Nacional de Ciencia y Tecnología (CONACyT: 48692-Q, ECS-218193; AZZ-407512) and Dirección General de Asunto del Personal Académico (DGAPA: IN205513; IN212416), by the Franco-Mexican researcher exchange program Consejo Nacional de Ciencia y Tecnología-Asociación Nacional de Universidades e Instituciones de Educación Superior—Evaluation-orientation de la Coopération Scientifique Nord (CONACyT-ANUIES-ECOS Nord: M14A02), and by the Institut Fédératif de la Recherche Biomédicale IFRB. AB and RH received travel grants from the Université Paris 13, France (“Professeur Invité” program 2018, 2019).

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Authors and Affiliations

  1. Centro Tlaxcala de Biología de la Conducta, Universidad Autónoma de Tlaxcala, Tlaxcala, Mexico

    José Alfredo Zepeda & Amando Bautista

  2. Doctorado en Ciencias Biológicas, Universidad Autónoma de Tlaxcala, Tlaxcala, Mexico

    José Alfredo Zepeda

  3. Preparatoria Alfonso Calderón Moreno, Benemérita Universidad Autónoma de Puebla, Puebla, Mexico

    José Alfredo Zepeda

  4. Laboratoire d’Ethologie Expérimentale et Comparée EA 4443, Université Paris 13, Sorbonne Paris Cité, F-93430, Villetaneuse, France

    Heiko G. Rödel & Raquel Monclús

  5. Insituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Mexico City, Mexico

    Robyn Hudson

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  1. José Alfredo Zepeda
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  2. Heiko G. Rödel
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  3. Raquel Monclús
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  4. Robyn Hudson
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  5. Amando Bautista
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Correspondence to Heiko G. Rödel or Amando Bautista.

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Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed were in accordance with the ethical standards of the institution where the studies were conducted and were approved by the Animal Care and Use Committee of the Centro Tlaxcala de Biología de la Conducta, protocol 056-2014-2018.

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Communicated by A. I. Schulte-Hostedde

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Zepeda, J.A., Rödel, H.G., Monclús, R. et al. Sibling differences in litter huddle position contribute to overall variation in weaning mass in a small mammal. Behav Ecol Sociobiol 73, 165 (2019). https://doi.org/10.1007/s00265-019-2777-6

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