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Long distance runners in the marine realm: New insights into genetic diversity, kin relationships and social fidelity of Indian Ocean male sperm whales

Justine Girardet, Francois Sarano, Gaëtan Richard, View ORCID ProfilePaul Tixier, View ORCID ProfileChristophe Guinet, View ORCID ProfileAlana Alexander, Véronique Sarano-Simon, Hugues Vitry, Axel Preud’homme, René Heuzey, Ana M. Garcia-Cegarra, View ORCID ProfileOlivier Adam, Bénédicte Madon, View ORCID ProfileJean-Luc Jung
doi: https://doi.org/10.1101/2021.04.23.440733
Justine Girardet
1Université de Brest, Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, ISYEB, Brest, France
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Francois Sarano
2Longitude 181, Valence, France
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Gaëtan Richard
3Université de Brest, Institut Universitaire Européen de la Mer, CNRS (UMS3113), Technopôle Brest Iroise, rue Dumont d’Urville, Plouzané, France
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Paul Tixier
4MARBEC Université de Montpellier-CNRS-IFREMER-IRD, Avenue Jean Monnet, Sète, France
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Christophe Guinet
5Centre d’Études Biologiques de Chizé, UMR 7372 - CNRS & Université de La Rochelle, Villiers-en-Bois, France
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Alana Alexander
6Department of Anatomy, University of Otago, Dunedin, New Zealand
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Véronique Sarano-Simon
2Longitude 181, Valence, France
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Hugues Vitry
7Marine Megafauna Conservation Organisation, Ile Maurice
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Axel Preud’homme
7Marine Megafauna Conservation Organisation, Ile Maurice
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René Heuzey
8Label Bleu Production, Marseille, France
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Ana M. Garcia-Cegarra
9Centro de Investigación de Fauna Marina y Avistamiento de Cetáceos, CIFAMAC, Mejillones, Chile and Departamento de Ciencias Básicas, Facultad de Ciencias, Universidad Santo Tomás, Antofagasta, Chile
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Olivier Adam
10Sorbonne Université, CNRS, Institut Jean Le Rond d’Alembert, UMR 7190, Paris, France
11Institute of Neurosciences Paris-Saclay, Bioacoustics Team, CNRS UMR 9197, Université Paris Sud, Orsay, France
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Bénédicte Madon
12Université de Brest, AMURE - Aménagement des Usages des Ressources et des Espaces marins et littoraux - Centre de droit et d’économie de la mer, Plouzané, France
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Jean-Luc Jung
1Université de Brest, Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, ISYEB, Brest, France
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  • For correspondence: jean-luc.jung@mnhn.fr
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Abstract

Adult male sperm whales (Physeter macrocephalus) are long distance runners of the marine realm, feeding in high latitudes and mating in tropical and subtropical waters where stable social groups of females and immatures live. Several areas of uncertainty still limit our understanding of their social and breeding behaviour, in particular concerning the potential existence of geographical and/or social fidelities.

In this study, using underwater observation and sloughed-skin sampling, we looked for male social fidelity to a specific matrilineal sperm whale group near Mauritius. In addition, we captured a wider picture of kin relationships and genetic diversity of male sperm whales in the Indian Ocean thanks to biopsies of eight unique individuals taken in a feeding ground near the Kerguelen and Crozet Archipelagos (Southern Indian Ocean).

Twenty-six adult male sperm whales, of which 13 were sampled, were identified when socializing with adult females and immatures off Mauritius. Long-term underwater observation recorded several noteworthy social interactions between adult males and adult females and/or immatures. We identified seven possible male recaptures over different years (three by direct observation, and four at the gametic level), which supports a certain level of male social fidelity. Several first- and second-degree kin relationships were highlighted between members of the social unit and adult males, confirming that some of the adult males observed in Mauritian waters are reproductive. Male social philopatry to their natal group can be excluded, as none of the males sampled shared the haplotype characteristic of the matrilineal social group. Mitochondrial DNA control region haplotype and nucleotide diversities calculated over the 21 total male sperm whales sampled were similar to values found by others in the Indian Ocean.

Our study strongly supports the existence of some levels of male sperm whale social fidelity, not directed to their social group of birth, in the Indian Ocean. Males sampled in breeding and feeding grounds are linked by kin relationships. Our results support a model of male mediated gene flow occurring at the level of the whole Indian Ocean, likely interconnected with large-scale geographical fidelity to ocean basin, and a small-scale social fidelity to matrilineal social groups.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted April 26, 2021.
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Long distance runners in the marine realm: New insights into genetic diversity, kin relationships and social fidelity of Indian Ocean male sperm whales
Justine Girardet, Francois Sarano, Gaëtan Richard, Paul Tixier, Christophe Guinet, Alana Alexander, Véronique Sarano-Simon, Hugues Vitry, Axel Preud’homme, René Heuzey, Ana M. Garcia-Cegarra, Olivier Adam, Bénédicte Madon, Jean-Luc Jung
bioRxiv 2021.04.23.440733; doi: https://doi.org/10.1101/2021.04.23.440733
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Long distance runners in the marine realm: New insights into genetic diversity, kin relationships and social fidelity of Indian Ocean male sperm whales
Justine Girardet, Francois Sarano, Gaëtan Richard, Paul Tixier, Christophe Guinet, Alana Alexander, Véronique Sarano-Simon, Hugues Vitry, Axel Preud’homme, René Heuzey, Ana M. Garcia-Cegarra, Olivier Adam, Bénédicte Madon, Jean-Luc Jung
bioRxiv 2021.04.23.440733; doi: https://doi.org/10.1101/2021.04.23.440733

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