Stress levels of dominants reflect underlying conflicts with subordinates in a cooperatively breeding species
- 286 Downloads
Maintaining dominance status had long been considered to be less stressful than subordination. However, no consistency in stress levels of dominant and subordinate individuals has been demonstrated. Tactics used to achieve and maintain dominance could be determinant. In cooperatively breeding species, conflicts between dominants and subordinates are expected since dominant individuals tend to monopolize reproduction while subordinates seldom reproduce. Reproductive skew models predict that subordinates’ reproductive opportunities are either allotted or subject to competition with dominants. In the former case, no policing of subordinates by dominants is expected. In the latter, dominant should exert a control over the subordinates possibly leading to higher stress levels in dominants than in subordinates, which could be further elevated as the number of potential competitors in the group increases. In the present study, we aimed to test these hypotheses by assessing individual’s stress level using the neutrophils to lymphocytes ratio (N:L) in a wild cooperatively breeding rodent, the Alpine marmot (Marmota marmota). We found that dominants exhibit higher N:L ratio than subordinates and that dominants’ N:L ratio increases with the number of unrelated same-sex subordinates in the group. We conclude that controlling unrelated subordinates is stressful for dominants, as expected under tug-of-war models. These stress patterns reveal conflicting relationships between dominants and subordinates over the reproduction and social status acquisition. This study highlights the influence of the nature, strength, and direction of conflicts on stress levels.
In cooperatively breeding species, reproductive skew models predict that subordinates’ reproductive opportunities are either allotted or subject to competition with dominants and, thus, can modulate the relative stress level between dominants and subordinates. In the first case, no policing of subordinates by dominants is expected, while in the second, dominant should exert a control over the subordinates which should lead to higher stress level in dominants than in subordinates, and particularly when subordinates are unrelated to the dominants. In Alpine marmots, we found that dominants exhibit higher stress level than subordinates and dominants’ stress level increased with the number of unrelated same-sex subordinates. These patterns are in agreement with the predictions of the tug-of war models of reproductive skew and indicate that controlling subordinates is costly for dominants.
KeywordsMarmota marmota Neutrophils to lymphocytes ratio Social rank Dominance Reproductive skew
We warmly thank all students and Earthwatch volunteers involved in marmots captures. We also sincerely thank Dr. G. Florant for carefully editing the manuscript and the two reviewers for their constructive comments.
This work was supported by the “Agence Nationale de la Recherche” (ANR, project ANR-13-JSV7-0005), the “Centre National de la Recherche Scientifique” (CNRS), the “Earthwatch Institute,” and the Rhône-Alpes region (grant 15.005146.01).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
The fieldwork conducted was undertaken after deliverance of the permit number AP n82010/121 by the Préfecture de la Savoie. AC and SL are authorized for experimentation with animals, issued by the French Ministry of Agriculture and Fisheries (diplomas n8R45GRETAF110 and 0ETRY20090520). The protocol has been approved by the ethical committee of the University of Claude Bernard Lyon 1 (n8BH2012-92 V1).
- Abbott DH (1993) Social conflict and reproductive suppression in marmoset and tamarin monkeys. In: Mason WA, Mendoza SP (eds) Primate Social Conflict. SUNY Press, Albany, pp 331–368Google Scholar
- Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T Jr, Sapolsky RM (2003) Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43:67–82. https://doi.org/10.1016/S0018-506X(02)00037-5 PubMedCrossRefGoogle Scholar
- Brown AB (1993) Hematology: principles and procedures, Sixth Edition. Lea & Febiger, Philadelphia, pp 453Google Scholar
- Clutton-Brock TH, Brotherton PNM, Russell AF, O'Riain MJ, Gaynor D, Kansky R, Griffin A, Manser M, Sharpe L, McIlrath G, Small T, Moss A, Monfort S (2001) Cooperation, control, and concession in meerkat groups. Science 291:478–481. https://doi.org/10.1126/science.291.5503.478 PubMedCrossRefGoogle Scholar
- Faulkes CG, Abbott DH (1997) The physiology of a reproductive dictatorship: regulation of male and female reproduction by a single breeding female in colonies of naked mole-rats. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 302–334Google Scholar
- Frame LH, Malcolm JR, Frame GW, Van Lawick H (1979) Social organization of African wild dogs (Lycaon pictus) on the Serengeti Plains, Tanzania 1967–19781. Z Für Tierpsychol 50:225–249. https://doi.org/10.1111/j.1439-0310.1979.tb01030.x CrossRefGoogle Scholar
- Garvy KA, Hellmann JK, Ligocki IY, Reddon AR, Marsh-Rollo SE, Hamilton IM, Balshine S, O'Connor CM (2015) Sex and social status affect territorial defence in a cooperatively breeding cichlid fish, Neolamprologus savoryi. Hydrobiologia 748:75–85. https://doi.org/10.1007/s10750-014-1899-0 CrossRefGoogle Scholar
- Gould L, Ziegler TE, Wittwer DJ (2005) Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Mahafaly reserve, Madagascar. Am J Primatol 67:5–23. https://doi.org/10.1002/ajp.20166 PubMedCrossRefGoogle Scholar
- Hailman JP, McGowan KJ, Woolfenden GE (1994) Role of helpers in the sentinel behaviour of the Florida scrub jay (Aphelocoma c. coerulescens). Ethology 97:119–140. https://doi.org/10.1111/j.1439-0310.1994.tb01034.x CrossRefGoogle Scholar
- Hawkey CM, Dennett TB (1989) A colour atlas of comparative veterinary haematology. Normal and abnormal blood cells in mammals, birds and reptiles, Wolfe publishing limited, IpswichGoogle Scholar
- Henry MD, Hankerson SJ, Siani JM, French JA, Dietz JM (2013) High rates of pregnancy loss by subordinates leads to high reproductive skew in wild golden lion tamarins (Leontopithecus rosalia). Horm Behav 63:675–683. https://doi.org/10.1016/j.yhbeh.2013.02.009 PubMedPubMedCentralCrossRefGoogle Scholar
- Khan MZ (1999) Ultimate and proximate explanations of helping behavior in the red-cockaded woodpecker (Picoides borealis). PhD thesis, Virginia Polytechnic Institute and State UniversityGoogle Scholar
- Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
- Lape JJ (1990) Mate guarding in the red-cockaded woodpecker. MSc thesis, North Carolina State UniversityGoogle Scholar
- Nakamichi M, Koyama N (2000) Intra-troop affiliative relationships of females with newborn infants in wild ring-tailed lemurs (Lemur catta). Am J Primatol 50:187–203. https://doi.org/10.1002/(SICI)1098-2345(200003)50:3<187::AID-AJP2>3.0.CO;2-Q PubMedCrossRefGoogle Scholar
- Perrin C (1993) Organisation socio-spatiale et distribution des activités chez la marmotte alpine (Marmota marmota Linné 1758). PhD thesis, Université Paris 7Google Scholar
- Reeve HK (1998) Game theory, reproductive skew, and nepotism. In: Dugatkin LA, Reeve HK (eds) Game theory and animal behaviour. Oxford University Press, Oxford, pp 118–145Google Scholar
- Romero LM, Romero RC (2002) Corticosterone responses in wild birds: The importance of rapid initial sampling. Condor 104:129–135. https://doi.org/10.1650/0010-5422(2002)104[0129,CRIWBT]2.0.CO;2Google Scholar
- Rood JP (1978) Dwarf mongoose helpers at the den. Z Tierpsychol 48:277–287. https://doi.org/10.1111/j.1439-0310.1978.tb00260.x CrossRefGoogle Scholar
- Rubenstein DR (2006) The evolution of the social and mating systems of the plural cooperatively breeding superb starling, Lamprotornis superbus. PhD thesis, Cornell UniversityGoogle Scholar
- Sanderson JL, Nichols HJ, Marshall HH, Vitikainen EIK, Thompson FJ, Walker SL, Cant MA, Young AJ (2015) Elevated glucocorticoid concentrations during gestation predict reduced reproductive success in subordinate female banded mongooses. Biol Lett 11:20150620. https://doi.org/10.1098/rsbl.2015.0620 PubMedPubMedCentralCrossRefGoogle Scholar
- Schaffner CM, French JA (2004) Behavioral and endocrine responses in male marmosets to the establishment of multimale breeding groups: evidence for non-monopolizing facultative polyandry. Int J Primatol 25:709–732. https://doi.org/10.1023/B:IJOP.0000023582.34854.43 CrossRefGoogle Scholar
- Sillero-Zubiri C, Macdonald DW (1998) Scent-marking and territorial behaviour of Ethiopian wolves Canis simensis. J Zool 245:351–361. https://doi.org/10.1111/j.1469-7998.1998.tb00110.x CrossRefGoogle Scholar
- Smith TE, French JA (1997) Social and reproductive conditions modulate urinary cortisol excretion in black tufted-ear marmosets (Callithrix kuhli). Am J Primatol 42:253–267. https://doi.org/10.1002/(SICI)1098-2345(1997)42:4<253::AID-AJP1>3.0.CO;2-W PubMedCrossRefGoogle Scholar
- van Kesteren F, Sillero-Zubiri C, Millar R, Argaw K, Macdonald DW, Paris M (2012) Sex, stress and social status: patterns in fecal testosterone and glucocorticoid metabolites in male Ethiopian wolves. Gen Comp Endocrinol 179:30–37. https://doi.org/10.1016/j.ygcen.2012.07.016 PubMedCrossRefGoogle Scholar
- Woolfenden GE, Fitzpatrick JW (1986) Sexual asymmetries in the life history of the Florida scrub jay. In: Rubenstein DI, Wrangham RW (eds) Ecological aspects of social evolution: birds and mammals. Princeton University Press, Princeton, pp 87–107Google Scholar
- Woolfenden GE, Fitzpatrick JW (1994) The Florida scrub jay: demography of a cooperative-breeding bird. Princeton University Press, PrincetonGoogle Scholar