Ecology

The effect of dominance rank on female reproductive success in social mammals

10.24072/pcjournal.158 - Peer Community Journal, Volume 2 (2022), article no. e48.

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Life in social groups, while potentially providing social benefits, inevitably leads to conflict among group members. In many social mammals, such conflicts lead to the formation of dominance hierarchies, where high-ranking individuals consistently outcompete other group members. Given that competition is a fundamental tenet of the theory of natural selection, it is generally assumed that high-ranking individuals have higher reproductive success than lower-ranking individuals. Previous reviews have indicated large variation across populations on the potential effect of dominance rank on reproductive success in female mammals. Here, we perform a meta-analysis based on 444 effect sizes from 187 studies on 86 mammal species to investigate how life-history, ecology and sociality modulate the relationship between female dominance rank and fitness. As predicted, we found that (1) dominance rank is generally positively associated with reproductive success, independent of the approach different studies have taken to answer this question; and that (2) the relationship between rank and reproductive success is conditional on life-history mechanisms, with higher effects of dominance rank on reproductive output than on survival, particularly in species with high reproductive investment. Contrary to our predictions, (3) the fitness benefits to high-ranking females appear consistent across ecological conditions rather than increasing when resources decrease. Instead, we found that the social environment consistently mitigates rank differences on reproductive success by modulating female competition, with, as predicted, (4) dominant females showing higher reproductive success than subordinates in two different types of societies: first, effect sizes are highest when females live in cooperatively breeding groups composed of a single dominant female and one or more subordinate females; second, they are also elevated when females form differentiated relationships which occurs when groups are composed of unrelated females. Our findings indicate that obtaining a high ranking position in a social group consistently provides female mammals with fitness benefits, even though future studies might show lower effects given various biases in the literature we were able to access, including, but not restricted to, a publication bias. They further draw a complex landscape of the level of social inequality across mammalian societies, reflected by variation in the benefits of social dominance, which appears to be shaped by reproductive and social competition more than by ecological competition.

Published online:
DOI: 10.24072/pcjournal.158
Shivani 1, 2; Huchard, Elise 3; Lukas, Dieter 1

1 Department of Human Behavior, Ecology & Culture; Max Planck Institute for Evolutionary Anthropology - Leipzig, Germany
2 Indian Institute of Science Education and Research Kolkata - Mohanpur, West Bengal, India
3 Institut des Sciences de l’Evolution de Montpellier, Centre National de la Recherche Scientifique, Université de Montpellier - Montpellier, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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Shivani; Huchard, Elise; Lukas, Dieter. The effect of dominance rank on female reproductive success in social mammals. Peer Community Journal, Volume 2 (2022), article  no. e48. doi : 10.24072/pcjournal.158. https://peercommunityjournal.org/articles/10.24072/pcjournal.158/

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100101

[1] Alexander, R. D. The Evolution of Social Behavior, Annual Review of Ecology and Systematics, Volume 5 (1974) no. 1, pp. 325-383 | DOI

[2] Altmann, J.; Alberts, S. C. Variability in reproductive success viewed from a life-history perspective in baboons, American Journal of Human Biology, Volume 15 (2003) no. 3, pp. 401-409 | DOI

[3] Balasubramaniam, K. N.; Dittmar, K.; Berman, C. M.; Butovskaya, M.; Cooper, M. A.; Majolo, B.; Ogawa, H.; Schino, G.; Thierry, B.; De Waal, F. B. M. Hierarchical Steepness, Counter-Aggression, and Macaque Social Style Scale, American Journal of Primatology, Volume 74 (2012) no. 10, pp. 915-925 | DOI

[4] Barsbai, T.; Lukas, D.; Pondorfer, A. Local convergence of behavior across species, Science, Volume 371 (2021) no. 6526, pp. 292-295 | DOI

[5] Bercovitch, F. B. Social stratification, social strategies, and reproductive success in primates, Ethology and Sociobiology, Volume 12 (1991) no. 4, pp. 315-333 | DOI

[6] Fedigan, L.; Bergstrom, M. Dominance among female white-faced capuchin monkeys (Cebus capucinus): hierarchical linearity, nepotism, strength and stability, Behaviour, Volume 147 (2010) no. 7, pp. 899-931 | DOI

[7] Botero, C. A.; Dor, R.; McCain, C. M.; Safran, R. J. Environmental harshness is positively correlated with intraspecific divergence in mammals and birds, Molecular Ecology, Volume 23 (2014) no. 2, pp. 259-268 | DOI

[8] Brown, G. R.; Silk, J. B. Reconsidering the null hypothesis: Is maternal rank associated with birth sex ratios in primate groups?, Proceedings of the National Academy of Sciences, Volume 99 (2002) no. 17, pp. 11252-11255 | DOI

[9] Burgin, C. J.; Colella, J. P.; Kahn, P. L.; Upham, N. S. How many species of mammals are there?, Journal of Mammalogy, Volume 99 (2018) no. 1, pp. 1-14 | DOI

[10] Cameron, E. Z.; Setsaas, T. H.; Linklater, W. L. Social bonds between unrelated females increase reproductive success in feral horses, Proceedings of the National Academy of Sciences, Volume 106 (2009) no. 33, pp. 13850-13853 | DOI

[11] Cant, M. A. Costly young and reproductive skew in animal societies, Behavioral Ecology, Volume 10 (1999) no. 2, pp. 178-184 | DOI

[12] Cavigelli, S.; Dubovick, T.; Levash, W.; Jolly, A.; Pitts, A. Female dominance status and fecal corticoids in a cooperative breeder with low reproductive skew: ring-tailed lemurs (Lemur catta), Hormones and Behavior, Volume 43 (2003) no. 1, pp. 166-179 | DOI

[13] Chamberlain, S. A.; Hovick, S. M.; Dibble, C. J.; Rasmussen, N. L.; Van Allen, B. G.; Maitner, B. S.; Ahern, J. R.; Bell-Dereske, L. P.; Roy, C. L.; Meza-Lopez, M.; Carrillo, J.; Siemann, E.; Lajeunesse, M. J.; Whitney, K. D. Does phylogeny matter? Assessing the impact of phylogenetic information in ecological meta-analysis, Ecology Letters, Volume 15 (2012) no. 6, pp. 627-636 | DOI

[14] Cheney, D. L.; Seyfarth, R. M.; Fischer, J.; Beehner, J.; Bergman, T.; Johnson, S. E.; Kitchen, D. M.; Palombit, R. A.; Rendall, D.; Silk, J. B. Factors Affecting Reproduction and Mortality Among Baboons in the Okavango Delta, Botswana, International Journal of Primatology, Volume 25 (2004) no. 2, pp. 401-428 | DOI

[15] Clutton‐Brock, T.; Huchard, E. Social competition and its consequences in female mammals, Journal of Zoology, Volume 289 (2013) no. 3, pp. 151-171 | DOI

[16] Clutton‐Brock, T. H.; Hodge, S. J.; Flower, T. P.; Spong, G. F.; Young, A. J. Adaptive Suppression of Subordinate Reproduction in Cooperative Mammals, The American Naturalist, Volume 176 (2010) no. 5, pp. 664-673 | DOI

[17] Cowlishaw, G.; Dunbar, R. Dominance rank and mating success in male primates, Animal Behaviour, Volume 41 (1991) no. 6, pp. 1045-1056 | DOI

[18] Datta, S. The acquisition of dominance among free-ranging rhesus monkey siblings, Animal Behaviour, Volume 36 (1988) no. 3, pp. 754-772 | DOI

[19] Digby, L. J.; Ferrari, S. F.; Saltzman, W. The role of competition in cooperatively breeding species In: Primates in Perspective (2006), pp. 85-106

[20] Drummond, A. J.; Suchard, M. A.; Xie, D.; Rambaut, A. Bayesian Phylogenetics with BEAUti and the BEAST 1.7, Molecular Biology and Evolution, Volume 29 (2012) no. 8, pp. 1969-1973 | DOI

[21] Ellis, L. Dominance and reproductive success among nonhuman animals: A cross-species comparison, Ethology and Sociobiology, Volume 16 (1995) no. 4, pp. 257-333 | DOI

[22] Fedigan, L. M. Dominance and reproductive success in primates, American Journal of Physical Anthropology, Volume 26 (1983) no. S1, pp. 91-129 | DOI

[23] Fedigan, L. M.; Jack, K. M. Sexual Conflict in White-Faced Capuchins, Evolution's Empress, Oxford University Press, 2013, pp. 281-303 | DOI

[24] Fortunato, L. Lineal kinship organization in cross-specific perspective, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 374 (2019) no. 1780 | DOI

[25] Frank, L. G. Social organization of the spotted hyaena Crocuta crocuta. II. Dominance and reproduction, Animal Behaviour, Volume 34 (1986) no. 5, pp. 1510-1527 | DOI

[26] Giles, S. L.; Nicol, C. J.; Harris, P. A.; Rands, S. A. Dominance rank is associated with body condition in outdoor-living domestic horses (Equus caballus), Applied Animal Behaviour Science, Volume 166 (2015), pp. 71-79 | DOI

[27] Holekamp, K. E.; Smale, L. Dominance Acquisition During Mammalian Social Development: The “Inheritance” of Maternal Rank, American Zoologist, Volume 31 (1991) no. 2, pp. 306-317 | DOI

[28] Holekamp, K. E.; Smith, J. E.; Strelioff, C. C.; Van Horn, R. C.; Watts, H. E. Society, demography and genetic structure in the spotted hyena, Molecular Ecology, Volume 21 (2012) no. 3, pp. 613-632 | DOI

[29] Huchard, E.; English, S.; Bell, M. B. V.; Thavarajah, N.; Clutton-Brock, T. Competitive growth in a cooperative mammal, Nature, Volume 533 (2016) no. 7604, pp. 532-534 | DOI

[30] Isaac, J. L. Potential causes and life-history consequences of sexual size dimorphism in mammals, Mammal Review, Volume 35 (2005) no. 1, pp. 101-115 | DOI

[31] Jarman, P. Mating system and sexcul dimorphism in large terrestrial, mammalian herbivores, Biological Reviews, Volume 58 (1983) no. 4, pp. 485-520 | DOI

[32] Jones, K. E.; Bielby, J.; Cardillo, M.; Fritz, S. A.; O'Dell, J.; Orme, C. D. L.; Safi, K.; Sechrest, W.; Boakes, E. H.; Carbone, C.; Connolly, C.; Cutts, M. J.; Foster, J. K.; Grenyer, R.; Habib, M.; Plaster, C. A.; Price, S. A.; Rigby, E. A.; Rist, J.; Teacher, A.; Bininda-Emonds, O. R. P.; Gittleman, J. L.; Mace, G. M.; Purvis, A. PanTHERIA: a species‐level database of life history, ecology, and geography of extant and recently extinct mammals, Ecology, Volume 90 (2009) no. 9, p. 2648-2648 | DOI

[33] Kappeler, P. M.; Nunn, C. L.; Vining, A. Q.; Goodman, S. M. Evolutionary dynamics of sexual size dimorphism in non-volant mammals following their independent colonization of Madagascar, Scientific Reports, Volume 9 (2019) no. 1 | DOI

[34] Kokko, H.; Johnstone, R. A. Social queuing in animal societies: a dynamic model of reproductive skew, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 266 (1999) no. 1419, pp. 571-578 | DOI

[35] Kurz, S. Statistical Rethinking with Brms, Ggplot2, and the Tidyverse, 2019 (https://solomonkurz.netlify.com/post/bayesian-meta-analysis/)

[36] Lajeunesse, M. J. Recovering Missing or Partial Data from Studies: a Survey of Conversions and Imputations for Meta-analysis, Handbook of Meta-analysis in Ecology and Evolution, Princeton University Press, 2013 | DOI

[37] Lakens, D. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs, Frontiers in Psychology, Volume 4 (2013) | DOI

[38] Lea, A. J.; Learn, N. H.; Theus, M. J.; Altmann, J.; Alberts, S. C. Complex sources of variance in female dominance rank in a nepotistic society, Animal Behaviour, Volume 94 (2014), pp. 87-99 | DOI

[39] Lemaître, J.-F.; Ronget, V.; Gaillard, J.-M. Female reproductive senescence across mammals: A high diversity of patterns modulated by life history and mating traits, Mechanisms of Ageing and Development, Volume 192 (2020) | DOI

[40] Lewontin, R. C.; Cohen, D. On population growth in a randomly varying environment, Proceedings of the National Academy of Sciences, Volume 62 (1969) no. 4, pp. 1056-1060 | DOI

[41] Loison, A.; Gaillard, J. M.; Pélabon, C.; Yoccoz, N. G. What factors shape sexual size dimorphism in ungulates?, Evolutionary Ecology Research, Volume 1 (1999) (https://www.evolutionary-ecology.com/issues/v01n05/jjar1019.pdf)

[42] Lukas, D.; Clutton-Brock, T. Cooperative breeding and monogamy in mammalian societies, Proceedings of the Royal Society B: Biological Sciences, Volume 279 (2012) no. 1736, pp. 2151-2156 | DOI

[43] Lukas, D.; Clutton-Brock, T. Costs of mating competition limit male lifetime breeding success in polygynous mammals, Proceedings of the Royal Society B: Biological Sciences, Volume 281 (2014) no. 1786 | DOI

[44] Lukas, D.; Clutton-Brock, T. Climate and the distribution of cooperative breeding in mammals, Royal Society Open Science, Volume 4 (2017) no. 1 | DOI

[45] Lukas, D.; Clutton-Brock, T. Social complexity and kinship in animal societies, Ecology Letters, Volume 21 (2018) no. 8, pp. 1129-1134 | DOI

[46] Lukas, D.; Huchard, E. The evolution of infanticide by males in mammalian societies, Science, Volume 346 (2014) no. 6211, pp. 841-844 | DOI

[47] Lukas, D.; Huchard, E. The evolution of infanticide by females in mammals, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 374 (2019) no. 1780 | DOI

[48] Lukas, d.; Reynolds, v.; Boesch, c.; Vigilant, l. To what extent does living in a group mean living with kin?, Molecular Ecology, Volume 14 (2005) no. 7, pp. 2181-2196 | DOI

[49] Majolo, B.; Lehmann, J.; de Bortoli Vizioli, A.; Schino, G. Fitness-related benefits of dominance in primates, American Journal of Physical Anthropology, Volume 147 (2012) no. 4, pp. 652-660 | DOI

[50] McElreath, R. Statistical Rethinking, Chapman and Hall/CRC, 2020 | DOI

[51] Nakagawa, S.; Lagisz, M.; Jennions, M. D.; Koricheva, J.; Noble, D. W. A.; Parker, T. H.; Sánchez‐Tójar, A.; Yang, Y.; O'Dea, R. E. Methods for testing publication bias in ecological and evolutionary meta‐analyses, Methods in Ecology and Evolution, Volume 13 (2022) no. 1, pp. 4-21 | DOI

[52] Nakagawa, S.; Lagisz, M.; O'Dea, R. E.; Rutkowska, J.; Yang, Y.; Noble, D. W. A.; Senior, A. M. The orchard plot: Cultivating a forest plot for use in ecology, evolution, and beyond, Research Synthesis Methods, Volume 12 (2021) no. 1, pp. 4-12 | DOI

[53] Nakagawa, S.; Santos, E. S. A. Methodological issues and advances in biological meta-analysis, Evolutionary Ecology, Volume 26 (2012) no. 5, pp. 1253-1274 | DOI

[54] Pandit, S. A.; van Schaik, C. P. A model for leveling coalitions among primate males: toward a theory of egalitarianism, Behavioral Ecology and Sociobiology, Volume 55 (2003) no. 2, pp. 161-168 | DOI

[55] Paradis, E.; Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R, Bioinformatics, Volume 35 (2019) no. 3, pp. 526-528 | DOI

[56] Preston, C.; Ashby, D.; Smyth, R. Adjusting for publication bias: modelling the selection process, Journal of Evaluation in Clinical Practice, Volume 10 (2004) no. 2, pp. 313-322 | DOI

[57] Pusey, A. Magnitude and sources of variation in female reproductive performance In: The evolution of primate societies (2012), pp. 343-366

[58] Pusey, A.; Williams, J.; Goodall, J. The Influence of Dominance Rank on the Reproductive Success of Female Chimpanzees, Science, Volume 277 (1997) no. 5327, pp. 828-831 | DOI

[59] R Core Team R: A Language and Environment for Statistical Computing. Vienna, Austria, 2020 (https://www.R-project.org/)

[60] Riehl, C. Kinship and Incest Avoidance Drive Patterns of Reproductive Skew in Cooperatively Breeding Birds, The American Naturalist, Volume 190 (2017) no. 6, pp. 774-785 | DOI

[61] Rubenstein, D. R.; Botero, C. A.; Lacey, E. A. Discrete but variable structure of animal societies leads to the false perception of a social continuum, Royal Society Open Science, Volume 3 (2016) no. 5 | DOI

[62] Rutberg, A. T.; Greenberg, S. A. Dominance, aggression frequencies and modes of aggressive competition in feral pony mares, Animal Behaviour, Volume 40 (1990) no. 2, pp. 322-331 | DOI

[63] Smith, R. J. Statistics of sexual size dimorphism, Journal of Human Evolution, Volume 36 (1999) no. 4, pp. 423-458 | DOI

[64] Smith, R. J.; Cheverud, J. M. International Journal of Primatology, 23 (2002) no. 5, pp. 1095-1135 | DOI

[65] Snyder, R. E.; Ellner, S. P. Pluck or Luck: Does Trait Variation or Chance Drive Variation in Lifetime Reproductive Success?, The American Naturalist, Volume 191 (2018) no. 4 | DOI

[66] Solomon, N. G.; French, J. A. Cooperative breeding in mammals, Cambridge University Press, 1997

[67] Stan Development Team Stan Modeling Language Users Guide and Reference Manual, 2020 (https://mc-stan.org)

[68] Stockley, P. Female multiple mating behaviour, early reproductive failure and litter size variation in mammals, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 270 (2003) no. 1512, pp. 271-278 | DOI

[69] Stockley, P.; Bro-Jørgensen, J. Female competition and its evolutionary consequences in mammals, Biological Reviews, Volume 86 (2011) no. 2, pp. 341-366 | DOI

[70] Strauss, E. D.; DeCasien, A. R.; Galindo, G.; Hobson, E. A.; Shizuka, D.; Curley, J. P. DomArchive: a century of published dominance data, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 377 (2022) no. 1845 | DOI

[71] Swedell, L.; Leedom, L.; Saunders, J.; Pines, M. Sexual conflict in a polygynous primate: costs and benefits of a male-imposed mating system, Behavioral Ecology and Sociobiology, Volume 68 (2014) no. 2, pp. 263-273 | DOI

[72] Thierry, B. Unity in diversity: Lessons from macaque societies, Evolutionary Anthropology: Issues, News, and Reviews, Volume 16 (2007) no. 6, pp. 224-238 | DOI

[73] Thouless, C.; Guinness, F. Conflict between red deer hinds: the winner always wins, Animal Behaviour, Volume 34 (1986) no. 4, pp. 1166-1171 | DOI

[74] Tibbetts, E. A.; Pardo-Sanchez, J.; Weise, C. The establishment and maintenance of dominance hierarchies, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 377 (2022) no. 1845 | DOI

[75] Upham, N. S.; Esselstyn, J. A.; Jetz, W. Inferring the mammal tree: Species-level sets of phylogenies for questions in ecology, evolution, and conservation, PLOS Biology, Volume 17 (2019) no. 12 | DOI

[76] Van Noordwijk, M. A.; Van Schaik, C. P. Scramble and Contest in Feeding Competition Among Female Long-Tailed Macaques (Macaca Fascicularis), Behaviour, Volume 105 (1988) no. 1-2, pp. 77-98 | DOI

[77] Vehrencamp, S. L. A model for the evolution of despotic versus egalitarian societies, Animal Behaviour, Volume 31 (1983) no. 3, pp. 667-682 | DOI

[78] Viechtbauer, W. Conducting Meta-Analyses in R with the metafor Package, Journal of Statistical Software, Volume 36 (2010) no. 3 | DOI

[79] Ward, A.; Webster, M. Sociality: The Behaviour of Group-Living Animals, Springer International Publishing, Cham, 2016 | DOI

[80] West, M. J. Foundress Associations in Polistine Wasps: Dominance Hierarchies and the Evolution of Social Behavior, Science, Volume 157 (1967) no. 3796, pp. 1584-1585 | DOI

[81] Williams, G. C. Adaptation and Natural Selection, Princeton University Press, 2018 | DOI

[82] Wilman, H.; Belmaker, J.; Simpson, J.; de la Rosa, C.; Rivadeneira, M. M.; Jetz, W. EltonTraits 1.0: Species-level foraging attributes of the world's birds and mammals, Ecology, Volume 95 (2014) no. 7, p. 2027-2027 | DOI

[83] Wilson, D. B. Practical Meta-Analysis Effect Size Calculator [Online Calculator], 2019 (https://www.campbellcollaboration.org/escalc/html/EffectSizeCalculator-Home.php)

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