Infant Mortality Risk and Paternity Certainty Are Associated with Postnatal Maternal Behavior toward Adult Male Mountain Gorillas (Gorilla beringei beringei)

RESEARCH ARTICLE Infant Mortality Risk and Paternity Certainty Are Associated with Postnatal Maternal Behavior toward Adult Male Mountain Gorillas (Gorilla beringei beringei) Stacy Rosenbaum1*, Jean Paul Hirwa2, Joan B. Silk3,4, Linda Vigilant5, Tara S. Stoinski6 1 Department of Anthropology, University of California Los Angeles, Los Angeles, California, United States of America, 2 Dian Fossey Gorilla Fund International, Musanze, Rwanda, 3 School of Human Evolution and Social Change, Arizona State University, Tempe, Arizona, United States of America, 4 Institute for Human Origins, Arizona State University, Tempe, Arizona, United States of America, 5 Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany, 6 Dian Fossey Gorilla Fund International, Atlanta, Georgia, United States of America * OPEN ACCESS Citation: Rosenbaum S, Hirwa JP, Silk JB, Vigilant L, Stoinski TS (2016) Infant Mortality Risk and Paternity Certainty Are Associated with Postnatal Maternal Behavior toward Adult Male Mountain Gorillas (Gorilla beringei beringei). PLoS ONE 11(2): e0147441. doi:10.1371/journal.pone.0147441 Editor: Elissa Z. Cameron, University of Tasmania, AUSTRALIA Received: May 19, 2015 Accepted: January 3, 2016 Published: February 10, 2016 Copyright: © 2016 Rosenbaum et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data are from studies included in the long-term Karisoke Research Center database maintained and owned by the Dian Fossey Gorilla Fund International, Atlanta GA USA. Data the authors used may be accessed by permission of the Dian Fossey Gorilla Fund International, by contacting Dr. Damien Caillaud (). Funding: This work was supported by an LSB Leakey Foundation Research Grant, http://www. leakeyfoundation.org/research-grants/ (to SR & JS); a National Science Foundation SBE Doctoral Dissertation Improvement Grant #1122321 http:// Abstract Sexually selected infanticide is an important source of infant mortality in many mammalian species. In species with long-term male-female associations, females may benefit from male protection against infanticidal outsiders. We tested whether mountain gorilla (Gorilla beringei beringei) mothers in single and multi-male groups monitored by the Dian Fossey Gorilla Fund’s Karisoke Research Center actively facilitated interactions between their infants and a potentially protective male. We also evaluated the criteria mothers in multimale groups used to choose a preferred male social partner. In single male groups, where infanticide risk and paternity certainty are high, females with infants <1 year old spent more time near and affiliated more with males than females without young infants. In multi-male groups, where infanticide rates and paternity certainty are lower, mothers with new infants exhibited few behavioral changes toward males. The sole notable change was that females with young infants proportionally increased their time near males they previously spent little time near when compared to males they had previously preferred, perhaps to encourage paternity uncertainty and deter aggression. Rank was a much better predictor of females’ social partner choice than paternity. Older infants (2–3 years) in multi-male groups mirrored their mothers’ preferences for individual male social partners; 89% spent the most time in close proximity to the male their mother had spent the most time near when they were <1 year old. Observed discrepancies between female behavior in single and multi-male groups likely reflect different levels of postpartum intersexual conflict; in groups where paternity certainty and infanticide risk are both high, male-female interests align and females behave accordingly. This highlights the importance of considering individual and group-level variation when evaluating intersexual conflict across the reproductive cycle. PLOS ONE | DOI:10.1371/journal.pone.0147441 February 10, 2016 1 / 24 Maternal Behavior and Male-Infant Relationships in Gorillas www.nsf.gov/funding/pgm_summ.jsp?pims_id=13453 (to SR); and a Wenner-Gren Foundation for Anthropological Research Dissertation Research Grant #201101446 http://www.wennergren.org/ programs/dissertation-fieldwork-grants (to SR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Introduction According to the sexually selected infanticide hypothesis, males kill infants when the infant’s death shortens the interval until the mother’s next conception, and the infanticidal male is likely to sire the mother’s next offspring [1]. In mammalian species in which the duration of lactation exceeds the duration of gestation, infanticide is common [2]. Infanticide accounts for a high proportion of infant mortality in a variety of species, including geladas (60%, [3]); solitary southern sea lions (23%, [4]); mountain gorillas (21%, [5]); lions (27%, [6]); chacma baboons; (31–76%, [7]); European rabbits (12%, [8]); wolverines (32%, [9]); white-faced capuchins (43–68%, [10]); and gibbons (83%, [11]). Sexually selected infanticide is believed to be a major selective pressure in primates, carnivores, and rodents (reviewed in [12, 13, 14]). Female mammals use a variety of tactics to counter the threat of infanticide and reduce its impact on their fitness (reviewed in [15]). These strategies are deployed from the time of conception to weaning. In some species with promiscuous mating systems, females mate with multiple partners around the time of likely conception and during pregnancy in an apparent effort to confuse paternity (baboons: [16]; California ground squirrels: [17]; Japanese macaques: [18]; patas monkeys: [19]; bank voles: [20]; reviewed in [15, 21]). In other species, females terminate pregnancies when infanticide risk is high (voles & mice: [22, 23]; feral horses: [24]; gelada baboons: [25, 26]). After birth, females use maternal aggression (e.g. mice: [27]; ringtailed lemurs: [28]), coalitionary aggression (lions: [29, 30]; chimpanzees: [31]; blue monkeys: [32]), avoidance of potentially infanticidal males (alpine marmots: [33]; brown bears: [34]; ursine colobus: [35]), territoriality (white-footed and deer mice: [36]), and/or accelerated weaning (vervet monkeys: [37]; baboons: [38]) to reduce the risk to their infants. Agent-based models and empirical evidence strongly support the hypothesis that lasting associations between males and females are an evolved anti-infanticide strategy in both monogamous and promiscuous species [11, 39, 40, 41, 42] (but see [43] for an alternative view). In monogamous systems, pair bonding across the entire reproductive cycle minimizes (...truncated)