Wild bonobo and chimpanzee females exhibit broadly similar patterns of behavioral maturation but some evidence for divergence.
Pan
development
ecological risk aversion
infanticide
self-domestication
Journal
American journal of physical anthropology
ISSN: 1096-8644
Titre abrégé: Am J Phys Anthropol
Pays: United States
ID NLM: 0400654
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
09
05
2019
revised:
21
08
2019
accepted:
13
09
2019
pubmed:
7
10
2019
medline:
28
8
2020
entrez:
7
10
2019
Statut:
ppublish
Résumé
Primates exhibit variation in rates of growth and development. Variation in female growth and development across ape species appears to be explained by the Ecological Risk Aversion Hypothesis (ERAH). Indeed, existing data on variation in somatic growth and reproductive maturation between humans' closest living ape relatives, bonobos and chimpanzees, appear to be consistent with this hypothesis. However, existing data on behavioral maturation between the two species appear to contradict this hypothesis. We present novel behavioral data on infant and juvenile females from wild populations of both species in order to further evaluate predictions of the ERAH as it relates to the speed of behavioral maturation. We analyzed 3 years of behavioral data on 17 female bonobos (<8 years of age) from LuiKotale, Democratic Republic of the Congo and 40 years of behavioral data on 30 age-matched female chimpanzees from Gombe, Tanzania. We compared the timing of (a) the attainment of independence from mothers and (b) the development of social skills using the following proxies: proximity between females and their mothers and the time that females spent engaged in eating, suckling, social play, social grooming, and riding on their mothers. We did not find species differences in the proportion of time that females spent in contact with their mothers or engaged in eating, suckling, social play, or social grooming. Female bonobos spent more time riding on their mothers than did female chimpanzees. Female bonobos spent more time at distances greater than 5 m from their mothers during the ages of 3-8 years, but females did not differ during the ages of 0-3 years. Behavioral maturation is largely similar between females of the two species based on the ages and proxies considered herein. We propose alternative explanations for the differences that we found in proximity and riding that do not invoke differences in underlying rates of maturation.
Types de publication
Comparative Study
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
100-109Subventions
Organisme : Explorers Club Washington Group
Pays : International
Organisme : George Washington University
Pays : International
Organisme : Jane Goodall Institute
Pays : International
Organisme : Leakey Foundation
Pays : International
Organisme : Leo S. Guthman Fund
Pays : International
Organisme : Max-Planck-Gesellschaft
Pays : International
Organisme : National Geographic Society
Pays : International
Organisme : NICHD NIH HHS
ID : R00 HD057992
Pays : United States
Organisme : Royal Zoological Society of Antwerp
Pays : International
Organisme : Sigma Xi
Pays : International
Organisme : The Federal Ministiry of Education and Research (Germany)
Pays : International
Organisme : Wenner-Gren Foundation
Pays : International
Informations de copyright
© 2019 Wiley Periodicals, Inc.
Références
Altmann, J. (1980). Baboon mothers and infants. Chicago, IL: University of Chicago Press.
Altmann, J., & Alberts, S. C. (2003). Variability in reproductive success viewed from a life-history perspective in baboons. American Journal of Human Biology, 15(3), 401-409.
Bădescu, I., Wikberg, E. C., MacDonald, L. J., Fox, S. A., Vayro, J. V., Crotty, A., & Sicotte, P. (2016). Infanticide pressure accelerates infant development in a wild primate. Animal Behaviour, 114, 231-239.
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2014). Fitting linear mixed-effects models using lme4. ArXiv Preprint ArXiv:1406.5823.
Behringer, V., Deschner, T., Murtagh, R., Stevens, J. M. G., & Hohmann, G. (2014). Age-related changes in thyroid hormone levels of bonobos and chimpanzees indicate heterochrony in development. Journal of Human Evolution, 66, 83-88.
Breuer, T., Hockemba, M. B.-N., Olejniczak, C., Parnell, R. J., & Stokes, E. J. (2009). Physical maturation, life-history classes and age estimates of free-ranging western gorillas-insights from Mbeli Bai, Republic of Congo. American Journal of Primatology, 71(2), 106-119.
Charnov, E. L., & Berrigan, D. (1993). Why do female primates have such long lifespans and so few babies? Or life in the slow lane. Evolutionary Anthropology: Issues, News, and Reviews, 1(6), 191-194.
Colmenares, F., & Gomendio, M. (1988). Changes in female reproductive condition following male take-overs in a colony of Hamadryas and hybrid baboons. Folia Primatologica, 50(3-4), 157-174.
De Lathouwers, M., & Van Elsacker, L. (2005). Reproductive parameters of female Pan paniscus and P. troglodytes: Quality versus quantity. International Journal of Primatology, 26(1), 55-71.
De Lathouwers, M., & Van Elsacker, L. (2006). Comparing infant and juvenile behavior in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): A preliminary study. Primates, 47(4), 287-293.
Doran, D. M. (1993). Comparative locomotor behavior of chimpanzees and bonobos: The influence of morphology on locomotion. American Journal of Physical Anthropology, 91(1), 83-98.
Emery Thompson, M. (2013). Reproductive ecology of female chimpanzees. American Journal of Primatology, 75(3), 222-237.
Emery Thompson, M., Muller, M. N., & Wrangham, R. W. (2012). The energetics of lactation and the return to fecundity in wild chimpanzees. Behavioral Ecology, 23(6), 1234-1241.
Fairbanks, L. A., & McGuire, M. T. (1987). Mother-infant relationships in Vervet monkeys: Response to new adult males. International Journal of Primatology, 8(4), 351-366.
Fairbanks, L. A. (1993). Juvenile vervet monkeys: Establishing relationships and practicing skills for the future. In L. A. Fairbanks & M. E. Pereira (Eds.), Juvenile primates: Life history, development, and behavior (pp. 211-227). New York: Oxford University Press.
Fox, J., Weisberg, S., Adler, D., Bates, D., Baud-Bovy, G., Ellison, S., … Zeileis, A. (2012). Package car. Vienna, AU: R foundation for statistical computing.
Fröhlich, M., Kuchenbuch, P., Müller, G., Fruth, B., Furuichi, T., Wittig, R. M., & Pika, S. (2016). Unpeeling the layers of language: Bonobos and chimpanzees engage in cooperative turn-taking sequences. Scientific Reports, 6(1), 25887.
Furuichi, T. (1989). Social interactions and the life history of female Pan paniscus in Wamba, Zaire. International Journal of Primatology, 10(3), 173-197.
Furuichi, T. (2009). Factors underlying party size differences between chimpanzees and bonobos: A review and hypotheses for future study. Primates, 50(3), 197-209.
Furuichi, T., Idani, G., Ihobe, H., Kuroda, S., Kitamura, K., Mori, A., … Kano, T. (1998). Population dynamics of wild bonobos. International Journal of Primatology, 19(6), 1029-1043.
Galbany, J., Abavandimwe, D., Vakiener, M., Eckardt, W., Mudakikwa, A., Ndagijimana, F., … McFarlin, S. C. (2017). Body growth and life history in wild mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda. American Journal of Physical Anthropology, 163(3), 570-590.
Garber, P. A., & Leigh, S. R. (1997). Ontogenetic variation in small-bodied New World primates: Implications for patterns of reproduction and infant care. Folia Primatologica, 68(1), 1-22.
Gruber, T., & Clay, Z. (2016). A comparison between bonobos and chimpanzees: A review and update. Evolutionary Anthropology, 25(5), 239-252.
Han, S., Andrés, A. M., Marques-Bonet, T., & Kuhlwilm, M. (2019). Genetic variation in Pan species is shaped by demographic history and Harbors lineage-specific functions. Genome Biology and Evolution, 11(4), 1178-1191.
Hare, B., Wobber, V., & Wrangham, R. (2012). The self-domestication hypothesis: Evolution of bonobo psychology is due to selection against aggression. Animal Behaviour, 83(3), 573-585.
Harvey, P. H., & Clutton-Brock, T. H. (1985). Life history variation in primates. Evolution, 39(3), 559-581.
Hinde, R. A. (1971). Development of social behavior. In A. M. Schrier & F. Stollnitz (Eds.), Behavior of nonhuman primates (Vol. 3, pp. 1-68). Amsterdam, NL: Elsevier.
Hohmann, G., Fowler, A., Sommer, V., & Ortmann, S. (2006). Frugivory and gregariousness of Salonga bonobos and Gashaka chimpanzees: The influence of abundance and nutritional quality of fruit. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 123-159). Cambridge, UK: Cambridge University Press.
Hohmann, G., & Fruth, B. (1996). Food sharing and status in unprovisioned bonobos. In P. Wiessner & W. Schiefenhövel (Eds.), Food and the status quest (pp. 47-67). Providence: Berghahn Books.
Hohmann, G., & Fruth, B. (2002). Dynamics in social organization of bonobos (Pan paniscus). In Behavioural diversity in chimpanzees and bonobos (pp. 138-150). Cambridge, UK: Cambridge University Press.
Hohmann, G., Ortmann, S., Remer, T., & Fruth, B. (2019). Fishing for iodine: What aquatic foraging by bonobos tells us about human evolution. BMC Zoology, 4(1), 5.
Hohmann, G., Vigilant, L., Mundry, R., Behringer, V., & Surbeck, M. (2019). Aggression by male bonobos against immature individuals does not fit with predictions of infanticide. Aggressive Behavior, 45(3), 300-309.
Janson, C. H., & van Schaik, C. P. (1993). Ecological risk aversion in juvenile primates: Slow and steady wins the race. In M. E. Pereira & L. A. Fairbanks (Eds.), Juvenile primates: Life history, development, and behavior (pp. 57-74). New York: Oxford University Press.
Joffe, T. H. (1997). Social pressures have selected for an extended juvenile period in primates. Journal of Human Evolution, 32(6), 593-605.
Kappeler, P. M. (1996). Causes and consequences of life-history variation among strepsirhine primates. The American Naturalist, 148(5), 868-891.
Knott, C. (2001). Female reproductive ecology of the apes: Implications for human evolution. In Reproductive ecology and human evolution (pp. 429-463). New York: Routledge.
Koops, K., Furuichi, T., & Hashimoto, C. (2015). Chimpanzees and bonobos differ in intrinsic motivation for tool use. Scientific Reports, 5, 1-10.
Kuroda, S. (1989). Developmental retardation and behavioral characteristics of pygmy chimpanzees. In Understanding chimpanzees (pp. 184-193). Cambridge, MA: Harvard University Press.
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82(13), 1-26.
Lehmann, J., & Boesch, C. (2009). Sociality of the dispersing sex: The nature of social bonds in west African female chimpanzees, Pan troglodytes. Animal Behaviour, 77(2), 377-387.
Leigh, S. R., & Bernstein, R. M. (2006). Ontogeny, life history, and maternal investment in baboons. In Reproduction and fitness in baboons: Behavioral, ecological, and life history perspectives (pp. 225-255). New York: Springer.
Leigh, S. R., & Shea, B. T. (1996). Ontogeny of body size variation in African apes. American Journal of Physical Anthropology, 99, 43-65.
Lenth, R. (2018). Emmeans: Estimated marginal means, aka least-squares means. R Package Version, 1(1).
Lonsdorf, E. V. (2017). Sex differences in nonhuman primate behavioral development. Journal of Neuroscience Research, 95(1-2), 213-221.
Lonsdorf, E. V., Markham, A. C., Heintz, M. R., Anderson, K. E., Ciuk, D. J., Goodall, J., & Murray, C. M. (2014). Sex differences in wild chimpanzee behavior emerge during infancy. PLoS One, 9(6), 1-9.
Malenky, R. K., & Wrangham, R. W. (1994). A quantitative comparison of terrestrial herbaceous food consumption by Pan paniscus in the Lomako Forest, Zaire, and Pan troglodytes in the Kibale Forest, Uganda. American Journal of Primatology, 32(1), 1-12.
McFarlin, S. C., Barks, S. K., Tocheri, M. W., Massey, J. S., Eriksen, A. B., Fawcett, K. A., … Sherwood, C. C. (2013). Early brain growth cessation in wild virunga mountain gorillas (Gorilla beringei beringei). American Journal of Primatology, 75(5), 450-463.
Meredith, S. L. (2013). Identifying proximate and ultimate causation in the development of primate sex-typed social behavior. In Building babies (pp. 411-433). New York: Springer.
Miller, J. A., Pusey, A. E., Gilby, I. C., Schroepfer-Walker, K., Markham, A. C., & Murray, C. M. (2014). Competing for space: Female chimpanzees are more aggressive inside than outside their core areas. Animal Behaviour, 87, 147-152.
Moscovice, L. R., Douglas, P. H., Martinez-Iñigo, L., Surbeck, M., Vigilant, L., & Hohmann, G. (2017). Stable and fluctuating social preferences and implications for cooperation among female bonobos at LuiKotale, Salonga National Park, DRC. American Journal of Physical Anthropology, 163(1), 158-172.
Murray, C. M., Eberly, L. E., & Pusey, A. E. (2006). Foraging strategies as a function of season and rank among wild female chimpanzees (Pan troglodytes). Behavioral Ecology, 17(6), 1020-1028.
Nowell, A. A., & Fletcher, A. W. (2007). Development of independence from the mother in Gorilla gorilla gorilla. International Journal of Primatology, 28(2), 441-455.
Nurmi, N. O., Hohmann, G., Goldstone, L. G., Deschner, T., & Schülke, O. (2018). The “tolerant chimpanzee”-Towards the costs and benefits of sociality in female bonobos. Behavioral Ecology, 29(6), 1325-1339.
Otali, E., & Gilchrist, J. S. (2006). Why chimpanzee (Pan troglodytes schweinfurthii) mothers are less gregarious than nonmothers and males: The infant safety hypothesis. Behavioral Ecology and Sociobiology, 59(4), 561-570.
Pusey, A. E., Oehlert, G. W., Williams, J. M., & Goodall, J. (2005). Influence of ecological and social factors on body mass of wild chimpanzees. International Journal of Primatology, 26(1), 3-31.
Pusey, A. E. (1990). Behavioural changes at adolescence in chimpanzees. Behaviour, 115(3-4), 203-246.
R Core Team. (2018). R: A language and environment for statistical computing. Vienna, AU: R foundation for Statistical Computing.
Ramos, G. L. (2014). Positional behavior of Pan paniscus at Lui Kotale. Democratic Republic of Congo: Indiana University.
Robbins, M. M., & Robbins, A. M. (2018). Variation in the social organization of gorillas: Life history and socioecological perspectives. Evolutionary Anthropology, 27(5), 218-233.
Robson, S. L., & Wood, B. (2008). Hominin life history: Reconstruction and evolution. Journal of Anatomy, 212(4), 394-425.
Saj, T. L., & Sicotte, P. (2005). Male takeover in Colobus vellerosus at Boabeng-Fiema monkey sanctuary, Central Ghana. Primates, 46(3), 211-214.
Sakamaki, T., Behncke, I., Laporte, M., Mulavwa, M., Ryu, H., Takemoto, H., … Furuichi, T. (2015). Intergroup transfer of females and social relationships between immigrants and residents in bonobo (Pan paniscus) societies. In T. Furuichi, J. Yamagiwa, & F. Aureli (Eds.), Dispersing primate females (pp. 127-164). New York: Springer.
Stearns, S. C. (1992). The evolution of life histories. Oxford, UK: Oxford University Press.
Stearns, S. C. (2000). Life history evolution: Successes, limitations, and prospects. Naturwissenschaften, 87(11), 476-486.
Stoinski, T. S., Perdue, B., Breuer, T., & Hoff, M. P. (2013). Variability in the developmental life history of the genus Gorilla. American Journal of Physical Anthropology, 152(2), 165-172.
Stumpf, R. M., Emery Thompson, M., Muller, M. N., & Wrangham, R. W. (2009). The context of female dispersal in Kanyawara chimpanzees. Behaviour, 146(4-5), 629-656.
Surbeck, M., & Hohmann, G. (2013). Intersexual dominance relationships and the influence of leverage on the outcome of conflicts in wild bonobos (Pan paniscus). Behavioral Ecology and Sociobiology, 67(11), 1767-1780.
Tokuyama, N., & Furuichi, T. (2016). Do friends help each other? Patterns of female coalition formation in wild bonobos at Wamba. Animal Behaviour, 119, 27-35.
van Noordwijk, M. A., Utami Atmoko, S. S., Knott, C. D., Kuze, N., Morrogh-Bernard, H. C., Oram, F., … Willems, E. P. (2018). The slow ape: High infant survival and long interbirth intervals in wild orangutans. Journal of Human Evolution, 125, 38-49.
van Noordwijk, M. A., & van Schaik, C. P. (2005). Development of ecological competence in Sumatran orangutans. American Journal of Physical Anthropology, 127(1), 79-94.
van Schaik, C. P., & Isler, K. (2012). Life-history evolution in primates. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies. Chicago, IL: University of Chicago Press.
Wakefield, M. L. (2013). Social dynamics among females and their influence on social structure in an East African chimpanzee community. Animal Behaviour, 85(6), 1303-1313.
Walker, K. K., Walker, C. S., Goodall, J., & Pusey, A. E. (2018). Maturation is prolonged and variable in female chimpanzees. Journal of Human Evolution, 114, 131-140.
Waller, M. T. (2011). The ranging behavior of bonobos in the Lomako Forest. Eugene, OR: University of Oregon.
Watts, D. P. (2010). Infanticide in mountain gorillas: New cases and a reconsideration of the evidence. Ethology, 81(1), 1-18.
Watts, D. P., & Pusey, A. E. (1993). Behavior of juvenile and adolescent great apes. In M. E. Pereira & L. A. Fairbanks (Eds.), Juvenile primates: Life history, development, and behavior: Life history, development, and behavior (pp. 148-167). Oxford, UK: Oxford University Press.
White, F. J., & Wood, K. D. (2007). Female feeding priority in bonobos, Pan paniscus, and the question of female dominance. American Journal of Primatology, 69(8), 837-850.
White, F. J., & Wrangham, R. W. (1988). Feeding competition and patch size in the chimpanzee species Pan paniscus and Pan troglodytes. Behaviour, 105(1), 148-164.
Wilson, M. L., Boesch, C., Fruth, B., Furuichi, T., Gilby, I. C., Hashimoto, C., … Wrangham, R. W. (2014). Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature, 513(7518), 414-417.
Wittig, R. M., & Boesch, C. (2003). Food competition and linear dominance hierarchy among female chimpanzees of the Taï National Park. International Journal of Primatology, 24(4), 847-867.
Wrangham, R., & Pilbeam, D. (2001). African apes as time machines. In All apes great and small (pp. 5-17). Boston: Kluwer Academic.
Yamamoto, S. (2015). Non-reciprocal but peaceful fruit sharing in wild bonobos in Wamba. Behaviour, 152(3-4), 335-357.
Young, J. W., & Shapiro, L. J. (2018). Developments in development: What have we learned from primate locomotor ontogeny? American Journal of Physical Anthropology, 165, 37-71.
Zhao, Q., Tan, C. L., & Pan, W. (2008). Weaning age, infant care, and behavioral development in Trachypithecus leucocephalus. International Journal of Primatology, 29(3), 583-591.