Abstract
All life histories are a complex of trade-offs that depend on individual conditions—including size, age, and sex—and adaptively mold suites of traits through the biased intergenerational transmission of successful physiological strategies. I explore intrapopulation variation in how female rhesus macaques on Cayo Santiago have negotiated a central life history trade-off: when to start reproducing. I emphasize how evolutionary quantitative genetic models require explicit links between hypothesized or measured patterns of selection and the genetic substrates that influence phenotypes and change intergenerationally. Perhaps counterintuitively, I also show how genetic models offer valuable insights on how environments, including those provided by mothers and other kin, affect offspring development and later female life histories. The emerging picture of female macaque maturation is one of the great flexibility and environmental responsiveness coupled with an important genetic component that is significantly entangled with later life history events.
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Altmann J (1980) Baboon mothers and infants. Cambridge, Harvard University Press
Altmann J, Alberts SC (2005) Growth rates in a wild primate population: ecological influences and maternal effects. Behav Ecol Sociobiol 57:490–501
Altmann J, Altmann SA, Hausfater G, McCuskey SA (1977) Life history of yellow baboons: physical development, reproductive parameters, and infant mortality. Primates 18:315–330
Arnold SJ (1994) Multivariate inheritance and evolution: a review of concepts. In: Boake CRB (ed) Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago, p 17–48
Bell G, Kofoupanou V (1986) The cost of reproduction. Oxf Surv Evol Biol 3:83–131
Bercovitch FB, Berard JD (1993) Life history costs and consequences of rapid reproductive maturation in female rhesus macaques. Behav Ecol Sociobiol 32:103–109
Bijma P (2006) Estimating maternal genetic effects in livestock. J Anim Sci 84:800–806
Blomquist GE (2009a) Environmental and genetic causes of maturational differences among rhesus macaque matrilines. Behav Ecol Sociobiol 63:1345–1352
Blomquist GE (2009b) Female age of first reproduction at Cayo Santiago: heritability and shared environments. Am J Phys Anthropol 138:94
Blomquist GE (2009c) Fitness-related patterns of genetic variation in rhesus macaques. Genetica 135:209–219
Blomquist GE (2009d) Trade-off between age of first reproduction and survival in a female primate. Biol Lett 5:339–342
Blomquist GE, Sade DS, Berard JD (2011) Rank-related fitness differences and their demographic pathways in semi-free ranging rhesus macaques (Macaca mulatta). Int J Primatol 31:193–208
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135
Brommer JE, Wilson AJ, Gustafsson L (2007) Exploring the genetics of aging in a wild passerine bird. Am Nat 170:643–650
Busse C (1982) Social dominance and offspring mortality among female chacma baboons. Int J Primatol 3:267
Caswell H (2001) Matrix population models: construction, analysis, and interpretation, 2nd edn. Sinauer Associates, Sunderland
Chapais B (2004) How kinship generates dominance structures: a comparative perspective. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, New York, pp 3–10
Charlesworth B (1994) Evolution in age-structured populations. 2nd edn. Cambridge University Press, New York
Charnov EL, Berrigan D (1993) Why do female primates have such long lifespans and so few babies? or life in the slow lane. Evol Anthropol 1:191–194
Cheney DL, Seyfarth RM, Fischer J, Beehner JC, Bergman TJ, Johnson SE, Kitchen DM, Palombit RA, Rendall D, Silk JB (2006) Reproduction, mortality, and female reproductive success in chacma baboons of the Okavango Delta, Botswana. In: Swedell L, Leigh SR (eds) Reproduction and fitness in baboons: behavioral, ecological, and life history perspectives. Springer, New York, pp 147–176
Cheverud JM, Moore AJ (1994) Quantitative genetics and the role of the environment provided by relatives in behavioral evolution. In: Boake CRB (ed) Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago, pp 67–100
Cheverud JM, Wolf JB (2009) The genetics and evolutionary consequences of maternal effects. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. University of Chicago Press, Chicago, pp 11–37
de Jong G, van Noordwijk AJ (1992) Acquisition and allocation of resources: genetic (co)variances, selection, and life histories. Am Nat 139:749–770
Ellis L (1995) Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ecol Sociobiol 16:257–333
Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford
Gagliardi C, Falkenstein KP, Franke DE, Kubisch HM (2010) Estimates of heritability for reproductive traits in captive rhesus macaque females. Am J Primatol 72:811–819
Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml User Guide, version 3.0. VSN International
Grafen A (1988) On the uses of data on lifetime reproductive success. In: Clutton-Brock TH (ed) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 454–471
Ha JC, Ha RR, Almasy L, Dyke B (2002) Genetics and caging type affect birth weight in captive pigtailed macaques (Macaca nemestrina). Am J Primatol 56:207–213
Harvey PH, Martin RD, Clutton-Brock TH (1987) Life histories in comparative perspective. In: Smuts B (ed) Primate societies. University of Chicago Press, Chicago, pp 181–196
Hird DW, Henrickson RV, Hendrickx AG (1975) Infant mortality in Macaca mulatta: neonatal and post-neonatal mortality at the California Primate Research Center, 1968–1972. A retrospective study. J Med Primatol 4:4–22
Hoffman CL, Higham JP, Mas-Rivera A, Ayala JE, Maestripieri D (2010) Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago. Behav Ecol 21:972–978
Houle D (1991) Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45:630–645
Hrdy SB (1999) Mother nature: a history of mothers, infants, and natural selection. Pantheon Books, New York
Hughes KA, Alipaz JA, Drnevich JM, Reynolds RM (2002) A test of evolutionary theories of aging. Proc Natl Acad Sci USA 99:14286–14291
Jaquish CE, Cheverud JM, Tardif SD (1996) Genetic and environmental impacts on litter size and early infant survival in three species of callitrichids. J Hered 87:74–77
Jaquish CE, Dyer T, Williams-Blangero S, Dyke B, Leland M, Blangero J (1997) Genetics of adult body mass and maintenance of adult body mass in captive baboons (Papio hamadryas subspecies). Am J Primatol 42:281–288
Jones JH, Wilson ML, Murray C, Pusey A (2010) Phenotypic quality influences fertility in gombe chimpanzees. J Anim Ecol 79:1262–1269
Kappeler PM, Pereira ME (2003) Primate life histories and socioecology. University of Chicago Press, Chicago
Kessler MJ, Berard JD, Rawlins RG, Bercovitch FB, Gerald MS, Laudenslager ML, Gonzalez-Martinez J (2006) Tetanus antibody titers and duration of immunity to clinical tetanus infections in free-ranging rhesus monkeys (Macaca mulatta). Am J Primatol 68:725–731
Kevles D (1985) In the name of eugenics. UCLA Press, Los Angeles
Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783
Kruuk LEB (2004) Estimating genetic parameters in natural populations using the ‘animal model’. Phil Trans Roy Soc Lond Ser B 359:873–890
Kruuk LEB, Hadfield JD (2007) How to separate genetic and environmental causes of similarity between relatives. J Evol Biol 20:1890–1903
Kruuk LEB, Slate J, Wilson AJ (2008) New answers for old questions: the evolutionary quantitative genetics of wild animal populations. Annu Rev Ecol Systemat 39:525–548
Lande R (1982) A quantitative genetic theory of life history evolution. Ecology 63:607–615
Lande R, Arnold SJ (1983) Measurement of selection on correlated characters. Evolution 37:1210–1226
Law R (1979) Optimal life histories under age-specific predation. Am Nat 114:399–417
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland
Maestripieri D (2003) Similarities in affiliation and aggression between cross-fostered rhesus macaque females and their biological mothers. Dev Psychobiol 43:321–327
Maestripieri D (2009) Maternal influences on offspring growth, reproduction, and behavior in primates. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. University of Chicago Press, Chicago, pp 256–291
Martin LJ, Mahaney MC, Bronikowski AM, Dee CK, Dyke B, Comuzzie AG (2002) Lifespan in captive baboons is heritable. Mech Ageing Dev 123:1461–1467
Merilä J, Sheldon BC (1999) Genetic architechture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83:103–109
Meyer K (2001) Estimates of direct and maternal covariance functions for growth of australian beef calves from birth to weaning. Genet Sel Evol 33:487–514
Nickerson SC (1995) Milk production: factors affecting milk composition. In: Harding F (ed) Milk quality. Blackie Academic and Professional, London, pp 3–24
Nurnberg P, Saurmann U, Kayser M, Lanfer C, Manz E, Widdig A, Berard J, Bercovitch FB, Kessler M, Schmidtke J, Krawczak M (1998) Paternity assessment in rhesus macaques (Macaca mulatta): Multilocus DNA fingerprinting and PCR marker typing. Am J Primatol 44:1–18
Price T, Schluter D (1991) On the low heritability of life history traits. Evolution 45:853–861
Provine, WB (1971) The origins of theoretical population genetics. University of Chicago Press, Chicago
Quinn JL, Charmantier A, Garant D, Sheldon BC (2006) Data depth, data completeness, and their influence on quantitative genetic estimation in two contrasting bird populations. J Evol Biol 19:994–1002
Ralls K, Ballou J (1982) Effects of inbreeding on infant mortality in captive primates. Int J Primatol 3:491–505
Räsänen K, Kruuk LEB (2007) Maternal effects and evolution at ecological time scales. Funct Ecol 21:408–421
Rawlins RG, Kessler MJ (1985) Climate and seasonal reproduction in the Cayo Santiago macaques. Am J Primatol 9:87–99
Rawlins RG, Kessler MJ (eds) (1986a) The Cayo Santiago macaques: history, behavior, and biology. SUNY Press, Albany
Rawlins RG, Kessler MJ (1986b) The history of the Cayo Santiago colony. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques: history, behavior, and ecology. State University of New York Press, Albany, pp 47–72
Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267
Rice SH (2004) Developmental associations between traits: covariance and beyond. Genetics 166:513–526
Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468
Robson EB (1978) The genetics of birth weight. In: Falkner F, Tanner JM (eds) Human growth: 1 principles and prenatal growth. Plenum Press, New York, pp 285–297
Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New York
Roff DA (2002) Life history evolution. 2nd edn. Sinauer Associates, Sunderland
Roff DA, Fairbairn DJ (2007) The evolution of trade-offs: where are we? J Evol Biol 20:433–447
Rogers J (2005) Genetics: a survey of nonhuman primate genetics, genetic management and applications to biomedical research. In: Coote SW (ed) The laboratory primate. Academic Press, New York, pp 487–501
Sade DS, Chepko-Sade BD, Schneider JM, Roberts SS, Richtsmeier JT (1985) Basic demographic observations on free-ranging rhesus monkeys. Human Relations Area Files, New Haven
Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308:648–652
Schino G, Troisi A (2005) Neonatal abandonment in Japanese macaques. Am J Phys Anthropol 126:447–452
Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234
Smith DG (1986) Incidence and consequences of inbreeding in three captive groups of rhesus macacques (Macaca mulatta). In: Benirschke K (ed) Primates: the road to self-sustaining populations. Springer, New York, pp 857–874
Stearns SC (1989) Trade-offs in life history evolution. Funct Ecol 3:259–268
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Stearns SC, Magwene P (2003) The naturalist in the world of genomics. Am Nat 161:171–180
Strier KB, Altmann J, Brockman DK, Bronikowski AM, Cords M, Fedigan LM, Lapp H, Liu X, Morris WF, Pusey AE, Stoinski TS, Alberts SC (2010) The primate life history database: a unique shared ecological data resource. Meth Ecol Evol 1:199–211
Stucki BR, Dow MM, Sade DS (1991) Variance in intrinsic rates of growth among free-ranging rhesus monkeys. Am J Phys Anthropol 84:181–191
Takahata Y, Suzuki S, Agetsuma N, Okayasu N, Sugiura H, Takahashi H, Yamagiwa J, Izawa K, Furuichi T, Hill DA, Maruhashi T, Saito C, Sato S, Sprague DS (1998) Reproduction of wild Japanese macaque females of Yakushima and Kinkazan islands: A preliminary report. Primates 39:339–349
Templeton AR (2006) Population genetics and microevolutionary theory. Wiley, Hoboken
Towne B, Czerwinski SA, Demerath EW, Blangero J, Roche AF, Siervogel RM (2005) Heritability of age at menarche in girls from the Fels longitudinal study. Am J Phys Anthropol 128:210–219
van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142
van Schaik CP, Janson CH (eds) (2000) Infanticide by males and its implications. Cambridge University Press, New York
Visscher PM, Hill WG, Wray NR (2008) Heritability in the genomics era—concepts and misconceptions. Nat Rev Genet 9:255–266
Vitzthum VJ (2003) A number no greater than the sum of its parts: the use and abuse of heritability. Hum Biol 75:539–558
Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411
Williams-Blangero S, Blangero J (1995) Heritability of age of first birth in captive olive baboons. Am J Primatol 37:233–239
Wilson AJ, Réale D (2006) Ontogeny of additive and maternal genetic effects: lessons from domestic mammals. Am Nat 167:E23–E38
Wilson AJ, Reale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26
Wilson ME, Gordon TP, Bernstein IS (1978) Timing of births and reproductive success in rhesus monkey social groups. J Med Primatol 7:202–212
Wolf JB, Brodie III ED, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13:64–69
Wolf JB, Brodie III ED, Moore AJ (1999) Interacting phenotypes and the evolutionary process, II. Selection resulting from social interactions. Am Nat 153:254–266
Wolf JB, Wade MJ (2009) What are maternal effects (and what are they not)? Phil Trans Roy Soc Lond Ser B 364:1107–1115
Acknowledgements
Thanks to Kate Clancy, Katie Hinde, and Julienne Rutherford for the invitation to contribute to this chapter. Cayo Santiago is part of the Caribbean Primate Research Center (CPRC) which is supported by the University of Puerto Rico, Medical Sciences Campus and the National Institutes of Health (NIH). The facility is also supported by Grant Number CM-5 P40 RR003640-20 from the National Center for Research Resources (NCRR), a component of NIH. The contents of this chapter are solely the responsibility of the author and do not necessarily represent the official views of NCRR or NIH. Additional funding for this research came from the University of Illinois Graduate College and the University of Missouri. Melissa Gerald, John Cant, Terry Kensler, Benedikt Hallgrimsson, and Jean Turnquist were all helpful resources while working with CPRC materials. Donald Sade, Richard Rawlins, John Berard, and Melissa Gerald must be credited for the upkeep of the demographic records on Cayo Santiago and Angel “Guelo” Figueroa, Edgar Davila, and Elizabeth Maldonado for their day-to-day maintenance. I also want to thank my wife, Rachel, who was busy building a baby and tackling the rest of life while I wrote this chapter.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this chapter
Cite this chapter
Blomquist, G.E. (2013). Quantitative Genetic Perspectives on Female Macaque Life Histories. In: Clancy, K., Hinde, K., Rutherford, J. (eds) Building Babies. Developments in Primatology: Progress and Prospects, vol 37. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4060-4_20
Download citation
DOI: https://doi.org/10.1007/978-1-4614-4060-4_20
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-4059-8
Online ISBN: 978-1-4614-4060-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)