Abstract
The life history of any species is determined by traits that characterize its developmental and reproductive rates as well as the reproductive effort spent over its lifetime. This chapter will present an overview of the current knowledge on the diversity of primate life history. It will explore potential links between life history and major biological factors, which are suggested as a partial explanation for the existing interspecific variations in life history. Furthermore, it will outline general principles and current hypotheses on the evolution of primate life history. This review will show that extant primates ranging from nocturnal ancestral primates to apes provide an important biological substrate illuminating the evolutionary roots and selective forces that shaped human life history.
References
Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36:199–221
Allman JM (1995) Brain and life span in catarrhine primates. In: Butler RN, Brody JA (eds) Delaying the onset of late-life dysfunction. Springer, New York, pp 221–241
Allman JM, Hasenstaub A (1999) Brains, maturation times, and parenting. Neurobiol Aging 20:447–454
Allman JM, McLaughlin T, Hakeem A (1993) Brain weight and life-span in primate species. Proc Natl Acad Sci USA 90:3559–3563
Altmann J, Samuels A (1992) Costs of maternal-care: infant carrying in baboons. Behav Ecol Sociobiol 29:391–398
Alvarez HP (2000) Grandmother hypothesis and primate life histories. Am J Phys Anthropol 113:435–450
Alvarez H (2002) Grandmothers and human longevity. In: Pagel M (ed) Encyclopedia of evolution, vol 2. Oxford University Press, Oxford, pp 631–634
Andriantompohavana R, Lei R, Zaonarivelo JR, Engberg SE, Nalanirina G, McGuire SM, Shore GD, Andrianasolo J, Herrington K, Brenneman RA, Louis EE Jr (2007) Molecular phylogeny and taxonomic revision of the woolly lemurs, genus Avahi (Primates: Lemuriformes). Spec Publ Mus Tex Tech Univ 51:1–59
Armstrong E (1983) Relative brain size and metabolism in mammals. Science 220:1302–1304
Arroyo-Rodríguez V, Asensio N, Cristóbal-Azkarate J (2008) Demography, life history and migrations in a Mexican mantled howler group in a rainforest fragment. Am J Primatol 70:114–118
Atramentowicz M (1996) Reproductive strategy of two small mammals of similar ecology: comparing a marsupial and a placental. In: Croft DB, Gansloβer U (eds) Comparison of marsupial and placental behaviour. Filander, Fürth, pp 252–261
Austad SN (1994) Menopause: an evolutionary perspective. Exp Gerontol 29:255-263
Austad SN, Fischer KE (1992) Primate longevity: its place in the mammalian scheme. Am J Primatol 28:251–261
Bales K, Dietz J, Baker A, Miller K, Tardif SD (2000) Effects of allocare-givers on fitness of infants and parents in callitrichid primates. Folia Primatol 71:27–38
Barrickman NL, Lin MJ (2010) Encephalization, expensive tissues, and energetics: an examination of the relative costs of brain size in strepsirrhines. Am J Phys Anthropol 143:579–590
Barrickman NL, Bastian ML, Isler K, van Schaik CP (2008) Life history costs and benefits of encephalization: a comparative test using data from long-term studies of primates in the wild. J Hum Evol 54:568–590
Barton R (1999) The evolutionary ecology of the primate brain. In: Lee PC (ed) Comparative primate socioecology. Cambridge University Press, Cambridge, pp 167–194
Barton RA, Capellini I (2011) Maternal investment, life histories, and the costs of brain growth in mammals. Proc Natl Acad Sci U S A 108:6169–6174
Bearder SK (1987) Lorises, bushbabies, and tarsiers: diverse societies in solitary foragers. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 11–24
Blomquist GE, Kowalewski MM, Leigh SR (2003) A phylogenetic approach to quantifying the relationship between age of first reproduction and maximum lifespan. Am J Phys Anthropol 36:68
Blurton Jones NG, Hawkes K, O’Connell JF (1989) Modelling and measuring costs of children in two foraging societies. In: Standen V, Foley RA (eds) Comparative socioecology: the behavioural ecology of humans and other mammals. Blackwell, Oxford, pp 367–390
Bogin B (1999) Patterns of human growth. Cambridge University Press, Cambridge
Bogin B (2009) Childhood, adolescence, and longevity: a multilevel model of the evolution of reserve capacity in human life history. Am J Hum Biol 21:567–577
Borries C, Lu A, Ossi-Lupo K, Larney E, Koenig A (2011) Primate life histories and dietary adaptations: a comparison of Asian colobines and macaques. Am J Phys Anthropol 144:286–299
Broadfield DC (2010) Grandparental investment and the epiphenomenon of menopause in recent human history. Behav Brain Sci 33:19–20
Bromage TG, Hogg RT, Lacruz RS, Hou C (2012) Primate enamel evinces long period biological timing and regulation of life history. J Theor Biol 305:131–144
Bronikowski AM, Altmann J, Brockman DK, Cords M, Fedigan LM, Pusey A, Stoinski T, Morris WF, Strier KB, Alberts SC (2011) Aging in the natural world: comparative data reveal similar mortality patterns across primates. Science 331:1325–1328
Calder WA III (1984) Size, function, and life history. Harvard University Press, Cambridge, MA
Catlett KK, Schwartz GT, Godfrey LR, Jungers WL (2010) “Life history space”: a multivariate analysis of life history variation in extant and extinct Malagasy lemurs. Am J Phys Anthropol 142:391–404
Chapman CA, Walker S, Lefebvre L (1990) Reproductive strategies of primates: the influence of body size and diet on litter size. Primates 31:1–13
Charnov EL (1991) Evolution of life history variation among female mammals. Proc Natl Acad Sci U S A 88:1134–1137
Charnov EL (1993) Life history invariants: some explorations of symmetry in evolutionary ecology. Oxford University Press, Oxford
Charnov EL (1997) Trade-off-invariant rules for evolutionarily stable life histories. Nature 387:393–394
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
Cheek DB (1975) The fetus. In: Cheek DB (ed) Fetal and postnatal cellular growth. Wiley, New York
Cheney DL, Seyfarth RM, Andelman SJ, Lee PC (1988) Reproductive success in vervet monkeys. In: Clutton-Brock TH (ed) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 384–402
Clutton-Brock TH (1991) The evolution of sex differences and the consequences of polgyny in mammals. In: Bateson P (ed) The development and integration of behaviour. Cambridge University Press, Cambridge, pp 229–253
Cords M (1987) Forest guenons and patas monkeys: male-male competition in one-male groups. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 98–111
Count EW (1947) Brain weight and body weight in man: their antecedents in growth and evolution. Ann N Y Acad Sci 46:993–1122
Cummings JR, Muchlinski MN, Kirk EC, Rehorek SJ, DeLeon VB, Smith TD (2012) Eye size at birth in prosimian primates: life history correlates and growth patterns. PLoS One 7:e36097
Deaner RO, Barton RA, van Schaik CP (2003) Primate brains and life histories: renewing the connection. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 233–265
Di Bitetti MS, Janson CH (2000) When will the stork arrive? Patterns of birth seasonality in neotropical primates. Am J Primatol 50:109–130
Dixson AF (1992) Observations on postpartum changes in hormones and sexual behavior in callithrichid primates: do females exhibit postpartum “estrus”? In: Itoigawa N, Sugiyama Y, Sackett GP, Thompson RKR (eds) Topics in primatology, vol 2, Behavior, ecology, and conservation. University of Tokyo Press, Tokyo, pp 141–149
Dobson FS, Oli MK (2008) The life histories of orders of mammals: fast and slow breeding. Curr Sci 95:862–865
Dukas R (1998) Evolutionary ecology of learning. In: Dukas R (ed) The evolutionary ecology of information processing and decision making. University of Chicago, Chicago, pp 129–174
Dunbar RIM (1995) The mating system of callitrichid primates: I. Conditions for the coevolution of pair bonding and twinning. Anim Behav 50:1057–1070
Dunbar RIM (2003) Why are apes so smart? In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 285–298
Dunbar RIM, Shultz S (2007) Evolution in the social brain. Science 317:1344–1347
Eberle M, Kappeler PM (2004) Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behav Ecol Sociobiol 57:77–90
Eisenberg JF (1981) The mammalian radiations: an analysis of trends in evolution, adaptation, and behavior. University of Chicago Press, Chicago
Erb WM, Borries C, Lestari NS, Hodges JK (2012) Annual variation in ecology and reproduction of wild simakobu (Simias concolor). Int J Primatol 33:1406–1419
Fedigan LM, Pavelka MSM (2001) Is there adaptive value to reproductive termination in Japanese macaques? A test of maternal investment hypotheses. Int J Primatol 22:109–125
Finch CE, Stanford CB (2004) Meat-adaptive genes and the evolution of slower aging in humans. Q Rev Biol 79:3–50
Fleagle JG (1999) Primate adaptation and evolution. Academic, New York
Foley RA, Lee PC (1992) Ecology and energetics of encephalization in hominid evolution. In: Whitten A, Widdowson EM (eds) Foraging strategies and natural diet of monkeys, apes and humans. Clarendon, Oxford, pp 63–72
Fürtbauer I, Schülke O, Heistermann M, Ostner J (2010) Reproductive and life history parameters of wild female Macaca assamensis. Int J Primatol 31:501–517
Ganzhorn JU, Klaus S, Ortmann S, Schmid J (2003) Adaptations to seasonality: some primate and nonprimate examples. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 132–147
Garber PA (1997) One for all and breeding for one: cooperation and competition as a tamarin reproductive. Evol Anthropol 5:187–199
Garber PA, Leigh SR (1997) Ontogenetic variation in small-bodied New World primates: implications for patterns of reproduction and infant care. Folia Primatol 68:1–22
Garcia C, Lee PC, Rosetta L (2009) Growth in colony living anubis baboon infants and its relationship with maternal activity budgets and reproductive status. Am J Phys Anthropol 138:123–135
Génin F (2008) Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. Int J Primatol 29:303–321
Godfrey LR, Samonds KE, Jungers WL, Sutherland MR (2003) Dental development and primate life histories. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 177–203
Gogarten JF, Brown LM, Chapman CA, Cords M, Doran-Sheehy D, Fedigan LM, Grine FE, Perry S, Pusey AE, Sterck EHM, Wich SA, Wright PC (2012) Seasonal mortality patterns in non-human primates: implications for variation in selection pressures across environments. Evolution 66:3252–3266
Goldizen AW (1987) Tamarins and marmosets: communal care of offspring. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 34–43
Gonzales-Lagos C, Sol D, Reader SM (2010) Large-brained mammals live longer. J Evol Biol 23:1064–1074
Groeneveld LF, Rasoloarison RM, Kappeler PM (2011) Morphometrics confirm taxonomic deflation in dwarf lemurs (Primates: Cheirogaleidae), as suggested by genetics. Zool J Linn Soc 161:229–244
Guthrie EH, Frost SR (2011) Pattern and pace of dental eruption in Tarsius. Am J Phys Anthropol 145:446–451
Hakeem A, Sandoval GR, Jones M, Allman JM (1996) Brain and life span in primates. In: Birren JE, Schaie KW (eds) Handbook of the psychology of aging. Academic, San Diego, pp 78–104
Harvey PH, Clutton-Brock TH (1985) Life history variation in primates. Evolution 39:559–581
Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford
Harvey PH, Purvis A (1999) Understanding the ecological and evolutionary reasons for life history variation: mammals as a case study. In: McGlade J (ed) Advanced ecological theory: principles and applications. Blackwell, Oxford, pp 232–248
Harvey PH, Martin RD, Clutton-Brock TH (1987) Life histories in comparative perspective. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 181–196
Hawkes K (2003) Grandmothers and the evolution of human longevity. Am J Hum Biol 15:380–400
Hawkes K, O’Connell JF, Blurton Jones NG, Alvarez H, Charnov EL (1998) Grandmothering, menopause, and the evolution of human. Proc Natl Acad Sci U S A 95:1336–1339
Hawkes K, O’Connell JF, Blurton Jones NG (2003) Human life histories: primate trade-offs, grandmothering socioecology, and the fossil record. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 204–231
Hill K, Hurtado AM (1991) The evolution of premature reproductive senescence and menopause in human females: an evaluation of the “grandmother” hypothesis. Hum Nat 2:313–350
Hill K, Hurtado AM (1996) Ache life history: the ecology and demography of a foraging people. Aldine de Gruyter, Hawthorne
Hill K, Hurtado AM (1999) Packer and colleagues’ model of menopause for humans. Hum Nat 10:199–204
Hill RA, Lee PC (1998) Predation risk as an influence on group size in cercopithecoid primates: implications for social structure. J Zool 245:447–456
Hinde K, Milligan LA (2011) Primate milk: proximate mechanisms and ultimate perspectives. Evol Anthropol 20:9–23
Hogg RT, Walker RS (2011) Life-history correlates of enamel microstructure in Cebidae (Platyrrhini, Primates). Anat Rec (Hoboken) 294:2193–2206
Huck M, Rotundo M, Fernandez-Duque E (2011) Growth and development in wild owl monkeys (Aotus azarai) of Argentina. Int J Primatol 32:1133–1152
Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behav Ecol 2:143–155
Isbell LA (1994) Predation on primates: ecological patterns and evolutionary consequences. Evol Anthropol 3:61–72
Isler K, van Schaik CP (2009) The Expensive Brain: a framework for explaining evolutionary changes in brain size. J Hum Evol 57:392–400
Isler K, van Schaik CP (2012) Allomaternal care, life history and brain size evolution in mammals. J Hum Evol 63:52–63
Jamison CS, Cornell LL, Jamison PL, Nakazato H (2002) Are all grandmothers equal? A review and a preliminary test of the grandmother hypothesis in Tokugawa Japan. Am J Phys Anthropol 119:67–76
Janson CH (2003) Puzzles, predation, and primates: using life history to understand selection pressures. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 103–131
Janson CH, Goldsmith ML (1995) Predicting group size in primates: foraging costs and predation risks. Behav Ecol 6:326–336
Janson CH, van Schaik CP (1993) Ecological risk aversion in juvenile primates: slow and steady wins the race. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development, and behavior. Oxford University Press, Oxford, pp 57–74
Janson CH, van Schaik CP (2000) The behavioral ecology of infanticide by males. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, UK, pp 469–494
Jarman PJ (1983) Mating system and sexual dimorphism in large terrestrial mammalian herbivores. Biol Rev 58:485–520
Jin T, Wang DZ, Zhao Q, Yin LJ, Qin DG, Ran WZ, Pan WS (2009) Reproductive parameters of wild Trachypithecus leucocephalus: seasonality, infant mortality and interbirth interval. Am J Primatol 71:558–566
Joffe TH (1997) Social pressures have selected for an extended juvenile period in primates. J Hum Evol 32:593–605
Johnson RL, Kapsalis E (1998) Menopause in free-ranging rhesus macaques: estimated incidence, relation to body condition, and adaptive significance. Int J Primatol 19:751–765
Jones JH (2011) Primates and the evolution of long, slow life histories. Curr Biol 21:R708–R717
Jones KE, Mac Larnon A (2001) Bat life histories: testing models of mammalian life-history evolution. Evol Ecol Res 3:465–476
Kachel AF, Premo LS (2012) Disentangling the evolution of early and late life history traits in humans. Evol Biol 39:638–649
Kamilar JM, Bribiescas RG, Bradley BJ (2010) Is group size related to longevity in mammals? Biol Lett 6:736–739
Kano T (1992) The last ape: Pygmy chimpanzee behavior and ecology. Stanford University Press, Stanford
Kaplan HS (2002) Human life histories. In: Pagel M (ed) Encyclopedia of evolution, vol 2. Oxford University Press, Oxford, pp 627–631
Kaplan HS, Robson AJ (2002) The emergence of humans: the coevolution of intelligence and longevity with intergenerational transfers. Proc Natl Acad Sci USA 99:10221–10226
Kaplan H, Hill K, Lancaster J, Hurtado AM (2000) A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol 9:156–185
Kaplan HS, Mueller T, Gangestad S, Lancaster JB (2003) Neural capital and life span evolution among primates and humans. In: Finch CE, Robine J-M, Christen Y (eds) Brain and longevity. Springer, Berlin, pp 69–97
Kappeler PM (1996) Causes and consequences of life-history variation among strepsirhine primates. Am Nat 148:868–891
Kappeler PM (1998) Nests, tree holes, and the evolution of primate life histories. Am J Primatol 46:7–33
Kappeler PM, Pereira ME (eds) (2003) Primate life histories and socioecology. University of Chicago Press, Chicago
Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740
Kappeler PM, Pereira ME, Van Schaik CP (2003) Primates life histories and socioecology. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 1–23
Kim PS, Coxworth JE, Hawkes K (2012) Increased longevity evolves from grandmothering. Proc R Soc Lond B 279:4880–4884
King SJ, Morelli T, Arrigo-Nelson S, Ratelolahy FJ, Godfrey LR, Wyatt J, Tecot S, Jernvall J, Wright PC (2011) Morphometrics and pattern of growth in wild sifakas (Propithecus edwardsi) at Ranomafana National Park, Madagascar. Am J Primatol 73:155–172
Kingdon J (1997) The Kingdon field guide to African mammals. Academic, San Diego
Kirkwood TBL, Rose MR (1991) Evolution of senescence: late survival sacrificed for reproduction. Philos Trans R Soc Lond B Biol Sci 332:15–24
Kozlowski J, Weiner J (1997) Interspecific allometries are byproducts of body size aptimization. Am Nat 149:352–380
Lahdenperä M, Lummaa V, Helle S, Tremblay M, Russell AF (2004) Fitness benefits of prolonged post-reproductive lifespan in woman. Nature 428:178–181
Langergraber KE, Prüfer K, Rowney C, Boesch C, Crockford C, Fawcett K, Inoue E, Inoue-Muruyama M, Mitani JC, Muller MN, Robbins MM, Schubert G, Stoinski TS, Viola B, Watts D, Wittig RM, Wrangham RW, Zuberbühler K, Pääbo S, Vigilant L (2012) Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc Natl Acad Sci USA 109:15716–1572
Larke A, Crews DE (2006) Parental investment, late reproduction, and increased reserve capacity are associated with longevity in humans. J Physiol Anthropol 25:119–131
Lee PC (1996) The meaning of weaning: growth, lactation, and life history. Evol Anthropol 5:87–96
Lee PC (1999) Comparative ecology of postnatal growth and weaning among haplorhine primates. In: Lee PC (ed) Comparative primate socioecology. Cambridge University Press, Cambridge, pp 111–136
Lee PC (2012) Growth and investment in hominin life history evolution: patterns, processes, and outcomes. Int J Primatol 33:1309–1331
Lee PC, Bowman JE (1995) Influence of ecology and energetics on primate mothers and infants. In: Pryce CR, Martin RD, Skuse D (eds) Motherhood in human and nonhuman primates. Karger, Basel, pp 47–58
Lee PC, Kappeler PM (2003) Socioecological correlates of phenotypic plasticity of primate life histories. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 41–65
Lee PC, Majluf P, Gordon IJ (1991) Growth, weaning and maternal investment from a comparative perspective. J Zool 225:99–114
Lefebvre L (2012) Primate encephalization. Prog Brain Res 195:393–394
Leigh SR (1994) Ontogenetic correlates of diet in anthropoid primates. Am J Phys Anthropol 94:499–522
Leigh SR (1996) Evolution of human growth spurts. Am J Phys Anthropol 101:455–474
Leigh SR (2004) Brain growth, life history, and cognition in primate and human evolution. Am J Primatol 62:139–164
Leigh SR (2012) Brain size growth and life history in human evolution. Evol Biol 39:587–599
Leigh SR, Park PB (1998) Evolution of human growth prolongation. Am J Phys Anthropol 107:331–350
Leigh SR, Shea BT (1995) Otogeny and the evolution of adult body size dimorphism in apes. Am J Primatol 36:37–60
Leonard WR, Robertson ML (1992) Nutritional requirements and human evolution: a bioenergetics model. Am J Hum Biol 4:179–195
Leutenegger W (1973) Maternal-fetal weight relationships in primates. Folia Primatol 20:280–293
Leutenegger W (1976) Allometry of neonatal size in eutherian mammals. Nature 263:229–230
Leutenegger W (1979) Evolution of litter size in primates. Am Nat 114:525–531
Levitis DA, Lackey LB (2011) A measure for describing and comparing postreproductive life span as a population trait. Methods Ecol Evol 2:446–453
Lindburg DG (1987) Seasonality of reproduction in primates. In: Mitchell G, Erwin J (eds) Comparative primate biology, vol 2B, Behavior, cognition and motivation. Alan R. Liss, New York, pp 167–218
Louis EE Jr, Coles MS, Andriantompohavana R, Sommer JA, Engberg SE, Zaonarivelo JR, Mayor MI, Brenneman RA (2006a) Revision of the mouse lemurs (Microcebus) of eastern Madagascar. Int J Primatol 27:347–389
Louis EE Jr, Engberg SE, Lei R, Geng H, Sommer JA, Randriamampionona R, Randriamanana JC, Zaonarivelo JR, Andriantompohavana R, Randria G, Ramaromilanto B, Prosper M, Rakotoarisoa G, Rooney A, Brenneman RA (2006b) Molecular and morphological analyses of the sportive lemurs (Family Megaladapidae: Genus Lepilemur) reveals 11 previously unrecognized species. Spec Publ Mus Tex Tech Univ 49:1–47
Lutermann H (2001) Weibchenassoziationen und Fortpflanzungsstrategien beim Grauen Mausmaki (Microcebus murinus) in Nordwest-Madagaskar. PhD thesis, University Hannover, Hannover
Mace R (2000) Evolutionary ecology of human life history. Anim Behav 59:1–10
Martin RD (1981) Relative brain size and basal metabolic rate in terrestrial vertebrates. Nature 293:57–60
Martin RD (1984) Scaling effects and adaptive strategies in mammalian reproduction. Symp Zool Soc Lond 51:81–117
Martin RD (1990) Primate origins and evolution: a phylogenetic reconstruction. Chapman and Hall, London
Martin RD (1996) Scaling of the mammalian brain: the maternal energy hypothesis. News Physiol Sci 11:149–156
Martin RD (2003) Foreword. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp xi–xx
Martin RD (2007) The evolution of human reproduction: a primatological perspective. Am J Phys Anthropol 50:59–84
Martin RD, Isler K (2010) The maternal energy hypothesis of brain evolution: an update. In: Broadfield DC, Yuan MS, Schick K, Toth N (eds) The human brain evolving: paleoneurological studies in honor of Ralph L. Holloway. Stone Age Institute Press, Gosport, pp 15–35
Martin RD, MacLarnon AM (1985) Gestation period, neonatal size, and maternal investment in placental mammals. Nature 313:220–223
Martin RD, MacLarnon AM (1988) Comparative quantitative studies of growth and reproduction. Symp Zool Soc Lond 60:39–80
Martin RD, MacLarnon AM (1990) Reproductive patterns in primates and other mammals: the dichotomy between altricial and precocial offspring. In: DeRousseau CJ (ed) Primate life history and evolution. Wiley-Liss, New York, pp 47–80
Martin RD, Genoud M, Hemelrijk CK (2005) Problems of allometric scaling analysis: examples from mammalian reproductive biology. J Exp Biol 208:1731–1747
Mitani JC, Watts D (1997) The evolution of non-maternal caretaking among anthropoid primates: do helpers help? Behav Ecol Sociobiol 40:213–220
Müller AE, Thalmann U (2000) Origin and evolution of primate social organisation: a reconstruction. Biol Rev 75:405–435
Mumby H, Vinicius L (2008) Primate growth in the slow lane: a study of inter-species variation in the growth constant A. Evol Biol 35:287–295
Mustoe AC, Jensen HA, French JA (2012) Describing ovarian cycles, pregnancy characteristics, and the use of contraception in female white-faced marmosets, Callithrix geoffroyi. Am J Primatol 74:1044–1053
Mutschler T, Nievergelt CM, Feistner ATC (2000) Social organization of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). Am J Primatol 50:9–24
Nash LT, Zimmermann E, Butynski TM (2013) Galago senegalensis Northern Lesser Galago (Senegal Lesser Galago, Senegal Lesser Bushbaby). In: Butynski TM, Kingdon J, Kalina J (eds) Mammals of Africa, vol II, Primates. Bloomsbury, London, pp 425–429
Nicolson NA (1987) Infants, mothers and other females. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 330–342
Okamoto K, Matsumura S, Watanabe K (2000) Life history and demography of wild moor macaques (Macaca maurus): summary of ten years observations. Am J Primatol 52:1–11
Owens IPF, Bennett PM (1995) Ancient ecological diversification explains life-history variation among living birds. Proc R Soc Lond B 261:227–232
Packer C, Collins DA, Sindimwo A, Goodall J (1995) Reproductive constraints on aggressive competition in female baboons. Nature 373:60–63
Pagel MD, Harvey PH (1989) Taxonomic differences in the scaling of brain on body weight among mammals. Science 244:1589–1593
Pagel MD, Harvey PH (1993) Evolution of the juvenile period in mammals. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development, and behavior. Oxford University Press, New York, pp 28–37
Pavelka MS, Fedigan LM (1999) Reproductive termination in female Japanese monkeys: a comparative life history perspective. Am J Phys Anthropol 109:455–464
Pereira ME (1995) Development and social dominance among group-living primates. Am J Primatol 37:143–175
Pereira ME, Fairbanks LA (1993) Juvenile primates: life history, development, and behavior. Oxford University Press, New York
Pereira ME, Leigh SR (2003) Modes of primate development. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 149–176
Pollock JI (1975) Field observations on Indri indri: a preliminary report. In: Tattersall I, Sussman RW (eds) Lemur biology. Plenum, New York, pp 287–311
Prentice AM, Whitehead RG (1987) The energetics of human reproduction. Symp Zool Soc Lond 75:275–304
Promislow DEL, Harvey PH (1990) Living fast and dying young: a comparative analysis of life-history variation among mammals. J Zool 220:417–437
Purvis A, Harvey PH (1995) Mammalian life history evolution: a comparative test of Charnov’s model. J Zool 237:259–283
Purvis A, Webster AJ, Agapow P-M, Jones KE, Isaac NJB (2003) Primate life histories and phylogeny. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 25–40
Radespiel U (2000) Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar. Am J Primatol 51:21–40
Ramanankirahina R, Joly M, Zimmermann E (2011) Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis). Am J Primatol 73:1261–1268
Randrianambinina B, Mbotizafy S, Rasoloharijaona S, Ravoahangimalala RO, Zimmermann E (2007) Seasonality in reproduction of Lepilemur edwardsi. Int J Primatol 28:783–790
Rao AJ, Ramesh V, Ramachandra SG, Krishnamurthy HN, Ravindranath N, Moudgal NR (1998) Growth and reproductive parameters of bonnet monkey (Macaca radiata). Primates 39:97–107
Rasoloarison RM, Goodman SM, Ganzhorn JU (2000) Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Int J Primatol 21:963–1019
Rasoloharijaona S, Rakotosamimanana B, Zimmermann E (2000) Infanticide by a male Milne-Edwards’ sportive lemur (Lepilemur edwardsi) in Ampijoroa NW-Madagascar. Int J Primatol 21:41–45
Rasoloharijaona S, Rakotosamimanana B, Randrianambinina B, Zimmermann E (2003) Pair-specific usage of sleeping sites and their implications for social organization in a nocturnal Malagasy primate, the Milne Edwards’ sportive lemur (Lepilemur edwardsi). Am J Phys Anthropol 122:251–258
Read AF, Harvey PH (1989) Life history differences among the eutherian radiations. J Zool 219:329–353
Reichard UH, Barelli C (2008) Life history and reproductive strategies of Khao Yai Hylobates lar: implications for social evolution in apes. Int J Primatol 29:823–844
Reiches MW, Ellison PT, Lipson SF, Sharrock KC, Gardiner E, Duncan LG (2009) Pooled energy budget and human life history. Am J Hum Biol 21:421–429
Richard AF (1985) Social boundaries in a Malagasy prosimian, the sifaka (Propithecus verreauxi). Int J Primatol 6:553–568
Ricklefs RE (1998) Evolutionary theories of aging: confirmation of a fundamental prediction, with implications for the genetic basis and evolution of life span. Am Nat 152:24–44
Robinson JG, Wright PC, Kinzey WG (1987) Monogamous cebids and their relatives: intergroup calls and spacing. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 44–53
Ross C (1988) The intrinsic rate of natural increase and reproductive effort in primates. J Zool 214:199–219
Ross C (1991) Life history patterns of New World monkeys. Int J Primatol 12:481–502
Ross C (1992a) Basal metabolic rate, body weight and diet in primates: an evaluation of the evidence. Folia Primatol 58:7–23
Ross C (1992b) Environmental correlates of the intrinsic rate of natural increase in primates. Oecologia 90:383–390
Ross C (1998) Primate life histories. Evol Anthropol 6:54–63
Ross C (2001) Park or ride? Evolution of infant carrying in primates. Int J Primatol 22:749–771
Ross C (2003) Life history, infant care strategies, and brain size in primates. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 266–284
Ross C, Jones KE (1999) Socioecology and the evolution of primate reproductive rates. In: Lee PC (ed) Comparative primate socioecology. Cambridge University Press, Cambridge, pp 73–110
Ross C, Mac Larnon A (2000) The evolution of non-maternal care in anthropoid primates: a test of the hypotheses. Folia Primatol 71:93–113
Ross AC, Porter LM, Power ML, Sodaro V (2010) Maternal care and infant development in Callimico goeldii and Callithrix jacchus. Primates 51:315–325
Rothe H, Darms K, Koenig A, Radespiel U, Juenemann B (1993) Long-term study of infant-carrying behavior in captive common marmosets (Callithrix jacchus): effect of nonreproductive helpers on the parents’ carrying performance. Int J Primatol 14:79–93
Rowe N, Myers M (eds) (2013) All the World’s Primates (alltheworldsprimates.org). Primate Conservation, Charlestown
Rowell TE, Richards JM (1979) Reproductive strategies of some African monkeys. J Mammal 60:58–69
Rudran R (1973) The reproductive cycles of two subspecies of purple-faced langurs (Presbytis senex) with relation to environmental factors. Folia Primatol 19:41–60
Sacher GA (1959) Relation of lifespan to brain weight and body weight in mammals. In: Wolstenholme GEW, O’Connor M (eds) The lifespan of animals: CIBA foundation colloquia on ageing, vol 5. J & A Churchill, London, pp 115–133
Scheumann M, Rabesandratana A, Zimmermann E (2007) Predation, communication and cognition in lemurs. In: Gursky SL, Nekaris KAI (eds) Primate anti-predator strategies. Springer, New York, pp 100–126
Schmelting B, Ehresmann P, Lutermann H, Randrianambinina B, Zimmermann E (2000) Reproduction of two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in north-west Madagascar: first results of a long term study. In: Lourenço WR, Goodman SM (eds) Diversité et Endémisme à Madagascar. Société de Biogéographie, Paris, pp 165–175
Schuppli C, Isler K, van Schaik CP (2012) How to explain the unusually late age at skill competence among humans. J Hum Evol 63:843–850
Smith BH, Tompkins RL (1995) Toward a life history of the Hominidae. Ann Rev Anthropol 24:257–279
Soini P (1982) Distribución geográfica ecología poblacional de Saguinus mystax. Report to the Peruvian Minister of Agriculture
Sol D (2009) Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol Lett 5:130–133
Solanki GS, Kumar A, Sharma BK (2007) Reproductive strategies of Trachypithecus pileatus in Arunachal Pradesh, India. Int J Primatol 28:1075–1083
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Tardif SD, Smucny DA, Abbott DH, Mansfield K, Schultz-Darken N, Yamamoto ME (2003) Reproduction in captive common marmosets (Callithrix jacchus). Comp Med 53:364–368
Tecot SR (2010) It’s all in the timing: birth seasonality and infant survival in Eulemur rubriventer. Int J Primatol 31:715–735
Tecot SR, Baden AL, Romine NK, Kamilar JM (2012) Infant parking and nesting, not allomaternal care, influence Malagasy primate life histories. Behav Ecol Sociobiol 66:1375–1386
Tilden CD, Oftedal OT (1997) Milk composition reflects pattern of maternal care in prosimian primates. Am J Primatol 41:195–211
Tilson RL (1981) Family formation strategies of Kloss’s gibbons. Folia Primatol 35:259–287
Utami SS, Goossens B, Bruford MW, de Ruiter JR, van Hooff J (2002) Male bimaturism and reproductive success in Sumatran orang-utans. Behav Ecol 13:643–652
van Schaik CP, Deaner RO (2002) Life history and cognitive evolution in primates. In: De Waal FBM, Tyack PL (eds) Animal social complexity: intelligence, culture, and individualized societies. Harvard University Press, Cambridge, MA, pp 5–25
van Schaik CP, van Hooff J (1983) On the ultimate causes of primate social systems. Behaviour 85:91–117
van Schaik CP, Isler K, Burkart JM (2012) Explaining brain size variation: from social to cultural brain. Trends Cogn Sci 16:277–284
Volampeno MSN, Masters JC, Downs CT (2011) Life history traits, maternal behavior and infant development of blue-eyed black lemurs (Eulemur flavifrons). Am J Primatol 73:474–484
Voland E, Beise J (2002) Opposite effects of maternal and paternal grandmothers on infant survival in historical Krummhörn. Behav Ecol Sociobiol 52:435–443
Walker RS, Gurven M, Burger O, Hamilton MJ (2008) The trade-off between number and size of offspring in humans and other primates. Proc R Soc Lond B 275:827–833
Weiss K (1981) Evolutionary perspectives on human aging. In: Amoss PT, Harrell S (eds) Other ways of growing old: anthropological perspectives. Stanford University Press, Stanford, pp 111–124
Wells JCK, DeSilva JM, Stock JT (2012) The obstetric dilemma: an ancient game of Russian roulette, or a variable dilemma sensitive to ecology? Am J Phys Anthropol 55:40–71
Whitten PL (1987) Infants and adult males. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 343–357
Whitten PL, Turner TR (2009) Endocrine mechanisms of primate life history trade-offs: growth and reproductive maturation in vervet monkeys. Am J Hum Biol 21:754–761
Wich SA, Utami-Atmoko SS, Setia TM, Rijksen HD, Schürmann C, van Hooff J, van Schaik CP (2004) Life history of wild Sumatran orangutans (Pongo abelii). J Hum Evol 47:385–398
Wirz A, Riviello MC (2008) Reproductive parameters of a captive colony of capuchin monkeys (Cebus apella) from 1984 to 2006. Primates 49:265–270
Wrogemann D, Radespiel U, Zimmermann E (2001) Comparison of reproductive characteristics and changes in body weight between captive populations of rufous and gray mouse lemurs. Int J Primatol 22:91–108
Young AL, Richard AF, Aiello LC (1990) Female dominance and maternal investment in strepsirhine primates. Am Nat 135:473–488
Young JW, Fernandez D, Fleagle JG (2010) Ontogeny of long bone geometry in capuchin monkeys (Cebus albifrons and Cebus apella): implications for locomotor development and life history. Biol Lett 6:197–200
Zhao Q, Tan CL, Pan W (2008) Weaning age, infant care, and behavioral development in Trachypithecus leucocephalus. Int J Primatol 29:583–591
Zimmermann E (1989) Reproduction, physical growth and behavioral development in slow loris (Nycticebus coucang, Lorisidae). Hum Evol 4:171–179
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Appendix
Appendix
See Table 1
Rights and permissions
Copyright information
© 2013 Springer-Verlag Berlin Heidelberg
About this entry
Cite this entry
Zimmermann, E., Radespiel, U. (2013). Primate Life Histories. In: Henke, W., Tattersall, I. (eds) Handbook of Paleoanthropology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-27800-6_38-7
Download citation
DOI: https://doi.org/10.1007/978-3-642-27800-6_38-7
Received:
Accepted:
Published:
Publisher Name: Springer, Berlin, Heidelberg
Online ISBN: 978-3-642-27800-6
eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences