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Life history costs and consequences of rapid reproductive maturation in female rhesus macaques

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Summary

Life history theory suggests that reproduction at one point in time involves costs in terms of energy, reduced survival, or probability of reproduction at a future point in time. ln long-lived iteroparous organisms, initiating reproduction at a relatively young age may exact a cost in terms of reduced survivorship, but an early age of first reproduction could be beneficial if it lengthens the breeding lifespan. Data collected over 30 years from one population of rhesus macaques, Macaca mulatta, were analyzed to determine the fertility and survivorship costs of initiating reproduction at a relatively young age. Low population density and high social status increased the chances of accelerating age at first parturition, but high dominance rank was not associated with greater lifetime reproductive success. Rapid reproductive maturation neither reduced short-term survivorship nor decreased lifespan. Fertility costs arose if young females reared a male, but not female, offspring. The fitness consequences of rapid reproductive maturation depend upon longevity, with age at death having a significantly greater impact on lifetime reproductive success than age at first parturition.

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References

  • Altman J, Hausfater G, Altmann SA (1988) Determinants of reproductive success in savannah baboons, Papio cynocephalus. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 403–418

    Google Scholar 

  • Altmann SA (1962) A field study on the sociobiology of rhesus monkeys (Macaca mulatta). Ann NY Acad Sci 102:338–435

    Google Scholar 

  • Bell G (1980) The costs of reproduction and their consequences. Am Nat 116:45–76

    Google Scholar 

  • Berard JD (1990) Life history patterns of male rhesus macaques. PhD diss, University of Oregon

  • Bercovitch FB (1991) Social stratification, social strategies, and reproductive success in primates. Ethol Sociobiol 12:315–333

    Google Scholar 

  • Bercovitch FB, Goy RW (1990) The socioendocrinology of reproductive development and reproductive success in macaques. In: Ziegler TE, Bercovitch FB (eds) Socioendocrinology of primate reproduction. Wiley-Liss, NY, pp 59–93

    Google Scholar 

  • Berman CM (1988) Maternal condition and offspring sex ratio in a group of free-ranging rhesus monkeys: an eleven year study. Am Nat 131:307–328

    Google Scholar 

  • Bryant DM (1979) Reproductive costs in the house martin (Delichon urbica). J Anim Ecol 48:655–675

    Google Scholar 

  • Chapais B, Schulman SR (1980) An evolutionary model of female dominance relations in primates. J Theor Biol 82:47–89

    Google Scholar 

  • Cheney CL, Seyfarth RM, Andelman SJ, Lee PC (1988) Reproductive success in vervet monkeys. In: Clutton-Brock TH (ed), Reproductive success. University of Chicago Press, Chicago, pp 384–402

    Google Scholar 

  • Clutton-Brock TH (ed) (1988) Reproductive success. University of Chicago Press, Chicago

    Google Scholar 

  • Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: Behavior and ecology of two sexes. University of Chicago Press, Chicago

    Google Scholar 

  • Clutton-Brock TH, Guinness FE, Albon SD (1983) The costs of reproduction to red deer hinds. J Anim Ecol 52:367–383

    Google Scholar 

  • Datta S (1988) The acquisition of dominance among free-ranging rhesus monkey siblings. Anim Behav 36:754–772

    Google Scholar 

  • De Steven D (1980) Clutch size, breeding success and parental survival in the tree swallow (Iridoprocne bicolor). Evolution 34:278–291

    Google Scholar 

  • Drickamer LC (1974) A ten-year summary of reproductive data for free-ranging Macaca mulatta. Folia Primatol 21:61–80

    Google Scholar 

  • Duggleby CR, Haseley PA, Rawlins RG, Kessler MJ (1986) An overview of blood group genetic studies on the Cayo Santiago rhesus monkeys. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques. SUNY Press, Albany, pp 269–282

    Google Scholar 

  • Ekman J, Askenmo C (1986) Reproductive cost, age-specific survival and a comparison of the reproductive strategy in two European tits (Genus Parus). Evolution 40:159–168

    Google Scholar 

  • Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton

    Google Scholar 

  • Falconer DS (1960) Introduction to quantitative genetics. Ronald Press, New York

    Google Scholar 

  • Fedigan LM (1983) Dominance and reproductive success in primates. Yrbk Phys Anthropol 26:91–129

    Google Scholar 

  • Fedigan LM, Fedigan L, Gouzoules S, Gouzoules H, Koyama N (1986) Lifetime reproductive success in female Japanese macaques. Folia Primatol 47:143–157

    Google Scholar 

  • Gadgil M, Bossert WH (1970) Life historical consequences of natural selection. Am Nat 104:1–24

    Google Scholar 

  • Green WCH, Berger J (1990) Maternal investment in sons and daughters: problems of methodology. Behav Ecol Sociobiol 27:99–102

    Google Scholar 

  • Gustaffson L, Part T (1990) Acceleration of senescence in the collared flycatcher Ficedula albicollis by reproductive costs. Nature 347:279–281

    Google Scholar 

  • Harcourt AH (1987) Dominance and fertility among female primates. J Zool 213:471–487

    Google Scholar 

  • Harvey PH, Clutton-Brock TH (1985) Life history variation in primates. Evol 39:559–581

    Google Scholar 

  • Harvey PH, Martin RD, Clutton-Brock TH (1987) Life histories in a comparative perspective. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 181–196

    Google Scholar 

  • Horn HS, Rubenstien DI (1984) Behavioural adaptations and life history. In: Krebs JR, Davies NB (eds) Behavioral ecology: An evolutionary approach, 2nd edn. Sinauer, Sunderland, pp 279–298

    Google Scholar 

  • Koyama N, Takahata Y, Huffman M, Norikoshi N, Suzuki H (1992) Reproductive parameters of female Japanese macaques: Thirty years data from the Arashiyama troops, Japan. Primates 33:33–47

    Google Scholar 

  • Lee PC, Moss CJ (1986) Early maternal investment in male and female African elephant calves. Behav Ecol Sociobiol 18:353–361

    Google Scholar 

  • Loy J (1988) Effects of supplementary feeding on maturation and fertility in primate groups. In: Fa J, Southwick CH (eds) Ecology and behavior of food-enhanced primate groups. Alan R. Liss, New York, pp 153–166

    Google Scholar 

  • Luckinbill LS, Arking R, Clark MG, Cirocco WW, Buck SA (1984) Selection for delayed senescence in Drosophila melanogaster. Evolution 38:996–1003

    Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  • Marriott BM (1988) Time budgets of rhesus monkeys (Macaca mulatta) in a forest habitat in Nepal and on Cayo Santiago. In: Fa J, Southwick CH (eds) Ecology and behavior of food-enhanced primate groups. Alan R. Liss, New York, pp 125–149

    Google Scholar 

  • Meikle DB, Vessey SH (1988) Maternal dominance rank and lifetime survivorship of male and female rhesus monkeys. Behav Ecol Sociobiol 22:379–383

    Google Scholar 

  • Newton I (ed) (1989) Lifetime reproductive success in birds. Academic Press, San Diego

    Google Scholar 

  • Nur N (1984) The consequences of brood size for breeding blue tits. I. Adult survival, weight change and the cost of reproduction. J Anim Ecol 53:479–496

    Google Scholar 

  • Partridge L, Harvey PH (1988) The ecological context of life history evolution. Science 241:1449–1455

    Google Scholar 

  • Paul A, Thommen D (1984) Timing of birth, female reproductive success and infant sex ratio in semifree-ranging Barbary macaques (Macaca sylvanus). Folia Primatol 42:2–16

    Google Scholar 

  • Pianka ER (1978) Evolutionary ecology. Harper & Row, New York

    Google Scholar 

  • Pianka ER, Parker WS (1975) Age-specific reproductive tactics. Am Nat 109:453–464

    Google Scholar 

  • Rawlins RG, Kessler MJ (1985) Climate and seasonal reproduction in the Cayo Santiago macaques. Am J Primatol 9:87–99

    Google Scholar 

  • Rawlins RG, Kessler MJ (1986a) The history of the Cayo Santiago colony. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques. SUNY Press, Albany, pp 13–45

    Google Scholar 

  • Rawlins RG, Kessler MJ (1986b) Demography of the free-ranging Cayo Santiago macaques (1976–1983). In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques. SUNY Press, Albany, pp 47–72

    Google Scholar 

  • Reiter J, Le Boeuf BJ (1991) Life history consequences of variation in age at primiparity in northern elephant seals. Behav Ecol Sociobiol 28:153–160

    Google Scholar 

  • Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267

    Google Scholar 

  • Roberts MS (1978) The annual reproductive cycle of captiva Macaca sylvanus. Folia Primatol 29:229–235

    Google Scholar 

  • Rose MR (1984) Laboratory evolution of postponed senescence in Drosophila melanogaster. Evolution 38:1004–1010

    Google Scholar 

  • Rose MR, Charlesworth B (1981a) Genetics of life-history in Drosophila melanogaster. I. Sib analysis of adult females. Genetics 97:173–186

    Google Scholar 

  • Rose MR, Charlesworth B (1981b) Genetics of life-history in Drosophila melanogaster. II. Exploratory selection experiments. Genetics 97:187–196

    Google Scholar 

  • Sade DS (1967) Determinants of dominance in a group of freeranging rhesus monkeys. In: Altmann SA (ed) Social communication among primates. University of Chicago Press, Chicago, pp 99–114

    Google Scholar 

  • Sade DS (1991) Intrapopulation variation in life-history parameters. In: DeRosseau CJ (ed) Primate life history and evolution. Wiley-Liss, New York, pp 181–194

    Google Scholar 

  • 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 (CT)

    Google Scholar 

  • Simpson MIA, Simpson AE, Hooley J, Zunz M (1981) Infantrelated influences on birth intervals in rhesus monkeys. Nature 290:49–51

    Google Scholar 

  • Smith JNM (1981) Does high fecundity reduce survival in song sparrows? Evolution 35:1142–1148

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. WH Freeman, San Francisco

    Google Scholar 

  • Soumah AG, Yokata N (1991) Female rank and feeding strategies in a free-ranging provisioned troop of Japanese macaques. Folia Primatol 57:191–200

    Google Scholar 

  • Stearns SC (1976) Life history tactics: a review of the ideas. Q Rev Biol 51:3–47

    Google Scholar 

  • Stearns SC (1977) The evolution of life-history traits. A critique of the theory and a review of the data. Annu Rev Ecol Syst 8:145–171

    Google Scholar 

  • Sugiyama Y, Ohsawa H (1982) Population dynamics of Japanese monkeys with special reference to the effect of artificial feeding. Folia Primatol 39:238–263

    Google Scholar 

  • Tuomi JT, Hakala T, Haukioja E (1983) Alternative concepts of reproductive efforts, costs of reproduction, and selection in life history evolution. Am Zool 23:25–34

    Google Scholar 

  • Via S, Lande R (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505–522

    Google Scholar 

  • Williams GC (1966a) Adaptation and natural selection. Princeton University Press, Princeton

    Google Scholar 

  • Williams GC (1966b) Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am Nat 100:687–690

    Google Scholar 

  • Wilson ME, Walker ML, Gordon TP (1983) Consequences of first pregnancy in rhesus monkeys. Am J Phys Anthropol 61:103–110

    Google Scholar 

  • Wolff JO (1988) Maternal investment and sex ratio adjustment in American bison calves. Behav Ecol Sociobiol 23:127–133

    Google Scholar 

  • Zar JH (1974) Biostatistical analysis. Prentice-Hall, Englewood Cliffs

    Google Scholar 

Download references

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Correspondence to: F.B. Bercovitch

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Bercovitch, F.B., Berard, J.D. Life history costs and consequences of rapid reproductive maturation in female rhesus macaques. Behav Ecol Sociobiol 32, 103–109 (1993). https://doi.org/10.1007/BF00164042

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