A COMPARATIVE STUDY OF LEUKOCYTE COUNTS AND DISEASE RISK IN PRIMATES
Charles L. Nunn
Biology Department, University of Virginia, Charlottesville, Virginia 22904-4328
Section of Evolution and Ecology, University of California, Davis, California 95616; E-mail: [email protected].
Search for more papers by this authorCharles L. Nunn
Biology Department, University of Virginia, Charlottesville, Virginia 22904-4328
Section of Evolution and Ecology, University of California, Davis, California 95616; E-mail: [email protected].
Search for more papers by this authorAbstract
Abstract Little is known about how the risk of disease varies across species and its consequences for host defenses, including the immune system. I obtained mean values of basal white blood cells (WBC) from 100 species of primates to quantify disease risk, based on the assumption that higher baseline WBC counts will be found in species that experience greater risk of acquiring infectious disease. These data were used to investigate four hypotheses: disease risk is expected to increase with (1) group size and population density; (2) greater contact with soil-borne pathogens during terrestrial locomotion; (3) a slow life history; and (4) increased mating promiscuity. After controlling for phylogeny, WBC counts increased with female mating promiscuity, as reflected in discrete categories of partner number, relative testes mass, and estrous duration. By comparison, the social, ecological, and life-history hypotheses were unsupported in comparative tests. In terms of confounding variables, some WBC types were associated with body mass or activity period, but these variables could not account for the association with mating promiscuity. Several factors may explain why hypotheses involving social, ecological, and life-history factors went unsupported in these tests, including the role of behavioral counterstrategies to disease, restrictions on female choice of mating partners, and the effect of transmission mode on parasite strategies and host defenses.
Literature Cited
- Abouheif, E. 1999. A method for testing the assumption of phylogenetic independence in comparative data. Evol. Ecol. Res. 1: 895–909.
-
Alexander, R. D.
1974. The evolution of social behavior.
Annu. Rev. Ecol. Syst.
5: 325–383.
10.1146/annurev.es.05.110174.001545 Google Scholar
- Antia, R., B. R. Levin, and R. M. May. 1994. Within-host population dynamics and the evolution of maintenance of microparasite virulence. Am. Nat. 144: 457–472.
- Arneberg, P., A. Skorping, B. Grenfell, and A. F. Read. 1998a. Host densities as determinants of abundance in parasite communities. Proc. R. Soc. Lond. B 265: 1283–1289.
- Arneberg, P., A. Skorping, and A. F. Read. 1998b. Parasite abundance, body size, life histories, and the energetic equivalence rule. Am. Nat. 151: 497–513.
- Barratt, C. L. R., A. E. Bolton, and I. D. Cooke. 1990. Functional significance of white blood cells in the male and female reproductive tract. Hum. Reprod. 5: 639–648.
- Barton, R. A., and P. H. Harvey. 2000. Mosaic evolution of brain structure in mammals. Nature 405: 1055–1058.
- Bearder, S. K. 1987. Lorises, bushbabies, and tarsiers: diverse societies in solitary foragers. Pp. 11–24 in B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham and T. T. Struhsaker, eds. Primate societies. Univ. of Chicago Press, Chicago , IL .
- Bennett, P. M., and C. M. Hawkey. 1988. Comparative haematology: phylogenetic and ecological aspects in mammals and birds. Pp. 33–48 in D. J. Blackmore, ed. Animal clinical biochemistry. Cambridge Univ. Press, Cambridge , U.K.
- Borer, W. Z. 2000. Reference intervals for the interpretation of laboratory tests. Pp. 1205–1213 in R. E. Rakel, ed. Conn's current therapy. W. B. Saunders, Philadelphia , PA .
- Clutton-Brock, T. H., and P. H. Harvey. 1977. Primate ecology and social organization. J. Zool. (Lond.) 183: 1–39.
- Clutton-Brock, T. H., and G. A. Parker. 1995. Sexual coercion in animal societies. Anim. Behav. 49: 1345–1365.
- Clutton-Brock, T. H., P. H. Harvey, and B. Rudder. 1977. Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature 269: 797–800.
-
Cohen, J.
1988. Statistical power analysis for the behavioral sciences. Erlbaum Associates,
Hillsdale
,
NJ
.
10.1046/j.1526-4610.2001.111006343.x Google Scholar
- Cohen, M. S., R. D. Weber, and P. A. Mardh. 1994. Genitourinary mucosal defenses. Pp. 117–127 in K. K. Holmes, P. F. Sparling, P. A. Mardh, S. M. Lemon, W. E. Stamm, P. Piot and J. N. Wasserheit, eds. Sexually transmitted diseases. McGraw-Hill, New York .
- Côté, I. M., and R. Poulin. 1995. Parasitism and group size in social animals: a meta-analysis. Behav. Ecol. 6: 159–165.
- Cotgreave, P., and D. H. Clayton. 1994. Comparative analysis of time spent grooming by birds in relation to parasite load. Behaviour 131: 171–187.
- Dacie, J. V., and S. M. Lewis. 1991. Practical haematology. Churchill Livingstone, Edinburgh .
-
Demas, G. E.,
V. Chefer,
M. I. Talan, and
R. J. Nelson. 1997. Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice.
Am. J. Physiol.
42: R1631–R1637.
10.1152/ajpregu.1997.273.5.R1631 Google Scholar
- Dixson, A. F. 1998. Primate sexuality. Oxford Univ. Press, Oxford , U.K.
- Dobson, A. P., and M. Meagher. 1996. The population dynamics of brucellosis in the Yellowstone National Park. Ecology 77: 1026–1036.
- Donovan, B. 2000a. The repertoire of human efforts to avoid sexually transmissible diseases: past and present. Part 1. Strategies used before or instead of sex. Sex. Transm. Infect. 76: 7–12.
- Donovan, B. 2000b. The repertoire of human efforts to avoid sexually transmissible diseases: past and present. Part 2. Strategies used during or after sex. Sex. Transm. Infect. 76: 88–93.
- Dudley, R., and K. Milton. 1990. Parasite deterrence and the energetic costs of slapping in howler monkeys, Alouatta palliata. J. Mammal. 71: 463–465.
-
Eberhard, W. G.
1996. Female control: sexual selection by cryptic female choice. Princeton Univ. Press,
Princeton
,
NJ
.
10.1515/9780691207209 Google Scholar
- Erdfelder, E., F. Faul, and A. Buchner. 1996. GPOWER: a general power analysis program. Behav. Res. Meth. Instr. Comp. 28: 1–11.
- Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125: 1–15.
- Fleagle, J. G. 1988. Primate adaptation and evolution. Academic Press, New York .
- Freckleton, R. P. 2000. Phylogenetic tests of ecological and evolutionary hypotheses: checking for phylogenetic independence. Funct. Ecol. 14: 129–134.
- Freeland, W. J. 1976. Pathogens and the evolution of primate sociality. Biotropica 8: 12–24.
- Garland, T. J., P. H. Harvey, and A. R. Ives. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 4: 18–32.
- Garland, T., Jr., A. W. Dickerman, C. M. Janis, and J. A. Jones. 1993. Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42: 265–292.
- Gittleman, J. L. 1985. Carnivore body size: ecological and taxonomic correlates. Oecologia (Heidelb.) 67: 540–554.
- Gittleman, J. L., and M. Kot. 1990. Adaptation: statistics and a null model for estimating phylogenetic effects. Syst. Zool. 39: 227–241.
- Goldizen, A. W. 1988. Tamarin and marmoset mating systems: unusual flexibility. Trends Ecol. Evol. 3: 36–40.
- Gregory, R. D. 1990. Parasites and host geographic range as illustrated by waterfowl. Funct. Ecol. 4: 645–654.
- Harcourt, A. H., P. H. Harvey, S. G. Larson, and R. V. Short. 1981. Testis weight, body weight and breeding system in primates. Nature 293: 55–57.
- Harcourt, A. H., A. Purvis, and L. Liles. 1995. Sperm competition: mating system, not breeding system, affects testes size of primates. Funct. Ecol. 9: 468–476.
- Hart, B. L. 1990. Behavioral adaptations to pathogens and parasites: five strategies. Neurosci. Biobehav. Rev. 14: 273–294.
- Hart, B. J., E. Korinek, and P. Brennan. 1987. Postcopulatory genital grooming in male rats: prevention of sexually transmitted infections. Physiol. Behav. 41: 321–325.
-
Harvey, P. H., and
M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford Univ. Press,
Oxford
,
U.K.
10.1093/oso/9780198546412.001.0001 Google Scholar
- Harvey, P. H., and A. Rambaut. 2000. Comparative analyses for adaptive radiations. Proc. R. Soc. Lond. B. Biol. Sci. 355: 1–7.
- Harvey, P. H., A. F. Read, J. L. John, R. D. Gregory, and A. E. Keymer. 1991. An evolutionary perspective: using the comparative method. Pp. 344–355 in C. A. Toft, A. Aeschlimann, and L. Bolis, eds. Parasite-host associations. Oxford Univ. Press, Oxford , U.K.
-
Hausfater, G., and
B. J. Meade. 1982. Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasite avoidance.
Primates
23: 287–297.
10.1007/BF02381167 Google Scholar
- Hawkey, C. M. 1977. The haematology of exotic mammals. Pp. 103–160 in R. K. Archer, L. B. Jeffcott and H. Lehmann, eds. Comparative clinical haematology. Blackwell Scientific, Oxford , U.K.
- Hawkey, C. M., and P. M. Bennett. 1988. Comparative haematology: clinical aspects in mammals and birds. Pp. 49–62 in D. J. Blackmore, ed. Animal clinical biochemistry. Cambridge Univ. Press, Cambridge , U.K.
- Hawkey, C. M., P. M. Bennett, S. C. Gascoyne, M. G. Hart, and J. K. Kirkwood. 1991. Erythrocyte size, number and hemoglobin content in vertebrates. Br. J. Haematol. 77: 392–397.
- Hill, R. A., and R. I. M. Dunbar. 1998. An evaluation of the roles of predation rate and predation risk as selective pressures on primate grouping behaviour. Behaviour 135: 411–430.
-
Hogarth, P. J.
1982. Immunological aspects of mammalian reproduction. Praeger Scientific,
Glasgow
,
Scotland
.
10.1007/978-94-011-6859-5 Google Scholar
- Holmes, K. K., P. F. Sparling, P. A. Mardh, S. M. Lemon, W. E. Stamm, P. Piot, and J. N. Wasserheit. 1994. Sexually transmitted diseases. McGraw-Hill, New York .
- Janson, C. H. 1998. Testing the predation hypothesis for vertebrate sociality: prospects and pitfalls. Behaviour 135: 389–410.
- Janson, C. H., and M. Goldsmith. 1995. Predicting group size in primates: foraging costs and predation risk. Behav. Ecol. 6: 326–336.
- John, J. L. 1995. Parasites and the avian spleen. Biol. J. Linn. Soc. 54: 87–106.
- Jolly, A. 1966. Lemur behavior. Univ. Chicago Press, Chicago , IL .
- Kavaliers, M., D. D. Colwell, K. P. Ossenkopp, and T. S. Perrot-Sinal. 1997. Altered responses to female odors in parasitized male mice: neuromodulatory mechanisms and relations to female choice. Behav. Ecol. Sociobiol. 40: 373–384.
- Klein, S. L., H. R. Gamble, and R. J. Nelson. 1999. Trichinella spiralis infection in voles alters female odor preference but not partner preference. Behav. Ecol. Sociobiol. 45: 323–329.
- Knell, R. J. 1999. Sexually transmitted disease and parasite-mediated sexual selection. Evolution 53: 957–961.
-
Larson, S. G.
1985. Organ weight scaling in primates. Pp.
91–113
in
W. L. Jungers, ed.
Size and scaling in primate biology. Plenum,
New York
.
10.1007/978-1-4899-3647-9_6 Google Scholar
-
Lloyd, S.
1995. Environmental influences on host immunity. Pp.
327–361
in
B. T. Grenfell and
A. P. Dobson, eds.
Ecology of infectious diseases in natural populations. Cambridge Univ. Press,
Cambridge
,
U.K.
10.1017/CBO9780511629396.013 Google Scholar
- Lockhart, A. B., P. H. Thrall, and J. Antonovics. 1996. Sexually transmitted diseases in animals: ecological and evolutionary implications. Biol. Rev. 71: 415–471.
- Loehle, C. 1995. Social barriers to pathogen transmission in wild animal populations. Ecology 76: 326–335.
- Luh, H.-K., J. L. Gittleman, and M. Kot. 1995. Phylogenetic autocorrelation. Ver. 1.1. Available via ftp:ftp.math.utk.edupubluhPAhqx.
- Maddison, W. P., and D. R. Maddison. 1992. MacClade. Sinauer Associates, Sunderland , MA .
- Marshburn, P. B., and W. H. Kutteh. 1994. The role of antisperm antibodies in infertility. Fertil. Steril. 61: 799–811.
- McGrew, W. C., C. E. G. Tutin, D. A. Collins, and S. K. File. 1989. Intestinal parasites of sympatric Pan troglodytes and Papio spp. at two sites: Gombe (Tanzania) and Mt. Assirik (Senegal). Am. J. Primatol. 17: 147–155.
- Milton, K. 1984. Habitat, diet, and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoids E. Geoffroy 1806). Int. J. Primatol. 5: 491–514.
- Milton, K. 1996. Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler monkey (Alouatta palliata) population in Panama. J. Zool. (Lond.) 239: 39–63.
- Milton, K., and M. L. May. 1976. Body weight, diet and home range area in primates. Nature 259: 459–462.
- Mitani, J., J. Gros-Louis, and A. F. Richards. 1996. Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primates. Am. Nat. 147: 966–980.
- Møller, A. P. 1997. Immune defence, extra-pair paternity, and sexual selection in birds. Proc. R. Soc. Lond. B 264: 561–566.
- Møller, A. P., R. Dufva, and K. Allander. 1993. Parasites and the evolution of host social behavior. Adv. Study Behav. 22: 65–102.
- Møller, A. P., R. Dufva, and J. Erritzoe. 1998. Host immune function and sexual selection in birds. J. Evol. Biol. 11: 703–719.
- Morand, S., and R. Poulin. 2000. Nematode parasite species richness and the evolution of spleen size in birds. Can. J. Zool. 78: 1356–1360.
- Moret, Y., and P. Schmid-Hempel. 2000. Survival for immunity: the price of immune system activation for bumblebee workers. Science 290: 1166–1168.
- Nordling, D., M. Andersson, S. Zohari, and L. Gustafsson. 1998. Reproductive effort reduces specific immune response and parasite resistance. Proc. R. Soc. Lond. B 265: 1291–1298.
- Nunn, C. L., and R. A. Barton. 2000. Allometric slopes and independent contrasts: a comparative test of Kleiber's law in primate ranging patterns. Am. Nat. 156: 519–533.
- Nunn, C. L., and R. A. Barton. 2001. Comparative methods for studying primate adaptation and allometry. Evol. Anthropol. 10: 81–98.
- Nunn, C. L., and K. K. Smith. 1998. Statistical analyses of developmental sequences: the craniofacial region in marsupial and placental mammals. Am. Nat. 152: 82–101.
-
Nunn, C. L., and
C. P. van Schaik. 2000. Intersexual conflict and ecological factors in primate social evolution. Pp.
388–419
in
C. P. Schaik and
C. Janson, eds.
Infanticide by males and its implications. Cambridge Univ. Press,
Cambridge
,
U.K.
10.1017/CBO9780511542312.018 Google Scholar
- Nunn, C. L., and C. P. van Schaik. 2001. Reconstructing the behavioral ecology of extinct primates. Pp. 159–216 in J. M. Plavcan, R. F. Kay, W. L. Jungers, and C. P. Schaik, eds. Reconstructing behavior in the fossil record. Kluwer Academic/Plenum, New York .
- Nunn, C. L., J. L. Gittleman, and J. Antonovics. 2000. Promiscuity and the primate immune system. Science 290: 1168–1170.
- Palombit, R. A. 1994. Extra-pair copulations in a monogamous ape. Anim. Behav. 47: 721–723.
- Pandya, I. J., and J. Cohen. 1985. The leukocytic reaction of the human uterine cervix to spermatozoa. Fertil. Steril. 43: 417–421.
- Penn, D., G. Schneider, K. White, P. Slev, and W. Potts. 1998. Influenza infection neutralizes the attractiveness of male odour to female mice (Mus musculus). Ethology 104: 685–694.
- Phillips, D. M., and S. Mahler. 1977. Leukocyte emigration and migration in the vagina following mating in the rabbit. Anat. Rec. 189: 45–60.
- Poulin, R. 1995. Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecol. Monogr. 65: 283–302.
- Price, T. 1997. Correlated evolution and independent contrasts. Philos. Trans. R. Soc. Lond. B 352: 519–529.
- Purvis, A. 1995. A composite estimate of primate phylogeny. Philos. Trans. R. Soc. Lond. B 348: 405–421.
- Purvis, A., and A. Rambaut. 1995. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comput. Applic. Biosci. 11: 247–251. Available via http:www.bio.ic.ac.ukevolvesoftwarecaicindex.html.
-
Purvis, A., and
A. J. Webster. 1999. Phylogenetically independent contrasts and primate phylogeny. Pp.
44–68
in
P. Lee, ed.
Comparative primate socioecology. Cambridge Univ. Press,
Cambridge
,
U.K.
10.1017/CBO9780511542466.005 Google Scholar
- Quinn, T. C. 1992. Sexually transmitted diseases. Advances in host defense mechanisms. Vol. 8. J. I. Gallin and A. S. Fauci, series Eds. Raven Press, New York .
- Reichard, U. 1995. Extra-pair copulation in a monogamous gibbon (Hylobates lar). Ethology 100: 99–112.
- Reeve, J., and E. Abouheif. 1999. Phylogenetic independence. Ver. 1.1. Available via http:life.bio.sunysb.edueeehab.
- Robinson, J. G., P. C. Wright, and W. G. Kinzey. 1987. Monogamous cebids and their relatives: intergroup calls and spacing. Pp. 47–53 in B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Stuhsaker, eds. Primate societies. Univ. Chicago Press, Chicago , IL .
- Roitt, I. M., J. Brostoff, and D. K. Male. 1998. Immunology. Gower Medical Publishing, London .
-
Ross, C., and
K. E. Jones. 1999. Socioecology and the evolution of primate reproductive rates. Pp.
73–110
in
P. C. Lee, ed.
Comparative primate socioecology. Cambridge Univ. Press,
Cambridge
,
U.K.
10.1017/CBO9780511542466.007 Google Scholar
- Rothman, K. J. 1990. No adjustments are needed for multiple comparisons. Epidemiology 1: 43–46.
- Rowe, N. 1996. The pictorial guide to the living primates. Pogonias Press, East Hampton , NY .
- Rubenstein, D. I., and M. E. Hohmann. 1989. Parasites and social behavior of island feral horses. Oikos 55: 312–320.
- Schwimmer, W. B., K. A. Ustay, and S. J. Behrman. 1967. An evaluation of immunologic factors of infertility. Fertil. Steril. 18: 167–180.
- Sheldon, B. C., and S. Verhulst. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11: 317–321.
- Smith, G., and A. P. Dobson. 1992. Sexually transmitted diseases in animals. Parasitol. Today 8: 159–166.
- Smith, R. J., and W. L. Jungers. 1997. Body mass in comparative primatology. J. Hum. Evol. 32: 523–559.
- Smuts, B. B., and R. W. Smuts. 1993. Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Adv. Study Behav. 22: 1–63.
-
Sokal, R. R., and
F. J. Rohlf. 1995. Biometry. 3rd ed.
W. H. Freeman and Co.,
New York
.
10.1577/1548-8659(1986)115<149:LOPDOR>2.0.CO;2 Google Scholar
- Stuart, M. D., L. L. Greenspan, K. E. Glander, and M. R. Clarke. 1990. A coprological survey of parasites of wild mantled howling monkeys, Alouatta palliata palliata. J. Wildl. Dis. 26: 547–549.
- Thomas, L., and F. Juanes. 1996. The importance of statistical power analysis: an example from Animal Behaviour. Anim. Behav. 52: 856–859.
- Thrall, P. H., J. Antonovics, and J. D. Bever. 1997. Sexual transmission of disease and host mating systems: within-season reproductive success. Am. Nat. 149: 485–506.
- Thrall, P. H., J. Antonovics, and A. P. Dobson. 2000. Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success. Proc. R. Soc. Lond. B 267: 1555–1563.
- Valderrama, X., J. G. Robinson, A. B. Attygalle, and T. Eisner. 2000. Seasonal anointment with millipedes in a wild primate: A chemical defense against insects J. Chem. Ecol. 26: 2781–2790.
-
van Schaik, C. P.,
M. A. van Noordwijk, and
C. L. Nunn. 1999. Sex and social evolution in primates. Pp.
204–240
in
P. C. Lee, ed.
Comparative primate socioecology. Cambridge Univ. Press,
Cambridge
,
U.K.
10.1017/CBO9780511542466.011 Google Scholar
- Wrangham, R. W. 1993. The evolution of sexuality in chimpanzees and bonobos. Hum. Nature 4: 47–79.
- Wrangham, R. W., J. L. Gittleman, and C. A. Chapman. 1993. Constraints on group size in primates and carnivores: population density and day-range as assays of exploitation competition. Behav. Ecol. Sociobiol. 32: 199–209.