Many mammal populations show significant deviations from an equal sex ratio at birth, but these effects are notoriously inconsistent1. This may be because more than one mechanism affects the sex ratio and the action of these mechanisms depends on environmental conditions. Here we show that the adaptive relationship between maternal dominance and offspring sex ratio previously demonstrated in red deer (Cervus elaphus)2,3, where dominant females produced more males, disappeared at high population density. The proportion of males born each year declined with increasing population density and with winter rainfall, both of which are environmental variables associated with nutritional stress during pregnancy. These changes in the sex ratio corresponded to reductions in fecundity, suggesting that they were caused by differential fetal loss. In contrast, the earlier association with maternal dominance is presumed to have been generated pre-implantation. The effects of one source of variation superseded the other within about two generations. Comparison with other ungulate studies indicates that positive associations between maternal quality and the proportion of male offspring born have only been documented in populations below carrying capacity.
This is a preview of subscription content
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Clutton-Brock, T. H. & Iason, G. R. Sex ratio variation in mammals. Q. Rev. Biol. 61, 339–373 (1986).
Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E. Great expectations: dominance, breeding success and offspring sex ratios in red deer. Anim. Behav. 34, 460–471 (1986).
Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E. Maternal dominance, breeding success and birth sex ratios in red deer. Nature 308, 358–360 (1984).
Trivers, R. L. & Willard, D. E. Natural selection of parental ability to vary the sex ratio of offspring. Science 179, 90–92 (1973).
Hiraiwa-Hasegawa, M. Skewed birth sex ratios in primates: should high-ranking mothers have daughters or sons? Trends Ecol. Evol. 8, 395–399 (1993).
Cassinello, J. High-ranking females bias their investment in favour of male calves in captive Ammotragus iervia. Behav. Ecol. Sociobiol. 38, 417–424 (1996).
Meikle, D. B., Drickamer, L. C., Bessey, S. H., Arthur, R. D. & Rosenthal, T. L. Dominance rank and parental investment in swine (Sus scrofa domesticus). Ethology 102, 969–978 (1996).
Kojola, I. & Eloranta, E. Influences of maternal body weight, age, and parity on sex ratio in semidomesticated reindeer (Rangifer t. tarandus). Evolution 43, 1331–1336 (1989).
Rutberg, A. T. Lactation and fetal sex ratios in American bison. Am. Nat. 127, 89–94 (1986).
Wauters, L. A., Decrombrugghe, S. A., Nour, N. & Matthysen, E. Do female roe deer in good condition produce more sons than daughters? Behav. Ecol. Sociobiol. 37, 189–193 (1995).
Flint, A. P. F., Albon, S. D. & Jafar, S. I. Blastocyst development and conceptus sex selection in red deer Cervus elaphus : studies of a free-living population on the Isle of Rum. Gen. Comp. Endocrinol. 106 374–383 (1997).
Mendl, M., Zenlla, A. J., Broom, D. M. & Whittemore, C. T. Maternal social-status and birth sex-ratio in domestic pigs: an analysis of mechanisms. Ethol. Sociobiol. 16, 257–333 (1995).
Nygren, T. & Kojola, I. Twinning and fetal sex ratio in moose: effects of maternal age and mass. Can. J. Zool. 75, 1945–1948 (1997).
Birgersson, B. Adaptive adjustment of the sex ratio: more data and considerations from a fallow deer population. Behav. Ecol. 9, 404–408 (1998).
Hewison, A. J. M. & Gaillard, J. M. Birth-sex ratios and local resource competition in roe deer, Capreolus capreolus. Behav. Ecol. 7, 461–464 (1996).
Festa-Bianchet, M. The social system of bighorn sheep: grouping patterns, kinship and female dominance rank. Anim. Behav. 42, 71–82 (1991).
Albon, S. D., Coulson, T. N. & Clutton-Brock, T. H. in Recent Developments in Deer Biology(ed. Milne, J. A.) 85–95 (Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen and Moredun Research Institute, Edinburgh, (1998).
Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. Red Deer—Behaviour and Ecology of Two Sexes(University of Chicago Press, Chicago, (1982).
Gomendio, M., Clutton-Brock, T. H., Albon, S. D., Guinness, F. E. & Simpson, M. J. Mammalian sex ratios and variation in costs of rearing sons and daughters. Nature 343, 261–263 (1990).
Flint, A. P. F., Albon, S. D., Loudon, A. S. I. & Jabbour, H. N. Behavioral dominance and corpus luteum function in red deer Cervus elaphus. Horm. Behav. 31, 296–304 (1997).
Albon, S. D., Clutton-Brock, T. H. & Guinness, F. E. Early development and population dynamics in red deer II. Density-independent effects and cohort variation. J. Anim. Ecol. 56, 69–81 (1987).
Coulson, T. N., Albon, S. D., Slate, J. & Pemberton, J. M. Sex dependent responses to inbreeding and outbreeding in red deer calves. Evolution(in the press).
Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E. Parental investment and sex differences in juvenile mortality in birds and mammals. Nature 313, 131–133 (1985).
Kent, J. P. Birth sex ratios in sheep over nine lambing seasons: years 7–9 and the effects of ageing. Behav. Ecol. Sociobiol. 36, 101–104 (1995).
Byers, J. A. American Pronghorn: Social Adaptations and the Ghosts of Predators Past(Univ. of Chicago Press, Chicago, (1997).
Green, W. C. H. & Rothstein, A. Sex bias or equal opportunity—patterns of maternal investment in bison. Behav. Ecol. Sociobiol. 29, 373–384 (1991).
Lloyd, P. H. & Rasa, O. A. E. Status, reproductive success and fitness in Cape mountain zebra (Equus zebra zebra). Behav. Ecol. Sociobiol. 25, 411–420 (1989).
Schall, R. Estimation in generalized linear models with random effects. Biometrika 78, 719–727 (1991).
We thank Scottish Natural Heritage for permission to work on Rum; their local staff for help and support; A. Alexander, A. Curnow, S. Morris and many others for field data collection; N.Barton, P. Brotherton, A. Cockburn, D. Elston, M. Forchhammer, H. Kruuk, J. Lindström, A. Manning and P. Meir for comments and discussion; and the NERC for funding this work.
About this article
Cite this article
Kruuk, L., Clutton-Brock, T., Albon, S. et al. Population density affects sex ratio variation in red deer. Nature 399, 459–461 (1999). https://doi.org/10.1038/20917
Effects of population structure and density on calf sex ratio in red deer (Cervus elaphus)—implications for management
European Journal of Wildlife Research (2018)
Estimating red deer (Cervus elaphus) population size in the Southern Black Forest: the role of hunting in population control
European Journal of Wildlife Research (2018)
Sex ratio variation in an exploited population of common octopus: ontogenic shifts and spatio-temporal dynamics
Behavioral Ecology and Sociobiology (2016)
Behavioral Ecology and Sociobiology (2015)