Behavioral Ecology and Sociobiology

, Volume 62, Issue 10, pp 1679–1687 | Cite as

Variation in offspring sex ratio among individual Weddell seal (Leptonychotes weddellii) females of different quality

  • Kelly M. ProffittEmail author
  • Robert A. Garrott
  • Jay J. Rotella
Original Paper


The Trivers–Willard model predicts that in polygynous species, superior-quality females will maximize their fitness by producing male offspring. Using a sample of 1,780 Weddell seal (Leptonychotes weddellii) pups recorded over 31 years, we investigated relationships between offspring sex ratio and maternal age, reproductive experience, an index of maternal lifetime reproductive output, and annual environmental variations. We found evidence that females with higher index of lifetime reproductive output were more likely to produce male than female offspring but found only weak evidence that large-scale environmental variations influenced sex ratios. Our results suggest that mothers manipulate offspring sex to maximize their own fitness, and inherent maternal quality may influence offspring sex. These findings support the Trivers–Willard sex-allocation model.


Sex ratio Trivers–Willard model Lifetime reproductive output Leptonychotes weddellii 



We thank all the personnel who participated in the long-term Weddell seal demography study since 1969. We also wish to thank Don B. Siniff for his insightful comments on an earlier version of this manuscript and three anonymous reviewers for constructive comments on this manuscript. Funding for this project was provided by a National Science Foundation grant, OPP-0225110, to R. A. Garrott, J. R. Rotella, and D. B. Siniff. The data were collected under various National Science Foundation grants to R. A. Garrott and J. R. Rotella at Montana State University, D. B. Siniff at the University of Minnesota, and J. W. Testa at the University of Alaska, Fairbanks.

Supplementary material

265_2008_596_MOESM1_ESM.doc (50 kb)
Table S1 Candidate a priori models explaining the effects of maternal and environmental characteristics on the odds of producing a male offspring. Covariates evaluated included an index of lifetime reproductive output (iLRO), maternal age (AGE), parity (PARITY), maternal identity (ID), summer sea-ice extent (SumExtent), winter sea-ice extent (WinExtent), southern oscillation (SOI), and year (YEAR) (DOC 51 kb).
265_2008_596_MOESM2_ESM.doc (24 kb)
Table S2 Histogram of index of maternal lifetime reproductive output for the 332 mothers included in analysis (DOC 24 kb
265_2008_596_MOESM3_ESM.doc (60 kb)
Table S3 Complete model-selection results for a priori models examining variation in Weddell seal offspring sex. Models are presented along with the AICc value, the ΔAICc value, and the Akaike model weight (w i ). Covariates evaluated include index of maternal lifetime reproductive output (iLRO), maternal age (AGE), sea-ice extent in the winter prior to conception (WinExtent), sea-ice extent in the summer of breeding and pregnancy (SumExtent), and the southern oscillation index (SOI) in the 3 months prior to conception. The random effects of maternal identity are represented by ID, and the random effects of year are represented by YEAR (DOC 61 kb).
265_2008_596_MOESM4_ESM.doc (30 kb)
Table S4 S4 Model-averaged coefficient estimates\(\left( {\widehat{\overline \beta }} \right)\), standard error\(\left( {{\text{SE}}\left( {\widehat{\overline \beta }} \right)} \right)\), and 95% confidence interval (CI) of each fixed covariate explaining variation in offspring sex. Predictor weights (w +(j)) are presented from the overall modeling exercise (DOC 30 KB).


  1. Anderson DR, Burnham KP (2002) Avoiding pitfalls when using information-theoretic methods. J Wildl Manage 66:912–918CrossRefGoogle Scholar
  2. Arnbom T, Fedak MA, Rothery P (1994) Offspring sex ratio in relation to female size in southern elephant seals, Mirounga leonina. Behav Ecol Sociobiol 35:373–378CrossRefGoogle Scholar
  3. Bartholomew GA (1970) A model for the evolution of pinniped polygnyny. Evolution 24:546–559CrossRefGoogle Scholar
  4. Blanchard P, Festa-Bianchet M, Gaillard JM, Jorgenson JT (2005) Maternal condition and offspring sex ratio in polygynous ungulates: a case study of bighorn sheep. Behav Ecol 16:274–279CrossRefGoogle Scholar
  5. Bradshaw CJ, Harcourt RG, Davis LS (2003) Male-biased sex ratios in New Zealand fur seal pups relative to environmental variation. Behav Ecol Sociobiol 53:297–307Google Scholar
  6. Bureau of Meteorology, Australian Government (2005) Southern Oscillation Index Archives, 1976 to present.
  7. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach. 2nd edition. Springer Science and Business Media, Inc., New YorkGoogle Scholar
  8. Burns JM, Trumble SJ, Castellini MA, Testa JW (1998) The diet of Weddell seals in McMurdo Sound, Antarctica as determined from scat collections and stable isotope analysis. Polar Biol 19:272–282CrossRefGoogle Scholar
  9. Byholm P, Ranta E, Kaitala V, Linden H, Saurola P, Wikman M (2002) Resource availability and goshawk offspring sex ratio variation: a large-scale ecological phenomenon. J Anim Ecol 71:994–1001CrossRefGoogle Scholar
  10. Cameron EZ (2004) Facultative adjustment of mammalian sex ratios in support of the Trivers–Willard hypothesis: evidence for a mechanism. Proc R Soc Lond B 271:1723–1728CrossRefGoogle Scholar
  11. Cameron MF, Siniff DB (2004) Age-specific survival, abundance, and immigration rates of a Weddell seal (Leptonychotes weddellii) population in McMurdo Sound, Antarctica. Can J Zool 82:601–615CrossRefGoogle Scholar
  12. Castellini MA, Davis RW, Kooyman GL (1992) Annual cycles of diving behavior and ecology of the Weddell seal. Bull Scripps Inst Oceanogr 28:1–54Google Scholar
  13. Charlesworth B, Leon JA (1976) The relation of reproductive effort to age. Am Nat 110:449–459CrossRefGoogle Scholar
  14. Charnov EL (1982) The theory of sex allocation. Princeton University Press, New Jersey, USAGoogle Scholar
  15. Clutton-Brock TH, Iason GR (1986) Sex ratio variation in mammals. Q Rev Biol 61:339–374PubMedCrossRefGoogle Scholar
  16. Clutton-Brock TH, Albon SD, Guinness FE (1984) Maternal dominance, breeding success and birth sex ratios in red deer. Nature 308:358–360CrossRefGoogle Scholar
  17. Clutton-Brock TH, Albon SD, Guinness FE (1986) Great expectations: dominance, breeding success and offspring sex ratios in red deer. Anim Behav 34:460–471CrossRefGoogle Scholar
  18. Comiso JC (1999, updated 2005) Bootstrap sea ice concentrations for NIMBUS-7 SMMR and DMSP SSM/I, 1978–2003. National Snow and Ice Data Center, Boulder, CO, USAGoogle Scholar
  19. Cote S, Festa-Bianchet M (2001) Offspring sex ration in relation to maternal age and social rank in mountain goats (Oreamnos americanus). Behav Ecol Sociobiol 49:260–265CrossRefGoogle Scholar
  20. Fabiani A, Galimberti F, Sanvito S, Hoelzel AR (2004) Extreme polygyny among southern elephant seals on Sea Lion Island, Falkland Islands. Behav Ecol 15:961–969CrossRefGoogle Scholar
  21. Festa-Bianchet M (1996) Offspring sex ratio studies of mammals: does publication depend upon the quality of the research or the direction of the results? Ecoscience 3:42–44Google Scholar
  22. Folmer V, Soares JC, Gabriel D, Rocha JB (2003) A high fat diet inhibits delta-aminolevulinate dehydratase and increases lipid peroxidation in mice. J Nutr 133:2165–2170PubMedGoogle Scholar
  23. Frank SA (1990) Sex allocation theory for birds and mammals. Ann Rev Ecolog Syst 21:13–55CrossRefGoogle Scholar
  24. Gelatt T, Davis C, Cameron MF, Siniff DB, Strobeck C (2000) The old and new: integrating population ecology and population genetics of Weddell seals. In: Davison W, Howard-Williams C, Broady P (eds) Antarctic ecosystems: models for wider ecological understanding. Caxton, Christchurch, pp 63–70Google Scholar
  25. Gosling LM (1986) Selective abortion of entire litters in the Coypu: adaptive control of offspring production in relation to quality and sex. Am Nat 127:772–795CrossRefGoogle Scholar
  26. Green WCH, Rothstein A (1991) Sex bias or equal opportunity? Patterns of maternal investment in bison. Behav Ecol Sociobiol 29:373–384CrossRefGoogle Scholar
  27. Gutierrez-Adan A, Granados J, Pintado B, de la Fuente J (2001) Influence of glucose on the sex ratio of bovine IM/IVF embryos cultured in vitro. Reprod Fertil Dev 13:361–365PubMedCrossRefGoogle Scholar
  28. Hadley GL (2006) Recruitment probabilities and reproductive costs for Weddell seals in Erebus Bay, Antartica. Ph.D. Montana State University, Bozeman, MTGoogle Scholar
  29. Hadley GL, Rotella J, Nichols JD, Garrott RA (2006) Variation in probability of first reproduction of Weddell seals. J Anim Ecol 75:1058–1070PubMedCrossRefGoogle Scholar
  30. Hadley GL, Rotella J, Garrott RA (2007) Influence of maternal characteristics and oceanographic conditions on survival and recruitment probabilities of Weddell seals. Oikos 116:601–613CrossRefGoogle Scholar
  31. Hewison AJM, Gaillard J-M (1999) Successful sons or advantaged daughters? The Trivers–Willard model and sex-biased maternal investment in ungulates. Trends Ecol Evol 14:229–234PubMedCrossRefGoogle Scholar
  32. Hill SE (1987) Reproductive ecology of Weddell seals (Leptonychotes weddellii) in McMurdo Sound, Antarctica. PhD thesis. University of Minnesota, St. Paul, MN, pp 106Google Scholar
  33. Hogg JT, Hass CC, Jenni DA (1992) Sex-biased maternal expenditure in Rocky Mountain bighorn sheep. Behav Ecol Sociobiol 31:243–251CrossRefGoogle Scholar
  34. Hosmer DW, Hosmer T, le Cessie S, Lemeshow S (1997) A comparison of goodness-of-fit tests for the logistic regression model. Stat Med 16:965–980PubMedCrossRefGoogle Scholar
  35. Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K, Johnson CA (2001) Climate change 2001: the scientific basis; contribution of the Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, p 881Google Scholar
  36. Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108PubMedCrossRefGoogle Scholar
  37. Komdeur J, Pen I (2002) Adaptive sex allocation in birds: the complexities of linking theory and practice. Philos Trans R Soc Lond B 357:373–380CrossRefGoogle Scholar
  38. Krackow S (1995) Potential mechanisms for sex ratio adjustment in mammals and birds. Biol rev Camb Philos Soc 70:225–241PubMedCrossRefGoogle Scholar
  39. Krüger O, Radford AN, Anderson C, Liversidge R (2005) Successful sons or disadvantaged daughters: sex-ratio variation in springbok. Proc R Soc Lond B 272:375–381CrossRefGoogle Scholar
  40. Kruuk L, Clutton-Brock TH, Albon SD, Pemberton J, Guinness FE (1999) Population density affects sex ratio variation in red deer. Nature 399:459–461PubMedCrossRefGoogle Scholar
  41. Kwok R, Comiso JC (2002) Southern ocean climate and sea ice anomalies associated with the southern oscillation. J Climate 15:487–501CrossRefGoogle Scholar
  42. Le Boeuf BJ, Reiter J (1988) Lifetime reproductive success in northern elephant seals. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 344–362Google Scholar
  43. Le Boeuf BJ, Condit R, Reiter J (1989) Parental investment and the secondary sex ratio in northern elephant seals. Behav Ecol Sociobiol 25:109–117CrossRefGoogle Scholar
  44. le Cessie S, van Houwelingen JC (1991) A goodness-of-fit test for binary regression models, based on smoothing methods. Biometrics 47:1267–1282CrossRefGoogle Scholar
  45. Leimar O (1996) Life-history analysis of the Trivers and Willard sex-ratio problem. Behav Ecol 7:316–325CrossRefGoogle Scholar
  46. Lukacs P, Thompson W, Kendall W, Gould W, Doherty P, Burnham K, Anderson D (2007) Concerns regarding a call for pluralism of information theory and hypothesis testing. J Appl Ecol 44:456–460CrossRefGoogle Scholar
  47. Mysterud A, Yoccoz NG, Stenseth NC, Langvatn R (2001) Effects of age, sex and density on body weight of Norwegian red deer: evidence of density-dependent senescence. Proc R Soc B 268:911–919Google Scholar
  48. National Ice Center (2005) Sea ice gridded climatology (SIGC) coverage and extent statistics, 1973–1994. (
  49. Neter J, Kutner MH, Nachtsheim CJ, Wasserman W (1996) Applied linear statistical models, 4th edn. McGraw-Hill, BostonGoogle Scholar
  50. Nicol S, Pauly T, Bindoff NL, Wright S, Thiele D, Hosie GW, Strutton PG, Woehler E (2000) Ocean circulation off east Antarctica affects ecosystem structure and sea-ice extent. Nature 406:504–507PubMedCrossRefGoogle Scholar
  51. Nygen T, Kojola I (1997) Twinning and fetal sex ratio in moose: effects of maternal age and mass. Can J Zool 75:1945–1948Google Scholar
  52. Palmer AR (2000) Quasireplication and the contract of error: lessons from sex ratios, heritabilities and fluctuating asymmetry. Ann Rev Ecolog Syst 31:441–480CrossRefGoogle Scholar
  53. Pianka ER, Parker WS (1975) Age-specific reproductive tactics. Am Nat 109:453–464CrossRefGoogle Scholar
  54. Post E, Forchhammer MC, Stenseth NC, Langvatn R (1999) Extrinsic modification of vertebrate sex ratios by climatic variation. Am Nat 154:194–204Google Scholar
  55. Proffitt KM, Garrott RA, Rotella J, Siniff DB, Testa JW (2007a) Exploring linkages between abiotic oceanographic processes and a top-trophic predator in an Antarctic ecosystem. Ecosystems 10:120–127CrossRefGoogle Scholar
  56. Proffitt KM, Garrott RA, Rotella J (2007b) Environmental and senescent related variations in Weddell seal body mass: implications for age-specific reproductive performance. Oikos 116:1683–1690CrossRefGoogle Scholar
  57. Proffitt KM, Garrott RA, Rotella J (2008) Long-term evaluation of body mass at weaning and post-weaning survival rates of Weddell seals in Erebus Bay, Antarctica. Mar Mamm Sci in pressGoogle Scholar
  58. Rosenfeld CS, Grimm KM, Livingston KA, Lamberson WE, Roberts RM (2003) Striking variation in the sex ratio of pups born to mice according to whether maternal diet is high in fat or carbohydrate. Proc Natl Acad Sci U S A 100:4628–4632PubMedCrossRefGoogle Scholar
  59. SAS Institute (2000) SAS/STAT user’s guide, Version 8. SAS Institute, Cary, North CarolinaGoogle Scholar
  60. Schwanz LE, Bragg JG, Charnov EL (2006) Material condition and faculative sex ratios in populations with overlapping generations. Am Nat 168:521–530Google Scholar
  61. Siniff DB, Demaster DP, Hofman RJ, Eberhardt LL (1977) An analysis of the dynamics of a Weddell seal population. Ecol Monogr 47:319–335CrossRefGoogle Scholar
  62. Testa JW, Siniff DB (1987) Population dynamics of Weddell seals (Leptonychotes weddellii) in McMurdo Sound, Antarctica. Ecol Monogr 57:149–165CrossRefGoogle Scholar
  63. Thomas DC, Barry SJ, Kilaan HP (1989) Fetal sex ratio in caribou: maternal age and condition effects. J Wildl Manage 53:885–890Google Scholar
  64. Trivers R, Willard D (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92PubMedCrossRefGoogle Scholar
  65. Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395PubMedCrossRefGoogle Scholar
  66. Waterhouse EJ (2001) Ross Sea region: a state of the environment report for the Ross Sea region of Antarctica. New Zealand Antarctic Institute, ChristchurchGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Kelly M. Proffitt
    • 1
    Email author
  • Robert A. Garrott
    • 1
  • Jay J. Rotella
    • 1
  1. 1.Department of EcologyMontana State UniversityBozemanUSA

Personalised recommendations