Evidence for sex-specific reproductive senescence in monogamous cooperatively breeding red wolves

  • Amanda M. Sparkman
  • Matthew Blois
  • Jennifer Adams
  • Lisette Waits
  • David A.W. Miller
  • Dennis L. Murray
Original Article


Sex-specific senescence has been construed as a function of mating system and differential investment in parental care, with males exhibiting low parental investment predicted to have more rapid senescence due to costly reproductive behavior. In monogamous mating systems, however, where parental investment may be more evenly distributed, rates of senescence are predicted to be more equivalent between the sexes than in polygynous mating systems. While many polygynous species do appear to support this pattern, evidence from monogamous species, particularly mammals, is scarce. Wolves are an excellent system with which to test this hypothesis, as they exhibit both monogamy and cooperative breeding, where parental investment is distributed across both breeders and non-breeders of both sexes. We examined patterns of age-specific reproduction in red wolves and red wolf-coyote hybrids. We found no evidence of decline in pup production with age in male wolves; among females, the production appeared better explained by hybrid status and age at first reproduction than age per se. Remarkably, however, there was strong evidence of sex differences in pup recruitment, with males, but not females, showing a steep decline in recruitment with age. Combined with previous work on aging in captive wolves, our findings contribute not only to the current understanding of the relationship between mating system and senescence but also to the plasticity of aging and the dynamics of female mate choice in the wild.

Significance statement

In this study, we test for signs of reproductive aging in red wolves using a 20-year dataset documenting age-specific reproduction in the wild. We find evidence that reproductive aging in males is evident for number of pups recruited, though not for number of pups born; we find no evidence for reproductive aging at either stage in wild female wolves. This sex difference stands in contrast to the general prediction that patterns of aging would be more monomorphic among monogamous species. Furthermore, this is especially of interest given that red wolves are cooperative breeders, with costs of reproduction spread across family groups. In general, this study constitutes a valuable contribution to an emerging literature geared at understanding patterns of aging in the context of diverse social and ecological variables.


Reproductive senescence Sexual selection Monogamy Cooperative breeding Canis rufus 



The Red Wolf Recovery Program is conducted by the US Fish and Wildlife Service (USFWS), and we are grateful to service personnel for their diligent efforts in the field and access to the data. The fieldwork was funded by the USFWS. The Natural Sciences and Engineering Research Council (Canada) supported data analysis and write-up. We also thank anonymous reviewers for their valuable comments on the manuscript. The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the USFWS.

Compliance with ethical standards


This study was funded by the US Fish and Wildlife Service

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The fieldwork on red wolves was conducted solely by the US Fish and Wildlife Service, and all work and procedures conformed to national standards for wildlife handling (Gannon et al. 2011).

Informed consent

Not applicable.

Supplementary material

265_2016_2241_MOESM1_ESM.docx (16 kb)
Table S1 (DOCX 15 kb)


  1. Adams JR (2006) A multi-faceted molecular approach to red wolf (Canis rufus) conservation and management. PhD dissertation, University of IdahoGoogle Scholar
  2. Auld JR, Perrins CM, Charmantier A (2013) Who wears the pants in a mute swan pair? Deciphering the effects of male and female age and identity on breeding success. J Anim Ecol 82:826–835CrossRefPubMedGoogle Scholar
  3. Bonduriansky R, Maklakov A, Zajitschek F, Brooks R (2008) Sexual selection, sexual conflict and the evolution of ageing and life span. Funct Ecol 22:443–453CrossRefGoogle Scholar
  4. Bourke AFG (2007) Kin selection and the evolutionary theory of aging. Annu Rev Ecol Syst 38:103–128CrossRefGoogle Scholar
  5. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  6. Cassidy KA, MacNulty DR, Stahler DR, Smith DW, Mech LD (2015) Group composition effects on aggressive interpack interactions of gray wolves in Yellowstone National Park. Behav Ecol 26:1352–1360CrossRefGoogle Scholar
  7. Clutton-Brock TH, Isvaran K (2007) Sex differences in ageing in natural populations of vertebrates. Proc R Soc Lond B 274:3097–3104CrossRefGoogle Scholar
  8. Crabtree RL (1988) Sociodemography of an unexploited coyote population. PhD dissertation, University of IdahoGoogle Scholar
  9. Creel S, Mills MGL, McNutt JW (2004) African wild dogs: demography and population dynamics of African wild dogs in three critical populations. In: MacDonald DW, Sillero-Zubiri C (eds) The biology and conservation of wild canids. Oxford University Press, Oxford, pp. 337–350CrossRefGoogle Scholar
  10. Finch CE (1994) Longevity, senescence, and the genome. University of Chicago Press, ChicagoGoogle Scholar
  11. Gese EM, Roberts BM, Knowlton FF (2016) Nutritional effects on reproductive performance of captive adult female coyotes (Canis latrans). Anim Reprod Sci 165:69–75CrossRefPubMedGoogle Scholar
  12. Graves BM (2007) Sexual selection effects on the evolution of senescence. Evol Ecol 21:663–668CrossRefGoogle Scholar
  13. Graves BM, Strand M, Lindsay AR (2006) A reassessment of sexual dimorphism in human senescence: theory, evidence, and causation. Am J Hum Biol 18:161–168CrossRefPubMedGoogle Scholar
  14. Green JS, Knowlton FF, Pitt WC (2002) Reproduction in captive wild-caught coyotes (Canis latrans). J Mammal 83:501–506CrossRefGoogle Scholar
  15. Hammers M, Richardson DS, Burke T, Komdeur J (2012) Age-dependent terminal declines in reproductive output in a wild bird. PLoS One 7:e40413CrossRefPubMedPubMedCentralGoogle Scholar
  16. Hosken DJ, Stockley P, Tregenza T, Wedell N (2009) Monogamy and the battle of the sexes. Annu Rev Entomol 54:361–378CrossRefPubMedGoogle Scholar
  17. Kyle CJ, Johnson AR, Patterson BR, Wilson PJ, Shami K, Grewal SK, White BN (2006) Genetic nature of eastern wolves: past, present and future. Cons Gen 7(2):273–287CrossRefGoogle Scholar
  18. Lee RD (2003) Rethinking the evolutionary theory of aging: transfers, not births, shape senescence in social species. P Natl Acad Sci USA 100:9637–9642CrossRefGoogle Scholar
  19. MacNulty DR, Smith DW, Mech LD, Eberly LE (2009a) Body size and predatory performance in wolves: is bigger better? J Anim Ecol 78:532–539CrossRefPubMedGoogle Scholar
  20. MacNulty DR, Smith DW, Vucetich JA, Mech LD, Stahler DR, Packer C (2009b) Predatory senescence in ageing wolves. Ecol Lett 12:1347–1356CrossRefPubMedGoogle Scholar
  21. Maklakov AA, Hall MD, Simpson SJ, Dessmann J, Clissold FJ, Zajitschek F, Lailvaux SP, Raubenheimer D, Bonduriansky R, Brooks RC (2009) Sex differences in nutrient-dependent reproductive ageing. Aging Cell 8:324–330CrossRefPubMedGoogle Scholar
  22. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655CrossRefPubMedGoogle Scholar
  23. McCarley H, Carley CJ (1979) Recent changes in distribution and status of wild red wolves (Canis rufus). Endangered Species Report 4. U.S. Fish and Wildlife Service, Albuquerque, NMGoogle Scholar
  24. Medawar PB (1952) An unsolved problem of biology. H.K. Lewis and Co, LondonGoogle Scholar
  25. Mills KJ, Brent R, Dennis L (2008) Direct estimation of early survival and movements in eastern wolf pups. J Wildl Manag 72(4):949–954Google Scholar
  26. Nussey DH, Coulson T, Festa-Bianchet M, Gaillard JM (2008) Measuring senescence in wild animal populations: towards a longitudinal approach. Funct Ecol 22:393–406CrossRefGoogle Scholar
  27. Packard JM (2003) Wolf behavior: reproductive, social and intelligent. In: Mech LD, Boitani L (eds) Wolves: behavior, ecology and conservation. University of Chicago Press, Chicago, pp. 35–65Google Scholar
  28. Phillips MK, Henry VG, Kelly BT (2003) Restoration of the red wolf. In: Mech LD, Boitani L (eds) Wolves: behavior, ecology and conservation. University of Chicago Press, Chicago, pp. 272–288Google Scholar
  29. Promislow DEL (1992) Costs of sexual selection in natural populations of mammals. Proc R Soc Lond B 247:203–210CrossRefGoogle Scholar
  30. Promislow DEL, Montgomerie R, Martin TE (1992) Mortality costs of sexual dimorphism in birds. Proc R Soc Lond B 250:143–150CrossRefGoogle Scholar
  31. Rabon DR (2014) Effects of age and experience on reproductive performance of captive red wolves (Canis rufus). Can J Zool 92:251–258CrossRefGoogle Scholar
  32. R Core Team (2014). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria,
  33. Reid JM, Bignal EM, Bignal S, McCracken DI, Bogdanova MI, Monaghan P (2010) Parent age, lifespan and offspring survival: structured variation in life history in a wild population. J Anim Ecol 79:851–862PubMedGoogle Scholar
  34. Sacks BN (2005) Reproduction and body condition of California coyotes (Canis latrans). J Mammal 86:1036–1041CrossRefGoogle Scholar
  35. Sharp SP, Clutton-Brock TH (2010) Reproductive senescence in a cooperatively breeding mammal. J Anim Ecol 79:176–183CrossRefPubMedGoogle Scholar
  36. Sparkman AM, Adams J, Beyer A, Steury TD, Waits L, Murray DL (2011a) Helper effects on pup lifetime fitness in the cooperatively breeding red wolf (Canis rufus). Proc R Soc Lond B 278:1381–1389CrossRefGoogle Scholar
  37. Sparkman AM, Adams JR, Steury TD, Waits LP, Murray DL (2011b) Direct fitness benefits of delayed dispersal in the cooperatively breeding red wolf (Canis rufus). Behav Ecol 22:199–205CrossRefGoogle Scholar
  38. Sparkman AM, Adams JR, Steury TD, Waits LP, Murray DL (2012) Pack social dynamics and inbreeding avoidance in the cooperatively breeding red wolf. Behav Ecol 23:1186–1194CrossRefGoogle Scholar
  39. Stahler DR, MacNulty DR, Wayne RK, vonHoldt B, Smith DW (2013) The adaptive value of morphological, behavioural and life-history traits in reproductive female wolves. J Anim Ecol 82:222–234CrossRefPubMedGoogle Scholar
  40. Torres R, Drummond H, Velando A (2011) Parental age and lifespan influence offspring recruitment: a long-term study in a seabird. PLoS One 6:e27245CrossRefPubMedPubMedCentralGoogle Scholar
  41. Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Aldine, Chicago, pp. 136–179Google Scholar
  42. USFWS (1984) Red wolf recovery plan. U.S. Fish and Wildlife Service, Atlanta, GAGoogle Scholar
  43. Velando A, Drummond H, Torres R (2006) Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis. Proc R Soc Lond B 273:1443–1448CrossRefGoogle Scholar
  44. vonHoldt BM, Cahill JA, Fan Z, Gronau I, Robinson J, Pollinger JP, Shapiro B, Wall J, Wayne RK (2016) Whole-genome sequence analysis shows that two endemic species of North American wolf are admixtures of the coyote and gray wolf. Sci Adv 2:e1501714CrossRefGoogle Scholar
  45. vonHoldt BM, Stahler DR, Smith DW, Earl DA, Pollinger JP, Wayne RK (2008) The genealogy and genetic viability of reintroduced Yellowstone grey wolves. Mol Ecol 17:252–274CrossRefPubMedGoogle Scholar
  46. Williams GC (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11:398–411CrossRefGoogle Scholar
  47. Windberg LA (1995) Demography of a high-density coyote population. Can J Zool 73:942–954CrossRefGoogle Scholar
  48. Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J Roy Stat Soc B 73:3–36CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Amanda M. Sparkman
    • 1
  • Matthew Blois
    • 2
  • Jennifer Adams
    • 3
  • Lisette Waits
    • 3
  • David A.W. Miller
    • 4
  • Dennis L. Murray
    • 5
  1. 1.Biology DepartmentWestmont CollegeSanta BarbaraUSA
  2. 2.School of JournalismUniversity of MontanaMissoulaUSA
  3. 3.Department of Fish and Wildlife SciencesUniversity of IdahoMoscowUSA
  4. 4.Department of Ecosystem Science and ManagementPennsylvania State UniversityUniversity ParkUSA
  5. 5.Department of BiologyTrent UniversityPeterboroughCanada

Personalised recommendations