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

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Abstract

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.

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References

  • Adams JR (2006) A multi-faceted molecular approach to red wolf (Canis rufus) conservation and management. PhD dissertation, University of Idaho

  • 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 82:826–835

    Article  PubMed  Google Scholar 

  • Bonduriansky R, Maklakov A, Zajitschek F, Brooks R (2008) Sexual selection, sexual conflict and the evolution of ageing and life span. Funct Ecol 22:443–453

    Article  Google Scholar 

  • Bourke AFG (2007) Kin selection and the evolutionary theory of aging. Annu Rev Ecol Syst 38:103–128

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • 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 26:1352–1360

    Article  Google Scholar 

  • Clutton-Brock TH, Isvaran K (2007) Sex differences in ageing in natural populations of vertebrates. Proc R Soc Lond B 274:3097–3104

    Article  CAS  Google Scholar 

  • Crabtree RL (1988) Sociodemography of an unexploited coyote population. PhD dissertation, University of Idaho

  • 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. 337–350

    Chapter  Google Scholar 

  • Finch CE (1994) Longevity, senescence, and the genome. University of Chicago Press, Chicago

    Google Scholar 

  • Gese EM, Roberts BM, Knowlton FF (2016) Nutritional effects on reproductive performance of captive adult female coyotes (Canis latrans). Anim Reprod Sci 165:69–75

    Article  PubMed  Google Scholar 

  • Graves BM (2007) Sexual selection effects on the evolution of senescence. Evol Ecol 21:663–668

    Article  Google Scholar 

  • Graves BM, Strand M, Lindsay AR (2006) A reassessment of sexual dimorphism in human senescence: theory, evidence, and causation. Am J Hum Biol 18:161–168

    Article  PubMed  Google Scholar 

  • Green JS, Knowlton FF, Pitt WC (2002) Reproduction in captive wild-caught coyotes (Canis latrans). J Mammal 83:501–506

    Article  Google Scholar 

  • Hammers M, Richardson DS, Burke T, Komdeur J (2012) Age-dependent terminal declines in reproductive output in a wild bird. PLoS One 7:e40413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosken DJ, Stockley P, Tregenza T, Wedell N (2009) Monogamy and the battle of the sexes. Annu Rev Entomol 54:361–378

    Article  CAS  PubMed  Google Scholar 

  • 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):273–287

    Article  Google Scholar 

  • Lee RD (2003) Rethinking the evolutionary theory of aging: transfers, not births, shape senescence in social species. P Natl Acad Sci USA 100:9637–9642

    Article  CAS  Google Scholar 

  • MacNulty DR, Smith DW, Mech LD, Eberly LE (2009a) Body size and predatory performance in wolves: is bigger better? J Anim Ecol 78:532–539

    Article  PubMed  Google Scholar 

  • MacNulty DR, Smith DW, Vucetich JA, Mech LD, Stahler DR, Packer C (2009b) Predatory senescence in ageing wolves. Ecol Lett 12:1347–1356

    Article  PubMed  Google Scholar 

  • 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 8:324–330

    Article  CAS  PubMed  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  CAS  PubMed  Google Scholar 

  • 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, NM

  • Medawar PB (1952) An unsolved problem of biology. H.K. Lewis and Co, London

    Google Scholar 

  • Mills KJ, Brent R, Dennis L (2008) Direct estimation of early survival and movements in eastern wolf pups. J Wildl Manag 72(4):949–954

  • Nussey DH, Coulson T, Festa-Bianchet M, Gaillard JM (2008) Measuring senescence in wild animal populations: towards a longitudinal approach. Funct Ecol 22:393–406

    Article  Google Scholar 

  • 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. 35–65

    Google Scholar 

  • 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. 272–288

    Google Scholar 

  • Promislow DEL (1992) Costs of sexual selection in natural populations of mammals. Proc R Soc Lond B 247:203–210

    Article  Google Scholar 

  • Promislow DEL, Montgomerie R, Martin TE (1992) Mortality costs of sexual dimorphism in birds. Proc R Soc Lond B 250:143–150

    Article  Google Scholar 

  • Rabon DR (2014) Effects of age and experience on reproductive performance of captive red wolves (Canis rufus). Can J Zool 92:251–258

    Article  Google Scholar 

  • R Core Team (2014). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/

  • 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 79:851–862

    PubMed  Google Scholar 

  • Sacks BN (2005) Reproduction and body condition of California coyotes (Canis latrans). J Mammal 86:1036–1041

    Article  Google Scholar 

  • Sharp SP, Clutton-Brock TH (2010) Reproductive senescence in a cooperatively breeding mammal. J Anim Ecol 79:176–183

    Article  PubMed  Google Scholar 

  • 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 278:1381–1389

    Article  Google Scholar 

  • 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 22:199–205

    Article  Google Scholar 

  • 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 23:1186–1194

    Article  Google Scholar 

  • 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 82:222–234

    Article  PubMed  Google Scholar 

  • Torres R, Drummond H, Velando A (2011) Parental age and lifespan influence offspring recruitment: a long-term study in a seabird. PLoS One 6:e27245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Aldine, Chicago, pp. 136–179

    Google Scholar 

  • USFWS (1984) Red wolf recovery plan. U.S. Fish and Wildlife Service, Atlanta, GA

    Google Scholar 

  • 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 273:1443–1448

    Article  Google Scholar 

  • 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:e1501714

    Article  Google Scholar 

  • 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 17:252–274

    Article  PubMed  Google Scholar 

  • Williams GC (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11:398–411

    Article  Google Scholar 

  • Windberg LA (1995) Demography of a high-density coyote population. Can J Zool 73:942–954

    Article  Google Scholar 

  • Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J Roy Stat Soc B 73:3–36

    Article  Google Scholar 

Download references

Acknowledgments

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.

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Authors and Affiliations

  1. Biology Department, Westmont College, 955 La Paz Rd, Santa Barbara, CA, 93108, USA

    Amanda M. Sparkman

  2. School of Journalism, University of Montana, 32 Campus Drive, Missoula, MT, 59812, USA

    Matthew Blois

  3. Department of Fish and Wildlife Sciences, University of Idaho, Moscow, ID, 83844-1136, USA

    Jennifer Adams & Lisette Waits

  4. Department of Ecosystem Science and Management, Pennsylvania State University, University Park, PA, 16802, USA

    David A.W. Miller

  5. Department of Biology, Trent University, K9J 7B8, Peterborough, ON, Canada

    Dennis L. Murray

Authors
  1. Amanda M. Sparkman
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  2. Matthew Blois
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  3. Jennifer Adams
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  4. Lisette Waits
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  5. David A.W. Miller
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  6. Dennis L. Murray
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Corresponding author

Correspondence to Amanda M. Sparkman.

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Funding

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).

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Not applicable.

Additional information

Communicated by C. Soulsbury

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Sparkman, A.M., Blois, M., Adams, J. et al. Evidence for sex-specific reproductive senescence in monogamous cooperatively breeding red wolves. Behav Ecol Sociobiol 71, 6 (2017). https://doi.org/10.1007/s00265-016-2241-9

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  • DOI: https://doi.org/10.1007/s00265-016-2241-9

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