Determinants of multiple paternity in a fluctuating population of ground squirrels

  • C. P. Wells
  • K. M. Tomalty
  • C. H. Floyd
  • M. B. McElreath
  • B. P. May
  • D. H. Van Vuren
Original Article

Abstract

Multiple paternity is common in vertebrates that produce several offspring in the same reproductive bout, but the rate often varies among and within populations. Three primary explanations for this variation have been advanced: null models based on encounter rate of mates, socioecological models dependent on the ability of males to monopolize females, and age- or condition-dependent models of female choice. We used 18 years of genetic and demographic data to examine the mating system and patterns of multiple paternity in a free-living population of golden-mantled ground squirrels (Callospermophilus lateralis). The mating system was polygynandrous, but opportunity for sexual selection was lower for females than for males. Annual reproductive success of males was low for yearlings and new immigrants and increased with breeding tenure in the population. Multiple paternity was evident in 62% of litters. In accordance with the socioecological model of male monopolization, rates of multiple paternity decreased with female spatial clustering, unless male–male competition, as indicated by male density, was also high. From Bateman gradients, we found no direct fitness benefit of multiple paternity for females. Though not statistically significant, multiple paternity appeared to decrease with maternal age and peri-oestrous mass, in possible support of the female choice model. Together, our results suggest that variation in the rate of multiple paternity in golden-mantled ground squirrels was determined by density and the active strategies of males and females.

Significance statement

Since the advent of molecular parentage assignment several decades ago, we have known that females of many species produce offspring with different fathers. Several theories have been developed for why females produce multiply-sired clutches or litters, but rarely are we able to identify the environmental, social, or individual conditions under which they do so. In this study, we genotyped offspring produced in one population of ground squirrels over 18 years, and found that the frequency of multiple paternity varied considerably from year to year, that density of female kin interacted with male density to influence multiple paternity, and that older and heavier females tended to be less likely to produce multiply-sired litters. These results demonstrate how dynamic population and individual characteristics of breeding males and females contribute to mating system variation in the same population over time.

Keywords

Multiple male mating Density Polygynandry Mating system variation Male reproductive success Callospermophilus lateralis 

References

  1. Andersson M, Iwasa Y (1996) Sexual selection. Trends Ecol Evol 11:53–58CrossRefPubMedGoogle Scholar
  2. Arct A, Drobniak SM, Cichon M (2015) Genetic similarity between mates predicts extrapair paternity—a meta-analysis of bird studies. Behav Ecol 26:959–968CrossRefGoogle Scholar
  3. Armitage KB (2014) Marmot biology: sociality, individual fitness, and population dynamics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  4. Arnqvist G, Rowe L (2005) Sexual Conflict. Princeton University Press, PrincetonCrossRefGoogle Scholar
  5. Atwell A, Wagner WE (2014) Female male choice plasticity is affected by the interaction between male density and female age in a field cricket. Anim Behav 98:177–183CrossRefGoogle Scholar
  6. Bartels MA, Thompson DP (1993) Spermophilus lateralis. Mamm Species 440:1–8CrossRefGoogle Scholar
  7. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368CrossRefPubMedGoogle Scholar
  8. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1–6, http://CRAN.R-project.org/package=lme4
  9. Bergeron P, Reale D, Humphries MM, Garant D (2011) Evidence of multiple paternity and mate selection for inbreeding avoidance in wild eastern chipmunks. J Evol Biol 24:1685–1694CrossRefPubMedGoogle Scholar
  10. Bergeron P, Montiglio P-O, Reale D, Humphries MM, Garant D (2012) Bateman gradients in a promiscuous mating system. Behav Ecol Sociobiol 66:1125–1130CrossRefGoogle Scholar
  11. Bronson MT (1979) Altitudinal variation in the life history of the golden-mantled ground squirrel (Spermophilus lateralis). Ecology 60:272–279CrossRefGoogle Scholar
  12. Bryja J, Patezenhauerová H, Albrecht T, Mošanský L, Stanko M, Stopka P (2008) Varying levels of female promiscuity in four Apodemus mice species. Behav Ecol Sociobiol 63:251–260CrossRefGoogle Scholar
  13. Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Curr Biol 16:R755–R765CrossRefPubMedGoogle Scholar
  14. Daly M (1978) The cost of mating. Am Nat 112:771–774CrossRefGoogle Scholar
  15. Dean MD, Ardlie KG, Nachman MW (2006) The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol Ecol 15:4141–4151CrossRefPubMedPubMedCentralGoogle Scholar
  16. Dobson FS, Risch TS, Murie JO (1999) Increasing returns in the life history of Columbian ground squirrels. J Anim Ecol 68:73–86CrossRefGoogle Scholar
  17. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, PrincetonGoogle Scholar
  18. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223CrossRefPubMedGoogle Scholar
  19. Ferron J (1985) Social behaviour of the golden-mantled ground squirrel (Spermophilus lateralis). Can J Zool 63:2529–2533CrossRefGoogle Scholar
  20. Gowaty PA, Bridges WC (1991) Behavioral, demographic, and environmental correlates of extrapair fertilizations in eastern bluebirds, Sialia sialis. Behav Ecol 2:339–350CrossRefGoogle Scholar
  21. Gray DA (1999) Intrinsic factors affecting female choice in house crickets: time cost, female age, nutritional condition, body size, and size-relative reproductive investment. J Insect Behav 12:691–700CrossRefGoogle Scholar
  22. Hanken J, Sherman PW (1981) Multiple paternity in Belding’s ground squirrel litters. Science 212:351–353CrossRefPubMedGoogle Scholar
  23. Hare JF, Todd G, Untereiner WA (2004) Multiple mating results in multiple paternity in Richardson’s ground squirrels, Spermophilus richardsonii. Can Field Nat 118:90–94CrossRefGoogle Scholar
  24. Hoogland JL (1998) Why do female Gunnison’s prairie dogs copulate with more than one male? Anim Behav 55:351–359CrossRefPubMedGoogle Scholar
  25. Hoogland JL (2013) Why do female prairie dogs copulate with more than one male?—insights from long-term research. J Mamm 94:731–744CrossRefGoogle Scholar
  26. Huchard E, Canale CI, Le Gros C, Perret M, Henry PY, Kappeler PM (2012) Convenience polyandry or convenience polygyny? Costly sex under female control in a promiscuous primate. Proc R Soc Lond B 279:1371–1379CrossRefGoogle Scholar
  27. Isvaran K, Clutton-Brock T (2007) Ecological correlates of extra-group paternity in mammals. Proc R Soc Lond B 274:219–224CrossRefGoogle Scholar
  28. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64CrossRefPubMedGoogle Scholar
  29. Jesmer BR, Van Vuren DH, Wilson JA, Kelt DA, Johnson ML (2011) Spatial organization in female golden-mantled ground squirrels. Am Midl Nat 165:162–168CrossRefGoogle Scholar
  30. Jones AG, Arguello JR, Arnold SJ (2002) Validation of Bateman’s principles: a genetic study of mating patterns and sexual selection in newts. Proc R Soc Lond B 269:2533–2539CrossRefGoogle Scholar
  31. Jones PH, Van Zant JL, Dobson FS (2012) Variation in reproductive success of male and female Columbian ground squirrels (Urocitellus columbianus). Can J Zool 90:736–743CrossRefGoogle Scholar
  32. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefPubMedGoogle Scholar
  33. Klemme I, Ylönen H, Eccard JA (2007) Reproductive success of male bank voles (Clethrionomys glareolus): the effect of operational sex ratio and body size. Behav Ecol Sociobiol 61:1911–1918CrossRefGoogle Scholar
  34. Kneip É, Van Vuren DH, Hostetler JA, Oli MK (2011) Influence of population density and climate on the demography of subalpine golden-mantled ground squirrels. J Mamm 92:367–377CrossRefGoogle Scholar
  35. Kodric-Brown A, Nicoletto PF (2001) Age and experience affect female choice in the guppy (Poecilia reticulata). Am Nat 157:316–323CrossRefPubMedGoogle Scholar
  36. Kokko H, Rankin DJ (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philos T Roy Soc B 361:319–334CrossRefGoogle Scholar
  37. Kokko H, Jennions MD, Brooks R (2006) Unifying and testing models of sexual selection. Annu Rev Ecol Evol S 37:43–66CrossRefGoogle Scholar
  38. Magnhagen C (1991) Predation risk as a cost of reproduction. Trends Ecol Evol 6:183–186CrossRefPubMedGoogle Scholar
  39. Martin JGA, Petelle MB, Blumstein DT (2014) Environmental, social, morphological, and behavioral constraints on opportunistic multiple paternity. Behav Ecol Sociobiol 68:1531–1538CrossRefGoogle Scholar
  40. Matějů J, Kratochvíl L (2013) Sexual size dimorphism in ground squirrels (Rodentia: Sciuridae: marmotini) does not correlate with body size and sociality. Front Zool 10:27CrossRefPubMedPubMedCentralGoogle Scholar
  41. McEachern MB, McElreath RL, Van Vuren DH, Eadie JM (2009) Another genetically promiscuous ‘polygynous’ mammal: mating system variation in Neotoma fuscipes. Anim Behav 77:449–455CrossRefGoogle Scholar
  42. McEachern MB, Van Vuren DH, Floyd CH, May B, Eadie JM (2011) Bottlenecks and rescue effects in a fluctuating population of golden-mantled ground squirrels (Spermophilus lateralis). Conserv Genet 12:285–296CrossRefGoogle Scholar
  43. McElreath R (2014) rethinking: Statistical Rethinking book package. R package version 1.391, https://github.com/rmcelreath/rethinking
  44. McFarlane SE, Lane JE, Taylor RW, Gorrell JC, Coltman DW, Humphries MM, Boutin S, McAdam AG (2011) The heritability of multiple male mating in a promiscuous mammal. Biol Lett 7:368–371CrossRefPubMedGoogle Scholar
  45. McKeever S (1964) The biology of the golden-mantled ground squirrel, Citellus lateralis. Ecol Monogr 34:383–401CrossRefGoogle Scholar
  46. Michener GR (1983) Kin identification, matriarchies, and the evolution of sociality in ground-dwelling sciurids. In: Eisenberg JF, Kleiman D (eds) Advances in the study of mammalian behavior. American Society of Mammalogists, Shippensburg, PA, pp 528–572Google Scholar
  47. Michener GR, McLean IG (1996) Reproductive behaviour and operational sex ratio in Richardson’s ground squirrels. Anim Behav 52:743–758CrossRefGoogle Scholar
  48. Morton ML, Sherman PW (1978) Effects of a spring snowstorm on behavior, reproduction, and survival of Belding’s ground squirrels. Can J Zool 56:2578–2590CrossRefGoogle Scholar
  49. Munroe K, Koprowski J (2011) Sociality, Bateman’s gradients, and the polygynandrous genetic mating system of round-tailed ground squirrels (Xerospermophilus tereticaudus). Behav Ecol Sociobiol 65:1811–1824CrossRefGoogle Scholar
  50. Murie JO (1995) Mating behavior of Columbian ground squirrels. I. Multiple mating by females and multiple paternity. Can J Zool 73:1819–1826CrossRefGoogle Scholar
  51. Naim DM, Telfer S, Sanderson S, Kemp SJ, Watts PC (2011) Prevalence of multiple mating by female common dormice, Muscardinus avellanarius. Conserv Genet 12:971–979CrossRefGoogle Scholar
  52. Phillips JA (1981) Growth and its relationship to the initial annual cycle of the golden-mantled ground squirrel, Spermophilus lateralis. Can J Zool 59:865–871CrossRefGoogle Scholar
  53. Raveh S, Heg D, Dobson FS, Coltman DW, Gorrell JC, Balmer A, Neuhaus P (2010) Mating order and reproductive success in male Columbian ground squirrels (Urocitellus columbianus). Behav Ecol 21:537–547CrossRefGoogle Scholar
  54. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/
  55. Schradin C, Lindholm AK, Johannesen J, Schoepf I, Yuen C-H, König B, Pillay N (2012) Social flexibility and social evolution in mammals: a case study of the African striped mouse (Rhabdomys pumilio). Mol Ecol 21:541–553CrossRefPubMedGoogle Scholar
  56. Schulte-Hostedde AI, Millar JS (2004) Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): implications for sperm competition and reproductive success. Behav Ecol Sociobiol 55:272–277CrossRefGoogle Scholar
  57. Schulte-Hostedde AI, Millar JS, Gibbs HL (2004) Sexual selection and mating patterns in a mammal with female-biased sexual size dimorphism. Behav Ecol 15:351–356CrossRefGoogle Scholar
  58. Schwagmeyer PL, Brown CH (1983) Factors affecting male-male competition in thirteen-lined ground squirrels. Behav Ecol Sociobiol 13:1–6CrossRefGoogle Scholar
  59. Schwagmeyer PL, Foltz DW (1990) Factors affecting the outcome of sperm competition in thirteen-lined ground squirrels. Anim Behav 39:156–162CrossRefGoogle Scholar
  60. Schwagmeyer PL, Wootner SJ (1986) Scramble competition polygyny in thirteen-lined ground squirrels: the relative contributions of overt conflict and competitive mate searching. Behav Ecol Sociobiol 19:359–364CrossRefGoogle Scholar
  61. Schwanz LE, Sherwin WB, Ognenovska K, Lacey EA (2016) Paternity and male mating strategies of a ground squirrel (Ictidomys parvidens) with an extended mating season. J Mamm 97:576–588CrossRefGoogle Scholar
  62. Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, PrincetonGoogle Scholar
  63. Sikes RS, Gannon WL (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mamm 92:235–253CrossRefGoogle Scholar
  64. Slatyer RA, Mautz BS, Backwell PRY, Jennions MD (2012) Estimating genetic benefits of polyandry from experimental studies: a meta-analysis. Biol Rev 87:1–33CrossRefPubMedGoogle Scholar
  65. Solomon NG, Keane B (2007) Reproductive strategies in female rodents. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological and evolutionary perspective. University of Chicago Press, Chicago, pp 42–56Google Scholar
  66. Sommaro LV, Chiappero MB, Vera NS, Coda JA, Priotto JW, Steinmann AR (2015) Multiple paternity in a wild population of the corn mouse: its potential significance for females. J Mamm 96:908–917CrossRefGoogle Scholar
  67. Stockley P, Searle JB, Macdonald DW, Jones CS (1993) Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proc R Soc Lond B 254:173–179CrossRefGoogle Scholar
  68. Streatfield CA, Mabry KE, Keane B, Crist TO, Solmon NG (2011) Intraspecific variability in the social and genetic mating systems of prairie voles Microtus ochrogaster. Anim Behav 82:1387–1398CrossRefGoogle Scholar
  69. Thonhauser KE, Thoβ M, Musolf K, Klaus T, Penn DJ (2014) Multiple paternity in wild house mice (Mus musculus musculus): effects on offspring genetic diversity and body mass. Ecol Evol 4:200–209CrossRefPubMedGoogle Scholar
  70. Waterman JM (1998) Mating tactics of male cape ground squirrels, Xerus inauris: consequences of year-round breeding. Anim Behav 56:459–466CrossRefPubMedGoogle Scholar
  71. Wells CP (2016) Reproductive ecology of female golden-mantled ground squirrels. Dissertation. University of California, DavisGoogle Scholar
  72. Wilgers DJ, Hebets EA (2012) Age-related female mating decisions are condition dependent in wolf spiders. Behav Ecol Sociobiol 66:29–38CrossRefGoogle Scholar
  73. Wolff JO, Macdonald DW (2004) Promiscuous females protect their offspring. Trends Ecol Evol 19:127–134CrossRefPubMedGoogle Scholar
  74. Zeh JA, Zeh DW (1997) The evolution of polyandry II: post-copulatory defenses against genetic incompatibility. Proc R Soc Lond B 264:69–75CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • C. P. Wells
    • 1
    • 2
  • K. M. Tomalty
    • 3
  • C. H. Floyd
    • 2
    • 4
  • M. B. McElreath
    • 5
  • B. P. May
    • 3
  • D. H. Van Vuren
    • 1
    • 2
  1. 1.Department of Wildlife, Fish, and Conservation BiologyUniversity of CaliforniaDavisUSA
  2. 2.Rocky Mountain Biological LaboratoryCrested ButteUSA
  3. 3.Department of Animal ScienceUniversity of CaliforniaDavisUSA
  4. 4.Department of BiologyUniversity of Wisconsin-Eau ClaireEau ClaireUSA
  5. 5.Department of PrimatologyMax Planck Institute for Evolutionary AnthropologyLeipzigGermany

Personalised recommendations