Abstract
Trivers and Willard proposed that female mammals should adjust their investment in male versus female offspring relative to their ability to produce high-quality offspring. We tested whether litter size–sex ratio trade-offs predicted by Adaptive Sex Allocation (ASA) theory occur among Richardson’s ground squirrel (Urocitellus richardsonii) dams over 10 distinct breeding years in a population where individuals experienced variability in food availability and habitat disruption. Litters of primiparous dams became increasingly female-biased with increasing litter size, but that trend waned among second litters born to dams, and reversed among third litters, with larger litters becoming more male-biased, suggesting that ASA is a product of interacting selection pressures. Trade-offs were not associated with habitat disruption, the availability of supplementary food, or dam age. An association between habitat disruption and male-biased sex ratios, the prevalence of litter size–sex ratio trade-offs and placental scar counts exceeding the number of juveniles at weaning in our population, but not in a geographically distinct population of conspecifics exposed to different environmental conditions reveal that the expression of ASA varies among populations and among years within populations, illustrating the conditional nature of ASA.
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Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72(5):1177–1196. https://doi.org/10.1016/j.anbehav.2006.05.001
Austad SN, Sunquist ME (1986) Sex-ratio manipulation in the common opossum. Nature 324(6092):58–60. https://doi.org/10.1038/324058a0
Bánszegi O, Szenczi P, Dombay K, Bilkó A, Altbäcker V (2012) Anogenital distance as a predictor of attractiveness, litter size and sex ratio of rabbit does. Physiol Behav 105(5):1226–1230. https://doi.org/10.1016/j.physbeh.2012.01.002
Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368. https://doi.org/10.1038/hdy.1948.21
Berube CH, Festa-Bianchet M, Jorenson JT (1996) Reproductive costs of sons and daughters in Rocky Mountain bighorn sheep. Behav Ecol 1(1):60–68. https://doi.org/10.1093/beheco/7.1.60
Boonstra R, Hik D, Singleton GR, Tinnikov A (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecolog Monographs 68(3):371–394. https://doi.org/10.1890/0012-9615(1998)068%5b0371:tiopis%5d2.0.co;2
Caley MJ, Nudds TD (1987) Sex-ratio adjustment in Odocoileus: does local resource competition play a role? Am Nat 129(3):452–457. https://doi.org/10.1086/284649
Cameron EL (2004) Facultative adjustment of mammalian sex ratios in support of the Trivers-Willard hypothesis: evidence for a mechanism. Proc Roy Soc Lond B 271(1549):1723–1728. https://doi.org/10.1098/rspb.2004.2773
Clark AB (1978) Sex ratio and local resource competition in a prosimian primate. Science 201(4351):163–165. https://doi.org/10.1126/science.201.4351.163
Clark MM, Bone S, Galef BG (1990) Evidence of sex-biased postnatal maternal investment by Mongolian gerbils. Anim Behav 39(4):735–744. https://doi.org/10.1016/S0003-3472(05)80385-9
Clark MM, Waddington CL, Galef BG (1991) Further evidence of sex-biased maternal investment by Mongolian gerbil dams. Anim Behav 42(1):161–162. https://doi.org/10.1016/S0003-3472(05)80621-9
Clutton-Brock TH, Iason GR (1986) Sex ratio variation in mammals. Quart Rev Biol 61(3):339–374. https://doi.org/10.1086/415033
Clutton-Brock TH, Sheldon BC (2010) Individuals and populations: the role of long–term, individual-based studies of animals in ecology and evolutionary biology. Trend Ecol Evol 25(10):562–573. https://doi.org/10.1016/j.tree.2010.08.002
Clutton-Brock TH, Albon SD, Guinness FE (1982) Competition between female relatives in a matrilocal mammal. Nature 300(5888):178–180. https://doi.org/10.1038/300178a0
Clutton-Brock TH, Albon SD, Guinness FE (1984) Maternal dominance, breeding success and birth sex ratios in red deer. Nature 308(5957):358–360. https://doi.org/10.1038/308358a0
Cockburn A, Scott MP, Dickman CR (1985) Sex ratio and intrasexual kin competition in mammals. Oecologia 66(3):427–429. https://doi.org/10.1007/BF00378310
Conway CH (1955) Embryo resorption and placental scar formation in the rat. J Mamm 36(4):516–532. https://doi.org/10.2307/1375806
CorelDRAW (2012) CorelDRAW Home & Student (Version X6). Corel Corporation. https://www.coreldraw.com/en/product/home-student/
Darwin C (1871) The descent of man and selection in relation to sex. John Murray, London
Dobson FS, Michener GR (1995) Maternal traits and reproduction in Richardson’s ground squirrels. Ecology 76:851–862. https://doi.org/10.2307/1939350
Dolf G, Gaillard C, Schelling C, Hofer A, Leighton E (2008) Cryptorchidism and sex ratio are associated in dogs and pigs. J Anim Sci 86(10):2480–2485. https://doi.org/10.2527/jas.2007-0607
Dušek A, Bartoš L, Sedláček F (2011) Mixed sex allocation strategies in a polytocous mammal, the house mouse (Mus musculus). Behav Ecol Sociobiol 65(12):2209–2271. https://doi.org/10.1007/s00265-011-1229-8
Fairbanks LA, McGuire MT (1995) Maternal condition and the quality of maternal care in vervet monkeys. Behaviour 132(9–10):733–754. https://doi.org/10.1163/156853995X00126
Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, Oxford
Fisher DO (1999) Offspring sex ratio variation in the bridled nailtail wallaby, Onychogalea fraenata. Behav Ecol Sociobiol 45(6):411–419. https://doi.org/10.1007/s002650050578
Gedir JV, Michener GR (2014) Litter sex ratios in Richardson’s ground squirrels: long term data support random sex allocation and homeostasis. Oecologia 174(4):1225–1239. https://doi.org/10.1007/s00442-013-2861-y
Grant VJ (2008) Sex of bovine embryos may be related to mothers’ preovulatory follicular testosterone. Biol Repro 78(5):812–815. https://doi.org/10.1095/biolreprod.107.066050
Gray C, Long S, Green C, Gardiner SM, Craigon J, Gardner DS (2013) Maternal fructose and/or salt intake and reproductive outcome in the rat: effects on growth, fertility, sex ratio, and birth order. Biol Repro 89(3):1–8. https://doi.org/10.1095/biolreprod.113.109595
Gubbels EJ, Scholten J, Janss L, Rothuizen J (2009) Relationship of cryptorchidism with sex ratios and litter sizes in 12 dog breeds. Anim Repro Sci 113(1):187–195. https://doi.org/10.1016/j.anireprosci.2008.07.004
Helmreich RL (1960) Regulation of reproductive rate by intra-uterine mortality in the deer mouse. Science 132(3424):417–418. https://doi.org/10.1126/science.132.3424.417
Hik DS (1995) Does risk of predation influence population dynamics? Evidence from cyclic decline of snowshoe hares. Wildl Res 22(1):115–129. https://doi.org/10.1071/WR9950115
Hothorn T, Hornik K (2017) exactRankTests: Exact Distributions for Rank and Permutation Tests. R package version 0.8-29., Accessed June 26, 2018. https://CRAN.R-project.org/package=exactRankTests
Isaac JL, Krockenberger AK, Johnson CN (2005) Adaptive sex allocation in relation to life-history in the common brushtail possum, Trichosurus vulpecula. J Anim Ecol 74(3):552–558. https://doi.org/10.1111/j.1365-2656.2005.00954.x
Johnson CN (1986) Philopatry, reproductive success of females, and maternal investment in the red-necked wallaby. Behav Ecol Sociobiol 19(2):143–150. https://doi.org/10.1007/BF00299949
Johnson CN, Clinchy M, Taylor AC, Krebs CJ, Jarman PJ, Payne A, Ritchie EG (2001) Adjustment of offspring sex ratios in relation to the availability of resources for philopatric offspring in the common brushtail possum. Proc Roy Soc Lond B 268(1480):2001–2005. https://doi.org/10.1098/rspb.2001.1723
Koskela E, Huitu O, Koivula M, Korpimäki E, Mappes T (2004) Sex-biased maternal investment in voles: importance of environmental conditions. Proc Roy Soc Lond B 271(1546):1385–1391. https://doi.org/10.1098/rspb.2004.2711
Krackow S (1997) Maternal investment, sex-differential prospects, and the sex ratio in wild house mice. Beha Ecol Sociobiol 41(6):435–443. https://doi.org/10.1007/s002650050404
Kruuk LEB, Clutton-Brock TH, Rose KE, Guinness FE (1999) Early determinants of lifetime reproductive success differ between the sexes in red deer. Proc Roy Soc Lond B 266(1429):1655–1661. https://doi.org/10.1098/rspb.1999.0828
Laws EA, Archie JW (1981) Appropriate use of regression analysis in marine biology. Marine Biol 65(1):13–16. https://doi.org/10.1007/BF00397062
Legendre P (2014) lmodel2: Model II Regression. R package version 1.7-2., Accessed July 17, 2017. https://CRAN.R-project.org/package=lmodel2
Maxwell D, Jennings S (2005) Power of monitoring programmes to detect decline and recovery of rare and vulnerable fish. J Appl Ecol 42(1):25–37. https://doi.org/10.1111/j.1365-2664.2005.01000.x
McClure PA (1981) Sex-biased litter reduction in food-restricted wood rats (Neotoma floridana). Science 211(4486):1058–1060. https://doi.org/10.1126/science.211.4486.1058
Michener GR (1973) Intraspecific aggression and social organization in ground squirrels. J Mammal 54(4):1001–1003. https://doi.org/10.2307/1379104
Michener GR (1979) Spatial relationships and social organization of adult Richardson’s ground squirrels. Can J Zool 57(1):125–139. https://doi.org/10.1139/z79-010
Michener GR (1981) Ontogeny of spatial relationships and social behaviour in juvenile Richardson’s ground squirrels. Can J Zool 59(9):1666–1676. https://doi.org/10.1139/z81-231
Michener GR (1982) Infanticide in ground squirrels. Anim Behav 30(3):936–938. https://doi.org/10.1016/S0003-3472(82)80173-5
Michener GR (1989a) Reproductive effort during gestation and lactation by Richardson’s ground squirrels. Oecologia 78(1):77–86. https://doi.org/10.1007/BF00377200
Michener GR (1989b) Sexual differences in interyear survival and life-span of Richardson’s ground squirrels. Can J Zool 67(7):1827–1831. https://doi.org/10.1139/z89-260
Michener GR (1996) Establishment of a colony of Richardson’s ground squirrel in southern Alberta. In Willms, W. D., Dormaar, J. F. (Eds.) Proceedings of the Fourth Prairie Conservation and Endangered Species Workshop, Provincial Museum of Alberta natural history occasional paper 23, 303-308, Provincial Museum of Alberta, Edmonton
Michener GR, Michener DR (1977) Population structure and dispersal in Richardson’s ground squirrels. Ecology 58(2):359–368. https://doi.org/10.2307/1935610
Moses RA, Boutin S, Teferi T (1998) Sex-biased mortality in woodrats occurs in the absence of parental intervention. Anim Behav 55(3):563–571. https://doi.org/10.1006/anbe.1997.0643
Myers P, Master LL, Garret RA (1985) Ambient temperature and rainfall: an effect on sex ratio and litter size in deer mice. J Mammal 66(2):289–298. https://doi.org/10.2307/1381241
O’Neill RV, DeAnglis DL, Waide JB, Allen TFH (1986) A hierarchical concept of ecosystems. Princeton University Press, Princeton
O’Regan D, Kenyon CJ, Seckl JR, Holmes MC (2010) Environmental disturbance confounds prenatal glucocorticoid programming experiments in Wistar rats. Lab Anim 44(3):199–205. https://doi.org/10.1258/la.2009.009032
Oddie K (1998) Sex discrimination before birth. Trend Ecol Evol 13(4):130–131. https://doi.org/10.1016/S0169-5347(97)01320-7
Owusu BA, Adu EK, Awotwi EK, Awumbila B (2010) Embryonic resorption, litter size and sex ratio in the grasscutter, Thryonomys swinderianus. Anim Repro Sci 118(2):366–371. https://doi.org/10.1016/j.anireprosci.2009.08.013
Pemberton JM, Albon SD, Guinness FE, Clutton-Brock TH, Dover GA (1992) Behavioral estimates of male mating success tested by DNA fingerprinting in a polygynous mammal. Behav Ecol 3(1):66–75. https://doi.org/10.1093/beheco/3.1.66
Pike TW (2005) Sex ratio manipulation in response to maternal condition in pigeons: evidence for pre-ovulatory follicle selection. Behav Ecol Sociobiol 58(4):407–413. https://doi.org/10.1007/s00265-005-0931-9
Ricker WE (1973) Linear regressions in fishery research. J Fish Res Board Can 30(3):409–434. https://doi.org/10.1139/f73-072
Roche JR, Lee JM, Berry DP (2006) Pre-conception energy balance and secondary sex ratio—partial support for the Trivers-Willard hypothesis in dairy cows. J Dairy Sci 89(6):2119–2125. https://doi.org/10.3168/jds.S0022-0302(06)72282-2
Rose KE, Clutton-Brock TH, Guinness FE (1998) Cohort variation in male survival and lifetime breeding success in red deer. J Anim Ecol 67(6):979–986. https://doi.org/10.1046/j.1365-2656.1998.6760979.x
Rosenfeld CS, Grimm KM, Livingston KA, Brokman AM, Lamberson WE, Roberts RM (2003) Striking variation in sex ratio of pups born to mice according to whether maternal diet is high in fat or carbohydrate. Proc Nat Acad Sci USA 100(8):4628–4632. https://doi.org/10.1073/pnas.0330808100
Ryan CP, Anderson WG, Gardiner LE, Hare JF (2012) Stress-induced sex ratios in ground squirrels: support for a mechanistic hypothesis. Behav Ecol 23(1):160–167. https://doi.org/10.1093/beheco/arr169
Ryan CP, Anderson WG, Berkvens CN, Hare JF (2014) Maternal gestational cortisol and testosterone are associated with trade-offs in offspring sex and number in a free-living rodent (Urocitellus richardsonii). PLoS ONE 9(10): https://doi.org/10.1371/journal.pone.0111052
Schell CJ, Young JK, Lonsdorf EV, Santymire RM (2013) Anthropogenic and physiologically induced stress responses in captive coyotes. J Mamm 94(5):1131–1140. https://doi.org/10.1644/13-MAMM-A-001.1
Schmidt CM, Hood WR (2012) Calcium availability influences litter size and sex ratio in white-footed mice (Peromyscus leucopus). PLoS ONE 7(8): https://doi.org/10.1371/journal.pone.0041402
Scholz F, Zhu A (2017) kSamples: K-Sample Rank Tests and their Combinations. R package version 1.2-7, Accessed March 7, 2018. https://cran.r-project.org/package=kSamples
Sergeant CJ, Moynahan BJ, Johnson WF (2012) Practical advice for implementing long-term ecosystem monitoring. J Appl Ecol 49(5):969–973. https://doi.org/10.1111/j.1365-2664.2012.02149.x
Sheriff MJ, Krebs CJ, Boonstra R (2009) The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J Anim Ecol 78(6):1249–1258. https://doi.org/10.1111/j.1365-2656.2009.01552.x
Spiegelhalter DJ, Best NG, Carlin BP, Van Der Linde A (2002) Bayesian measures of model complexity and fit. J Roy Stat Soc B 64(4):583–639. https://doi.org/10.1111/1467-9868.00353
Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3(3):259–268. https://doi.org/10.2307/2389364
Sullivan TP, Sullivan DS, Lindgren PMF, Ransome DB (2013) Stand structure and small mammals in intensively managed forests: scale, time, and testing extremes. For Ecol Manag 310:1071–1087. https://doi.org/10.1016/j.foreco.2013.02.025
Tait DEN (1980) Abandonment as a reproductive tactic – the example of grizzly bears. Am Nat 115(6):800–808. https://doi.org/10.1086/283601
Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179(4068):90–92. https://doi.org/10.1126/science.179.4068.90
Van Meter PE, French JA, Dloniak SM, Watts HE, Kolowski JM, Holekamp KE (2009) Fecal glucocorticoids reflect socio-ecological and anthropogenic stressors in the lives of wild spotted hyenas. Horm Behav 55(2):329–337. https://doi.org/10.1016/j.yhbeh.2008.11.001
Voland E (1984) Human sex-ratio manipulation: historical data from a German parish. J Human Evol 13(1):99–107. https://doi.org/10.1016/S0047-2484(84)80080-9
Wickham H (2009) ggplot2: Elegant graphics for data analysis. Springer Verlag, New York
Wild G, West SA (2007) A sex allocation theory for vertebrates: combining local resource competition and condition-dependent allocation. Am Nat 170(5):E112–E128. https://doi.org/10.1086/522057
Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat 100(916):687–690. https://doi.org/10.1086/282461
Williams GC (1979) The question of adaptive sex ratio in outcrossed vertebrates. Proc Roy Soc Lond B 205(1161):567–580. https://doi.org/10.1098/rspb.1979.0085
Wood T (2018) Alarm calling, stress, and fitness in central versus peripheral territories of Richardson’s ground squirrels (Urocitellus richardsonii). MSc Thesis, University of Manitoba, Winnipeg 61 pp. https://mspace.lib.umanitoba.ca/bitstream/handle/1993/33331/Wood_Thomas.pdf?
Yeaton RI (1972) Social behavior and social organization in Richardson’s ground squirrel (Spermophilus richardsonii) in Saskatchewan. J Mamm 53(1):139–147. https://doi.org/10.2307/1378834
Acknowledgements
We thank the Assiniboine Park Zoo for providing access to ground squirrels on their property, and Drs. Charlene Berkvens, Chris Enright, Heather Anholt and Ms. Brittany Semeniuk for their guidance in dissecting out ground squirrel ovarian horns. We also thank Kevin Bairos–Novak, Lindsay Bristow, Taylor Carey, Taylor Connolly, Katie Downs, Daniel Enright, Justin Feilberg, Melanie Fetterly, Angela Freeman, Laura Gardiner, Leanne Harapiak, Christine Legal, Holly McCullough, Maria Modanu, Dave Swan, Lynne Reykdal, Cole Robson-Hyska, Anthony Roche, Calen Ryan, Lindsay Skyner, Amy Thompson, David Wilson, Jennifer Sloan and Thomas Wood who contributed to the collection of litter data over the years. Funding for this research was provided by Discovery Grants awarded by the Natural Sciences and Engineering Research Council of Canada (NSERC) to JFH, a University of Manitoba Graduate Enhancement of Tri-Council Support stipend paid to ARY, scholarships from NSERC and the Faculty of Science awarded to student participants, and funds awarded to JFH from the University of Manitoba Faculty of Science Field Work Support Program.
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ARY collated and analysed data collected by JFH and his trainees in the course of field research on Richardson’s ground squirrels. JFH conceived the present study, which ARY refined in the context of his M.Sc. research, and presented in his Master’s thesis. JFH wrote the first draft of the manuscript based on a chapter within ARY’s thesis, which was exchanged between JFH and ARY over the course of multiple revisions, and ultimately revised in light of initial review comments to produce the present manuscript.
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Yeo, A.R., Hare, J.F. Richardson’s ground squirrel litter size–sex ratio trade-off reveals conditional adaptive sex allocation. Oecologia 195, 915–925 (2021). https://doi.org/10.1007/s00442-021-04900-3
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DOI: https://doi.org/10.1007/s00442-021-04900-3