, Volume 189, Issue 3, pp 675–685 | Cite as

Reduced body size of insular black-tailed deer is caused by slowed development

  • Eric S. LongEmail author
  • Karissa L. Courtney
  • Julia C. Lippert
  • Cara M. Wall-Scheffler
Population ecology – original research


Adult body size correlates strongly with fitness, but mean body sizes frequently differ among conspecific populations. Ultimate, fitness-based explanations for these deviations in animals typically focus on community-level or physiological processes (e.g., competition, thermoregulation). However, proximate mechanisms underlying adaptive body size adjustments remain poorly understood. Adjustments in adult body size may result from shifts in growth-related life-history traits, such as the length of time to achieve adult body size (i.e., growth period) and how quickly the body increases in size (i.e., growth rate). Since insular populations often demonstrate dramatic shifts in adult body size, island populations represent a natural experiment by which to test the proximate mechanisms of size change. Here, using dental eruption patterns, we show that a dwarfed population of black-tailed deer (Odocoileus hemionus columbianus) experiences significant heterochronic shifts relative to mainland conspecifics. Namely, juvenile development slowed, such that teeth erupted ≥ 1 year later, but cranial growth suggested no concurrent adjustments in skeletal growth period. Thus, slowed growth rate, shown here with teeth, combined with unchanged growth period resulted in dwarfism, consistent with ultimate predictions for insular, resource-limited populations. Therefore, selection on body size may act on life-history traits that influence body size, rather than acting on body size directly.


Dwarfism Growth rate Heterochrony Island rule Life history 



We thank T. Crowley, Jr. for generously providing access to land. L. Arnold, T. Hildebrand, B. McMillen, R. Pedersen, and Z. Wilson provided technical support in extracting and processing teeth. Accommodations in the field were provided by the Thomas B. Crowley Laboratory at the Blakely Island Field Station.

Author contribution statement

ESL, KLC, and JCL collected samples and analyzed data, CMWS directed data collection, ESL and CMWS wrote the manuscript and secured funding for the project.


This work was supported by the Murdock Charitable Trust and a faculty research grant, through the Seattle Pacific University Center for Scholarship and Faculty Development.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.


  1. Abrams PA, Leimar O, Nylin S, Wiklund C (1996) The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. Am Nat 147:381–395. CrossRefGoogle Scholar
  2. Abrams PA, Rowe L (1996) The effects of predation on the age and size of maturity of prey. Evolution 50:1052–1061. CrossRefGoogle Scholar
  3. Adler GH, Levins R (1994) The island syndrome in rodent populations. Q Rev Biol 69:473–490. CrossRefGoogle Scholar
  4. Alonso-Alvarez C, Bertrand S, Faivre B, Sorci G (2007) Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches. Funct Ecol 21:873–879. CrossRefGoogle Scholar
  5. Anders U, von Koenigswald W, Ruf I, Smith BH (2011) Generalized individual dental age stages for fossil and extant placental mammals. Paläontol Z 85:321–339. CrossRefGoogle Scholar
  6. Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177. CrossRefGoogle Scholar
  7. Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407. CrossRefGoogle Scholar
  8. Bowyer RT, Kie JG, Van Ballenberghe V (1996) Sexual segregation in black-tailed deer: effects of scale. J Wildl Manag 60:10–17. CrossRefGoogle Scholar
  9. Brown JH, Marquet PA, Taper ML (1993) Evolution of body size: consequences of an energetic definition of fitness. Am Nat 142:573–584. CrossRefGoogle Scholar
  10. Burke A (1993) Observation of incremental growth structures in dental cementum using the scanning electron microscope. Archaeozoologia 5:41–54Google Scholar
  11. Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer, New York. Google Scholar
  12. Cao H, Wang J, Li X, Florez S, Huang Z, Venugopalan SR, Elangovan S, Skobe Z, Margolis HC, Martin JF, Amendt BA (2010) MicroRNAs play a critical role in tooth development. J Dent Res 89:779–784. CrossRefGoogle Scholar
  13. Case TJ (1978) A general explanation for insular body size trends in terrestrial vertebrates. Ecology 59:1–18. CrossRefGoogle Scholar
  14. Case TJ (1978) On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. Quart Rev Biol 53:243–282. CrossRefGoogle Scholar
  15. Clutton-Brock TH (1988) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, ChicagoGoogle Scholar
  16. Clutton-Brock TH, Harvey PH (1978) Mammals, resources and reproductive strategies. Nature 273:191–195. CrossRefGoogle Scholar
  17. Core Team R (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  18. Dammers K (2006) Using osteohistology for ageing and sexing. In: Ruscillo D (ed) Recent advances in ageing and sexing animal bones. Oxbow Books, Oxford, pp 9–39Google Scholar
  19. Day T, Abrams PA, Chase JM (2002) The role of size-specific predation in the evolution and diversification of prey life histories. Evolution 56:877–887. CrossRefGoogle Scholar
  20. Dean CM (2006) Tooth microstructure tracks the pace of human life-history evolution. Proc R Soc B 273:2799–2808. CrossRefGoogle Scholar
  21. Dirks W, Bowman JE (2007) Life history theory and dental development in four species of catarrhine primates. J Hum Evol 53:309–320. CrossRefGoogle Scholar
  22. Dmitriew CM, Blows MW, Rowe L (2010) Ontogenetic change in genetic variance in size depends on growth environment. Am Nat 175:640–649. CrossRefGoogle Scholar
  23. Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116. CrossRefGoogle Scholar
  24. Elamin F, Liversidge HM (2013) Malnutrition has no effect on the timing of human tooth formation. PLoS One 8(8):e72274. CrossRefGoogle Scholar
  25. Eveleth PB (1979) Population differences in growth: environmental and genetic factors. In: Falkner F, Tanner JM (eds) Human growth. Springer, New York, pp 373–383CrossRefGoogle Scholar
  26. Flinn EB, Strickland BK, Demarais S, Christiansen D (2013) Age and gender affect epiphyseal closure in white-tailed deer. Southeast Nat 12:297–306. CrossRefGoogle Scholar
  27. Foster JB (1964) Evolution of mammals on islands. Nature 202:234–235. CrossRefGoogle Scholar
  28. Gadgil M, Bossert WH (1970) Life historical consequences of natural selection. Am Nat 104:1–24. CrossRefGoogle Scholar
  29. Geist V (1998) Deer of the world. Stackpole Books, MechanicsburgGoogle Scholar
  30. Gillespie JH, Turelli M (1989) Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121:129–138Google Scholar
  31. Honěk A (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483–492. CrossRefGoogle Scholar
  32. Houle D (1998) How should we explain variation in the genetic variance of traits? Genetica 102:241–253. CrossRefGoogle Scholar
  33. Jin Y, Wang C, Cheng S, Zhao A (2017) MicroRNA control of tooth formation and eruption. Arch Oral Biol 73:302–310. CrossRefGoogle Scholar
  34. Jordana X, Marín-Moratalla N, DeMiguel D, Kaiser TM, Köhler M (2012) Evidence of correlated evolution of hypsodonty and exceptional longevity in endemic insular mammals. Proc R Soc B 279:3339–3346. CrossRefGoogle Scholar
  35. Jordana X, Marín-Moratalla N, Moncunill-Solé B, Bover P, Alcover JA, Köhler M (2013) First fossil evidence for the advance of replacement teeth coupled with life history evolution along an anagenetic mammalian lineage. PLoS One 25(8):e70743. CrossRefGoogle Scholar
  36. Jordana X, Köhler M (2011) Enamel microstructure in the fossil bovid Myotragus balearicus (Majorca, Spain): implications for life-history evolution of dwarf mammals in insular ecosystems. Palaeogeogr Palaeoclimatol Palaeoecol 300:59–66. CrossRefGoogle Scholar
  37. Josse J, Husson F (2016) missMDA: a package for handling missing values in multivariate data analysis. J Stat Softw 70:1–31. CrossRefGoogle Scholar
  38. Kaplan EL, Meier P (1958) Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457–481. CrossRefGoogle Scholar
  39. Kingsolver JG, Huey RB (2008) Size, temperature, and fitness: three rules. Evol Ecol Res 10:251–268Google Scholar
  40. Kingsolver JG, Pfennig DW (2004) Individual-level selection as a cause of Cope's rule of phyletic size increase. Evolution 58:1608–1612. CrossRefGoogle Scholar
  41. Kjosness K, Hines JE, Lovejoy O, Reno P (2014) The pisiform growth plate is lost in humans and supports a role for Hox in growth plate formation. J Anat 225:527–538. CrossRefGoogle Scholar
  42. Köhler M, Moyà-Solà S (2009) Physiological and life history strategies of a fossil large mammal in a resource-limited environment. Proc Natl Acad Sci. Google Scholar
  43. Köhler (2010) Fast or slow? The evolution of life history traits associated with insular dwarfing. In: Pérez-Mellado V, Ramon C (eds) Islands and evolution, vol 19. Institut Menorqui d’Estudis Recerca, Barcelona, pp 261–280Google Scholar
  44. Lawlor TE (1982) The evolution of body size in mammals: evidence from insular populations in Mexico. Am Nat 119:54–72. CrossRefGoogle Scholar
  45. Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18. CrossRefGoogle Scholar
  46. Lewall EF, Cowan IM (1963) Age determination in black-tail deer by degree of ossification of the epiphyseal plate in the long bones. Can J Zool 41:629–636. CrossRefGoogle Scholar
  47. Lister AM (1996) Dwarfing in island elephants and deer: processes in relation to time of isolation. Symp Zool Soc Lond 69:277–292Google Scholar
  48. Loe LE, Meisingset EL, Mysterud A, Langvatn R, Stenseth NC (2004) Phenotypic and environmental correlates of tooth eruption in red deer (Cervus elaphus). J Zool 262:83–89. CrossRefGoogle Scholar
  49. Loe LE, Bonenfant C, Mysterud A, Severinsen T, Øritsland NA, Langvatn R, Stien A, Irvine RJ, Stenseth NC (2007) Activity pattern of arctic reindeer in a predator-free environment: no need to keep a daily rhythm. Oecologia 152:617–624. CrossRefGoogle Scholar
  50. Lomolino MV (1985) Body size of mammals on islands: the island rule reexamined. Am Nat 125:310–316. CrossRefGoogle Scholar
  51. Lomolino MV (2005) Body size evolution in insular vertebrates: generality of the island rule. J Biogeogr 32:1683–1699. CrossRefGoogle Scholar
  52. Lomolino MV, Sax DF, Palombo MR, van der Geer AA (2012) Of mice and mammoths: evaluations of causal explanations for body size evolution in insular mammals. J Biogeogr 39:842–854. CrossRefGoogle Scholar
  53. Long ES, Diefenbach DR, Rosenberry CS, Wallingford BD (2008) Multiple proximate and ultimate causes of natal dispersal in white-tailed deer. Behav Ecol 19:1235–1242. CrossRefGoogle Scholar
  54. Long ES, Jacobsen TC, Nelson BJ, Steensma KMM (2013) Conditional daily and seasonal movement strategies of male Columbia black-tailed deer (Odocoileus hemionus columbianus). Can J Zool 91:679–688. CrossRefGoogle Scholar
  55. Mangel M, Munch SB (2005) A life-history perspective on short-and long-term consequences of compensatory growth. Am Nat 166:E155–E176. CrossRefGoogle Scholar
  56. Marín-Moratalla N, Jordana X, García-Martínez R, Köhler M (2011) Tracing the evolution of fitness components in fossil bovids under different selective regimes. C R Palevol. 10:469–478. CrossRefGoogle Scholar
  57. Martin TG, Arcese P, Scheerder N (2011) Browsing down our natural heritage: deer impacts on vegetation structure and songbird populations across an island archipelago. Biol Cons 144:459–469. CrossRefGoogle Scholar
  58. Mateo JM (2009) Maternal influences on development, social relationships, and survival behaviors. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. Chicago University Press, Chicago, pp 133–158. CrossRefGoogle Scholar
  59. McNab BK (2010) Geographic and temporal correlations of mammalian size reconsidered: a resource rule. Oecologia 164:13–23. CrossRefGoogle Scholar
  60. McNay RS, Voller JM (1995) Mortality causes and survival estimates for adult female Columbian black-tailed deer. J Wildl Manag 59:138–146. CrossRefGoogle Scholar
  61. Meiri S, Cooper N, Purvis A (2008a) The island rule: made to be broken? Proc R Soc Lond B Biol Sci 275:141–148. CrossRefGoogle Scholar
  62. Meiri S, Meijaard E, Wich SA, Groves CP, Helgen KM (2008b) Mammals of Borneo—small size on a large island. J Biogeogr 35:1087–1094. CrossRefGoogle Scholar
  63. Mitchell B (1967) Growth layers in dental cement for determining the age of Red Deer (Cervus elaphus L.). J Anim Ecol 36:279–293. CrossRefGoogle Scholar
  64. Mori A, Hasegawa M (2002) Early growth of Elaphe quadrivirgata from an insular gigantic population. Curr Herpetol 21:43–50. CrossRefGoogle Scholar
  65. Muggeo VM (2003) Estimating regression models with unknown break-points. Stat Med 22:3055–3071. CrossRefGoogle Scholar
  66. Muggeo VM (2008) Segmented: an R package to fit regression models with broken-line relationships. R News 8:20–25Google Scholar
  67. Nacarino-Meneses C, Jordana X, Orlandi-Oliveras G, Köhler M (2017) Reconstructing molar growth from enamel histology in extant and extinct Equus. Sci Rep 7:15965. CrossRefGoogle Scholar
  68. Nussey DH, Pemberton JM, Pilkington JG, Blount JD (2009) Life history correlates of oxidative damage in a free-living mammal population. Funct Ecol 23:809–817. CrossRefGoogle Scholar
  69. Palkovacs EP (2003) Explaining adaptive shifts in body size on islands: a life history approach. Oikos 103:37–44. CrossRefGoogle Scholar
  70. Pierce BM, Bleich VC, Bowyer RT (2000) Selection of mule deer by mountain lions and coyotes: effects of hunting style, body size, and reproductive status. J Mamm 81:462–472.;2 CrossRefGoogle Scholar
  71. Pike-Tay A (1991) Red deer hunting in the Upper Palaeolithic of south-west France: a study in seasonality. BAR International Series 569. British Archaeological Reports, OxfordGoogle Scholar
  72. Pollock KH, Winterstein SR, Bunck CM, Curtis PD (1989) Survival analysis in telemetry studies: the staggered entry design. J Wildl Manag 53:7–15. CrossRefGoogle Scholar
  73. Purdue JR (1983) Epiphyseal closure in white-tailed deer. J Wildl Manag 47:1207–1213. CrossRefGoogle Scholar
  74. Raia P, Meiri S (2006) The island rule in large mammals: paleontology meets ecology. Evolution 60:1731–1742. CrossRefGoogle Scholar
  75. Rauter CM, Moore AJ (2002) Quantitative genetics of growth and development time in the burying beetle Nicrophorus pustulatus in the presence and absence of post-hatching parental care. Evolution 56:96–110. CrossRefGoogle Scholar
  76. Robinette WL, Jones DA, Rogers G, Gashwiler JS (1957) Notes on tooth development and wear for Rocky Mountain mule deer. J Wildl Manag 21:134–153. CrossRefGoogle Scholar
  77. Roff DA (1992) The evolution of life histories. Chapman and Hall, New YorkGoogle Scholar
  78. Rollo CD (2002) Growth negatively impacts the life span of mammals. Evol Dev 4:55–61. CrossRefGoogle Scholar
  79. Serrano E, Angibault JM, Cargnelutti B, Hewison AM (2007) The effect of animal density on metacarpus development in captive fallow deer. Small Rumin Res 72:61–65. CrossRefGoogle Scholar
  80. Severinghaus CW (1949) Tooth development and wear as criteria of age in white-tailed deer. J Wildl Manage 13:195–216. CrossRefGoogle Scholar
  81. Shim KS (2015) Pubertal growth and epiphyseal fusion. Ann Pediatr Endocrinol Metab 20:8–12. CrossRefGoogle Scholar
  82. Sibly R, Calow P, Nichols N (1985) Are patterns of growth adaptive? J Theor Biol 112:553–574. CrossRefGoogle Scholar
  83. Simpson M, Asling CW, Evans HM (1950) Some endocrine influences on skeletal growth and differentiation. Yale J Biol Med 23(1):b1–B27Google Scholar
  84. Smith BH (2000) Schultz’s rule’and the evolution of tooth emergence and replacement patterns in primates and ungulates. In: Teaford MF, Smith MM, Ferguson MW (eds) Development, function and evolution of teeth. Cambridge University Press, Cambridge, pp 212–227CrossRefGoogle Scholar
  85. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  86. Thomas DC, Bandy PJ (1975) Accuracy of dental-wear age estimates of black-tailed deer. J Wildl Manag 39:674–678. CrossRefGoogle Scholar
  87. Thompson JL, Nelson AJ (2000) The place of Neandertals in the evolution of hominid patterns of growth and development. J Hum Evol 38:475–495. CrossRefGoogle Scholar
  88. Turelli M, Barton NH (2004) Polygenic variation maintained by balancing selection: pleiotropy, sex-dependent allelic effects and G× E interactions. Genetics 166:1053–1079. CrossRefGoogle Scholar
  89. Van den Bergh GD, Kaifu Y, Kurniawan I, Kono RT, Brumm A, Setiyabudi E, Aziz F, Morwood MJ (2016) Homo floresiensis-like fossils from the early Middle Pleistocene of Flores. Nature 534:245–248. CrossRefGoogle Scholar
  90. Vreeland JK, Diefenbach DR, Wallingford BD (2004) Survival rates, mortality causes, and habitats of Pennsylvania white-tailed deer fawns. Wildl Soc Bull 32:542–553.[542:SRMCAH]2.0.CO;2 CrossRefGoogle Scholar
  91. Wall CM (2004) Coastal ungulates: the seasonal use of ibex and Barbary sheep among Mediterranean hominins. PhD dissertation, Department of Biological Anthropology, University of Cambridge, Cambridge, EnglandGoogle Scholar
  92. Wall-Scheffler CM (2007) Digital cementum luminance analysis and the Haua Fteah hominins: how seasonality and season of use changed through time. Archaeometry 49:815–826. CrossRefGoogle Scholar
  93. Wall-Scheffler CM, Foley RA (2008) Digital cementum luminance analysis (DCLA): a tool for the analysis of climatic and seasonal signals in dental cementum. Int J Osteoarchaeol 18:11–27. CrossRefGoogle Scholar
  94. Weise M, De-Levi S, Barnes KM, Gafni R, Abad V, Baron J (2001) Effects of estrogen on growth plate senescence and epiphyseal fusion. Proc Natl Acad Sci 98:6871–6876. CrossRefGoogle Scholar
  95. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Ann Rev Ecol Syst 15:393–425. CrossRefGoogle Scholar
  96. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46(sup1):S120–S139CrossRefGoogle Scholar
  97. Wikelski M, Romero LM (2003) Body size, performance and fitness in Galapagos marine iguanas. Integr Comp Biol 43:376–386. CrossRefGoogle Scholar
  98. Wilson AJ, Pemberton JM, Pilkington JG, Clutton-Brock TH, Coltman DW, Kruuk LEB (2007) Quantitative genetics of growth and cryptic evolution of body size in an island population. Evol Ecol 21:337–356. CrossRefGoogle Scholar
  99. Wilson MC, Kenady SM, Schalk RF (2009) Late Pleistocene Bison antiquus from Orcas Island, Washington, and the biogeographic importance of an early postglacial land mammal dispersal corridor from the mainland to Vancouver Island. Quat Res 71:49–61. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologySeattle Pacific UniversitySeattleUSA

Personalised recommendations