Digit ratios in two lacertid lizards: sexual dimorphism and morphological and physiological correlates

Abstract

Digit length ratio (primarily 2D:4D) has become increasingly popular as a possible biomarker of intrauterine steroid exposure in the human medical, social and psychological literature. Human males tend to have lower digit ratios than females, and individuals with low ratios tend to excel in physical performance, especially in endurance-related sports. Because early limb development is evolutionarily conservative, it has been speculated that these trends should also be visible in other tetrapod vertebrates. However, studies on non-human vertebrates are scant, and their results suggest that sexual dimorphism in digit ratios and the associations with physical performance are much more intricate and taxon-specific than presumed. In this study, we compared digit ratios of two Podarcis lizards among sexes, colour morphs and species. We also tested for associations with three performance characteristics that are of ecological relevance. Both species examined exhibit male-larger sexual dimorphism in digit ratio. 2D:4D, 3D:4D and 2D:3D ratios are tightly correlated within the manus and the pes, but less so between manus and pes. In the colour polymorphic species P. melisellensis, the yellow morph exhibits higher dimorphism than the orange and white morphs. Digit ratios did not correlate with individual performance for sprint speed or endurance, but within males of P. melisellensis, individuals with higher digit ratios correlated positively with head size and bite force. We conclude that digit ratios in lizards deserve attention, because they exhibit sexual dimorphism and correlate with ecologically relevant morphological and performance variables. As lizard species differ widely in mating systems, reproductive mode, habitat use and locomotor behaviour, they seem excellent model animals for studying patterns in digit length ratios.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Abouheif E, Fairbairn DJ (1997) A comparative analysis of allometry for sexual size dimorphism: assessing Rensch’s rule. Am Nat 149:540–562

    Article  Google Scholar 

  2. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with image. J Bioph Int 11:36–42

    Google Scholar 

  3. Arnold EN (1987) Resource partition among lacertid lizards in southern Europe. J Zool 1:739–782

    Article  Google Scholar 

  4. Baker F (1888) Anthropological notes on the human hand. Am Anthropol 1:51–76

    Article  Google Scholar 

  5. Bauwens D, Garland T Jr, Castilla AM, Van Damme R (1995) Evolution of sprint speed in lacertid lizards: morphological, physiological, and behavioral covariation. Evolution 49:848–863

    Article  Google Scholar 

  6. Bininda-Emonds OR, Jeffery JE, Sánchez-Villagra MR, Hanken J, Colbert M, Pieau C, Selwood L, Ten Cate C, Raynaud A, Osabutey CK, Richardson MK (2007) Forelimb-hindlimb developmental timing changes across tetrapod phylogeny. BMC Evol Biol 7:182

    PubMed Central  Article  PubMed  Google Scholar 

  7. Brandt Y (2003) Lizard threat display handicaps endurance. Proc R Soc Lond B 270:1061–1068

    CAS  Article  Google Scholar 

  8. Brown WM, Finn CJ, Breedlove SM (2002) Sexual dimorphism in digit-length ratios of laboratory mice. Anat Rec 267:231–234

    Article  PubMed  Google Scholar 

  9. Burley NT, Foster VS (2002) Digit ratio varies with sex, egg order and strength of mate preference in zebra finches. Proc R Soc Lond B 271:239–244

    Article  Google Scholar 

  10. Burton LA, Henninger D, Hafetz J (2005) Gender differences in relations of mental rotation, verbal fluency, and SAT scores to finger-length ratios as hormonal indexes. Developm Neuropsychol 28:93–505

    Google Scholar 

  11. Castilla AM, Van Damme R, Bauwens D (1999) Field body temperatures, mechanisms of thermoregulation and evolution of thermal characteristics in lacertid lizards. Natura Croatica 8:275–286

    Google Scholar 

  12. Chang JL, Doughty S, Wade J, Lovern MB (2006) Sexual dimorphism in the second-to-fourth digit length ratio in green anoles, Anolis carolinensis (Squamata: polychrotidae), from the southeastern United States. Can J Zool 84:1489–1494

    Article  Google Scholar 

  13. Collaer ML, Hines M (1995) Human behavioral sex-differences: a role for gonadal hormones during early development. Psychol Bull 118:55–107

    CAS  Article  PubMed  Google Scholar 

  14. Cox RM, Skelly SL, John-Alder HB (2003) A comparative test of adaptive hypotheses for sexual size dimorphism in lizards. Evolution 57:1653–1669

    Article  PubMed  Google Scholar 

  15. Direnzo GV, Stynoski JL (2012) Patterns of second-to-fourth digit length ratios (2D:4D) in two species of frogs and two species of lizards at La Selva, Costa Rica. Anat Rec 295:597–603

    Article  Google Scholar 

  16. Downes S, Bauwens D (2002) An experimental demonstration of direct behavioural interference in two Mediterranean lacertid lizard species. Anim Behav 63:1037–1046

    Article  Google Scholar 

  17. Dreiss AN, Navarro C, De Lope F, Moller AP (2007) Digit ratios, secondary sexual characters and condition in barn swallows Hirunda rustica. Behav Ecol 19:16–21

    Article  Google Scholar 

  18. Ecker A (1875) Einige Bemerkungen über einen Schwankengen Charakter in der Hand des Menschen. Arch Anthropol 8:67–75

    Google Scholar 

  19. Eikenaar C, Husak J, Escallon C, Moore IT (2012) Variation in testosterone and corticosterone in amphibians and reptiles: relationships with latitude, elevation, and breeding season length. Am Nat 180:642–654

    Article  PubMed  Google Scholar 

  20. Forstmeier W (2005) Quantitative genetics and behavioural correlates of digit ratio in the zebra finch. Proc R Soc Lond B 272:2641–2649

    Article  Google Scholar 

  21. Garland T Jr, Losos JB (1994) Ecological morphology of locomotor performance in squamate reptiles. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, pp 240–302

    Google Scholar 

  22. Garland T Jr, Hankins T, Huey RB (1990) Locomotor capacity and social dominance in male lizards. Funct Ecol 4:243–250

    Article  Google Scholar 

  23. Gil D (2008) Hormones in avian eggs: physiology, ecology and behaviour. Adv Stud Behav 38:37–398

    Google Scholar 

  24. Golby J, Meggs J (2011) Exploring the organizational effect of prenatal testosterone upon the sporting brain. J Sport Sci Med 10:445–451

    Google Scholar 

  25. Gomes CM, Kohlsdorf T (2012) Evolution of sexual dimorphism in the digit ratio 2D:4D-relationships with body size and microhabitat use in iguanian lizards. PLoS ONE 6:e28465

    Article  Google Scholar 

  26. Harrison MA (2010) An exploratory study of the relationship between second toe length and androgen linked behaviours. J Soc Evol Cult Psychol 4:241–253

    Article  Google Scholar 

  27. Herrel A, Van Damme R, Vanhooydonck B, De Vree F (2001) The implications of bite performance for diet in two species of lacertid lizards. Can J Zool 79:662–670

    Article  Google Scholar 

  28. Hews DK, Moore MC (1996) A critical period for the organization of alternative male phenotypes of tree lizards by exogenous testosterone? Physiol Behav 60:425–429

    CAS  Article  PubMed  Google Scholar 

  29. Hews DK, Knapp R, Moore MC (1994) Early exposure to androgens affects adult expression of alternative male types in tree lizards. Horm Behav 28:1–21

    Article  Google Scholar 

  30. Hönekopp J, Schuster M (2010) A meta-analysis on 2D:4D and athletic prowess: substantial relationships but neither hand out-predicts the other. Pers Indiv Diff 48:4–10

    Article  Google Scholar 

  31. Hönekopp J, Manning JT, Müller C (2006) Digit ratio (2D:4D) and physical fitness in males and females: evidence for effects of prenatal androgens on sexually selected traits. Horm Behav 49:545–549

    Article  PubMed  Google Scholar 

  32. Huey RB, Stevenson RD (1979) Integrating thermal physiology and ecology of ectotherms: discussion of approaches. Am Zool 19:357–366

    Article  Google Scholar 

  33. Husak JF (2006) Does speed help you survive? A test with collared Lizards of different ages. Funct Ecol 20:174–179

    Article  Google Scholar 

  34. Husak JF, Fox SF, Lovern MB, Van Den Bussche RA (2006a) Faster lizards sire more offspring: sexual selection on whole-animal performance. Evolution 60:2122–2130

    CAS  Article  PubMed  Google Scholar 

  35. Husak JF, Lappin AK, Fox SF, Lemos-Espinal JA (2006b) Bite-force performance predicts dominance in male venerable collared lizards (Crotaphytus antiques). Copeia 2006:301–306

    Article  Google Scholar 

  36. Huyghe K, Vanhooydonck B, Scheers H, Molina-Borja M, Van Damme R (2005) Morphology, performance and fighting capacity in male lizards, Gallotia galloti. Funct Ecol 19:800–807

    Article  Google Scholar 

  37. Huyghe K, Vanhooydonck B, Herrel A, Tadic Z, Van Damme R (2007) Morphology, performance, behaviour and ecology of three colour morphs in males of the lizard Podarcis melisellensis. Integr Comp Biol 47:211–220

    Article  PubMed  Google Scholar 

  38. Huyghe K, Husak JF, Herrel A, Tadic Z, Moore IT, Van Damme R, Vanhooydonck B (2009) Relationships between hormones, physiological performance and immunocompetence in a color-polymorphic lizard species, Podarcis melisellensis. Horm Behav 55:488–494

    CAS  Article  PubMed  Google Scholar 

  39. Irschick DJ, Le Galliard JF (2008) Studying the evolution of whole-organism performance capacity: sex selection, and haiku—an introduction. Evol Ecol Res 10:155–156

    Google Scholar 

  40. Lailvaux SP, Herrel A, Vanhooydonck B, Meyers JJ, Irschick DJ (2004) Performance capacity, fighting tactics, and the evolution of life-stage morphs in the green anole lizard (Anolis carolinensis). Proc R Soc Lond B 271:2501–2508

    Article  Google Scholar 

  41. Lancaster LT, McAdam AG, Wingfield JC, Sinervo BR (2007) Adaptive social and maternal induction of antipredator dorsal patterns in a lizard with alternative social strategies. Ecol Lett 10:798–808

    Article  PubMed  Google Scholar 

  42. LeGalliard JF, Clobert J, Ferrière R (2004) Physical performance and Darwinian fitness in lizards. Nature 432:502–505

    CAS  Article  Google Scholar 

  43. Leoni B, Rubolini D, Romano M, di Giancamillo M, Saino N (2008) Avian hind-limb digit length ratios measured from radiographs are sexually dimorphic. J Anat 213:425–430

    PubMed Central  Article  PubMed  Google Scholar 

  44. Lombardo MP, Thorpe PA, Brown BM, Sian K (2008) Digit ratios in birds. Anat Rec 291:1611–1618

    Article  Google Scholar 

  45. López P, Martín J (2002) Locomotor capacity and dominance in male lizards Lacerta monticola: a trade-off between survival and reproductive success? Biol J Linn Soc 77:201–209

    Article  Google Scholar 

  46. Manning JT (2002) Digit ratio: a pointer to fertility, behavior, and health. Rutgers University Press, New Brunswick

    Google Scholar 

  47. Manning JT (2008) The finger ratio. Faber and Faber, London

    Google Scholar 

  48. Manning JT, Hill MR (2009) Digit ratio (2D:4D) and sprinting speed in boys. Am J Human Biol 21:210–213

    CAS  Article  Google Scholar 

  49. Manning JT, Scutt D, Wilson J, Lewis-Jones DI (1998) The ratio of 2nd to 4th digit length: a predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Hum Reprod 13:3000–3004

    CAS  Article  PubMed  Google Scholar 

  50. Manning JT, Bundred PE, Taylor R (2003) The ratio of 2nd and 4th digit length: a prenatal correlate of ability in sport. In: Reilly T, Marfell-Jones M (eds) Kinanthropometry vol. VIII. Routledge, London, pp 165–174

  51. Manning JT, Morris L, Caswell N (2007) Endurance running and digit ratio (2D:4D): implications for fetal testosterone effects on running speed and vascular health. Am J Hum Biol 19:416–421

    Article  PubMed  Google Scholar 

  52. McFadden D, Bracht MS (2002) The relative lengths and weights of metacarpals and metatarsals in baboons (Papio hamadryas). Horm Behav 43:347–355

    Article  Google Scholar 

  53. McFadden D, Shubel E (2002) Relative lengths of fingers and toes in human males and females. Horm Behav 42:492–500

    Article  PubMed  Google Scholar 

  54. McFadden D, Westhafer JG, Pasanen EG, Carlson CL, Tucker DM (2005) Physiological evidence of hypermasculinization in boys with the inattentive type of attention-deficit hyperactivity disorder (ADHD). Clin Neurosci Res 5:233–246

    Article  Google Scholar 

  55. McIntyre MH (2006) The use of digit ratios as markers for prenatal androgen action. Reprod Biol Endocrinol 4:10

    PubMed Central  Article  PubMed  Google Scholar 

  56. McIntyre MH, Cohn BA, Ellison PT (2006) Sex dimorphism in digital formulae of children. Am J Phys Anthropol 129:143–150

    Article  PubMed  Google Scholar 

  57. Miles DB (2004) The race goes to the swift: fitness consequences of variation in sprint performance in juvenile lizards. Evol Ecol Res 6:63–75

    Google Scholar 

  58. Moore MC, Hews DK, Knapp R (1998) Hormonal control and evolution of alternative male phenotypes: generalisations of models for sexual differentiation. Am Zool 38:133–151

    CAS  Article  Google Scholar 

  59. Murphy BF, Thompson MB (2011) A review of the evolution of viviparity in squamate reptiles: the past, present and future role of molecular biology and genomics. J Comp Physiol B 181:575–594

    Article  PubMed  Google Scholar 

  60. Navarro C, de Lope F, Moller AP (2007) Digit ratios (2D:4D), secondary sexual characters and cell-mediated immunity in house sparrows Passer domesticus. Behav Ecol Sociobiol 61:1161–1168

    Article  Google Scholar 

  61. Nelson E, Shultz S (2010) Finger length ratios (2D:4D) in anthropoids implicate reduced prenatal androgens in social bonding. Am J Phys Anthropol 141:395–405

    PubMed  Google Scholar 

  62. Nevo E, Gorman GC, Soulé M, Yang SY, Clover R, Jovanoviç V (1972) Competitive exclusion between insular Lacerta species (Sauria: lacertidae) notes on experimental introductions. Oecologia 10:183–190

    Article  Google Scholar 

  63. Olmo E, Signorino G (2005) Chromorep: a reptile chromosomes database. Internet references: http://193.206.118.100/professori/chromorep.pdf

  64. Perry G, Levering K, Girard I, Garland T Jr (2004) Locomotor performance and social dominance in male Anolis cristatellus. Anim Behav 67:37–47

    Article  Google Scholar 

  65. Putz DA, Gaulin SJC, Sporter RJ, McBurney DH (2004) Sex hormones and finger length: what does 2D:4D indicate? Evol Hum Behav 25:182–199

    Article  Google Scholar 

  66. Radovanovic M (1959) Zum Problem der Speziation bei Inseleidechsen. Zool Jahrb Abt Syst Geogr Biol Jena 86:395–436

    Google Scholar 

  67. Robson MA, Miles DB (2000) Locomotor performance and dominance in male tree lizards, Urosaurus dorsalis. Funct Ecol 14:338–344

    Article  Google Scholar 

  68. Romano M, Rubolini D, Martinelli R, Alquati AB, Saino N (2005) Experimental manipulation of yolk testosterone affects digit length ratios in the ring-necked pheasant (Phasianus colchicus). Horm Behav 48:342–346

    CAS  Article  PubMed  Google Scholar 

  69. Roney JR, Whitham JC, Leoni M, Bellem A, Wielebnowski N, Maestripieria D (2004) Relative digit lengths and testosterone levels in Guinea baboons. Horm Behav 45:285–290

    CAS  Article  PubMed  Google Scholar 

  70. Rubolini D, Pupin F, Sacchi R, Gentilli A, Zuffi MAL, Galeotti P, Saino N (2006) Sexual dimorphism in digit length ratios in two lizard species. Anat Rec 288A:491–497

    Article  Google Scholar 

  71. Saino N, Rubolini D, Romano M, Boncoraglio G (2007) Increased egg estradiol concentration feminizes digit ratios of male pheasants (Phasianus colchicus). Naturwissenschaften 94:207–212

    CAS  Article  PubMed  Google Scholar 

  72. Sinervo B, Miles DB, Frankino WA, Klukowski M, DeNardo DF (2000) Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm Behav 38:222–223

    CAS  Article  PubMed  Google Scholar 

  73. Talarovicova A, Krsková L, Blazeková J (2009) Testosterone enhancement during pregnancy influences the 2D:4D ratio and open field motor activity of rat siblings in adulthood. Horm Behav 55:235–239

    CAS  Article  PubMed  Google Scholar 

  74. Tamiya R, Lee SY, Ohtake F (2011) Second to fourth digit ratio and the sporting success of sumo wrestlers. Evol Human Behav 33:130–136

    Article  Google Scholar 

  75. Tobler M, Healey M, Olsson M (2011) Digit ratio, color polymorphism and egg testosterone in the Australian painted dragon. PLoS ONE 6:e16225

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  76. Tobler M, Healey M, Olsson M (2012) Digit ratio, polychromatism and associations with endurance and antipredator behaviour in male painted dragon lizard. Anim Behav 84:1261–1269

    Article  Google Scholar 

  77. Uller T (2008) Developmental plasticity and the evolution of parental effects. Trends Ecol Evol 23:432–438

    Article  PubMed  Google Scholar 

  78. Van Berkum FH (1988) Latitudinal patterns of the thermal sensitivity of sprint speed in lizards. Am Nat 132:327–343

    Article  Google Scholar 

  79. Van Damme R, Aerts P, Vanhooydonck B (1997) No trade-off between sprinting and climbing in two populations of the lizard Podarcis hispanica (Reptilia: Lacertidae). Biol J Linn Soc 60:493–503

    Article  Google Scholar 

  80. Vervust B, Grbac I, Van Damme R (2007) Differences in morphology, performance and behaviour between recently diverged populations of Podarcis sicula mirror differences in predation pressure. Oikos 116:1343–1352

    Article  Google Scholar 

  81. Vervust B, Lailvaux S, Grbac I, Van Damme R (2008) Do morphological condition indices predict locomotor performance in the lizard Podarcis sicula? Acta Oecol 34:244–251

    Article  Google Scholar 

  82. Viets BE, Ewert MA, Talent LG, Nelson CE (1994) Sex-determining mechanisms in squamate reptiles. J Exp Zool 270:45–56

    Article  Google Scholar 

  83. Voracek M (2009) Comparative study of digit ratios (2d:4d and other) and novel measures of relative finger length: testing magnitude and consistency of sex differences across samples. Percept Motor Skills 108:83–93

    Article  PubMed  Google Scholar 

  84. Voracek M, Loibl L (2009) Scientometric analysis and bibliography of digit ratio (2D:4D) research, 1998–2008. Psychol Rep 104:922–956

    Article  PubMed  Google Scholar 

  85. Voracek M, Reimer B, Dressler SG (2010) Digit ratio (2D:4D) predicts sporting success among female fencers independent from physical, experience, and personality factors. Scand J Med Sci Sports 20:853–860

    CAS  Article  PubMed  Google Scholar 

  86. Warner DA, Andrews RM (2002) Laboratory and field experiments identify sources of variation in phenotypes and survival of hatchling lizards. Biol J Linn Soc 76:105–124

    Article  Google Scholar 

  87. Yan RHY, Malisch JL, Hannon RM, Hurd PL, Garland T Jr (2008) Selective breeding for a behavioral trait changes digit ratio. PLoS ONE 3:e3216

    PubMed Central  Article  PubMed  Google Scholar 

  88. Yan RHY, Bunning M, Wahlsten D, Hurd PL (2009) Digit ratio (2D:4D) differences between 20 strains of inbred mice. PLoS ONE 4:e5801

    PubMed Central  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was funded by an FWO Project Grant, No. G.0149.09 N. K.H. is a postdoctoral fellow of the FWO-VI (Grant No. 1210215 N).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Katleen Huyghe.

Additional information

Communicated by A. Schmidt-Rhaesa.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Van Damme, R., Wijnrocx, K., Boeye, J. et al. Digit ratios in two lacertid lizards: sexual dimorphism and morphological and physiological correlates. Zoomorphology 134, 565–575 (2015). https://doi.org/10.1007/s00435-015-0275-6

Download citation

Keywords

  • Podarcis
  • Whole-animal performance
  • Developmental instability
  • Colour polymorphism