The erratic and contingent progression of research on territoriality: a case study

  • Ambika KamathEmail author
  • Jonathan Losos


Our understanding of animal mating systems has changed dramatically with the advent of molecular methods to determine individuals’ reproductive success. But why are older behavioral descriptions and newer genetic descriptions of mating systems often seemingly inconsistent? We argue that a potentially important reason for such inconsistencies is a research trajectory rooted in early studies that were equivocal and overreaching, followed by studies that accepted earlier conclusions at face value and assumed, rather than tested, key ideas about animal mating systems. We illustrate our argument using Anolis lizards, whose social behavior has been studied for nearly a century. A dominant view emerging from this behavioral research was that anoles display strict territorial polygyny, where females mate with just the one male in whose territory they reside. However, all genetic evidence suggests that females frequently mate with multiple males. We trace this mismatch to early studies that concluded that anoles are territorial based on limited data. Subsequent research assumed territoriality implicitly or explicitly, resulting in studies that were unlikely to uncover or consider important any evidence of anoles’ departures from strict territorial polygyny. Thus, descriptions of anole behavior were largely led away from predicting a pattern of female multiple mating. We end by considering the broader implications of such erratic trajectories for the study of animal mating systems and posit that precise definitions, renewed attention to natural history, and explicitly questioning assumptions made while collecting behavioral observations will allow us to move towards a fuller understanding of animal mating systems.

Significance statement

Mismatches between behavioral and genetic descriptions of mating systems are widespread across animals. We argue that these discrepancies can arise from the erratic and contingent progression of research on space use behavior and social interactions. We demonstrate such a trajectory in Anolis lizards, where decades of behavioral data led not only to the conclusion that anoles are territorial but also to the erroneous expectation, disproven by genetic evidence, that each female mates with just one male. The earliest studies concluded that anoles are territorial based on flimsy evidence, leading subsequent studies to implicitly and explicitly assume territorial behavior; later studies were thus unlikely to detect, or consider important, departures from territoriality that could facilitate female multiple mating. Such research trajectories are likely not unique to anoles, and we contend that avoiding these trajectories requires renewed and continued attention to the natural history of even well-studied organisms.


Anolis History Mating system Territorial Polygyny 



J.A. Stamps and R.R. Tokarz gave us valuable feedback on previous drafts that substantially improved the manuscript, as did C.M. Donihue, Y.E. Stuart, S.R. Prado-Irwin, P. Muralidhar, M.E. Kemp, N.E. Herrmann, M.R. Lambert, E.E. Burnell, D.P. Rice, J.H. Boyle, L.J. Martin, and two anonymous reviewers.

Supplementary material

265_2017_2319_MOESM1_ESM.docx (32 kb)
ESM 1 (DOCX 31 kb)


  1. Alworth TJ (1986) Perch availability and season affect aggression levels in the territorial lizard, Anolis carolinensis. Am Zool 26:1041CrossRefGoogle Scholar
  2. Avise JC, Jones AG, Walker D et al (2002) Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annu Rev Genet 36:19–45CrossRefPubMedGoogle Scholar
  3. Birkhead TR (2010) How stupid not to have thought of that: post-copulatory sexual selection. J Zool 281:78–93CrossRefGoogle Scholar
  4. Boomsma JJ, Kronauer DJC, Pedersen JS (2009) The evolution of social insect mating systems. In: Gadaue J, Fretwell J (eds) Organization of insect societies. Harvard University Press, Cambridge, pp 3–25Google Scholar
  5. Bush JM, Quinn MM, Balreira EC, Johnson MA (2016) How do lizards determine dominance? Applying ranking algorithms to animal social behaviour. Anim Behav 118:65–74CrossRefGoogle Scholar
  6. Calsbeek R (2009) Sex-specific adult dispersal and its selective consequences in the brown anole, Anolis sagrei. J Anim Ecol 78:617–624CrossRefPubMedGoogle Scholar
  7. Calsbeek R, Bonneaud C, Prabhu S, Manoukis N, Smith TB (2007) Multiple paternity and sperm storage lead to increased genetic diversity in Anolis lizards. Evol Ecol Res 9:495–503Google Scholar
  8. Clutton-Brock T (2009) Sexual selection in females. Anim Behav 77:3–11CrossRefGoogle Scholar
  9. Coltman DW, Festa-Bianchet M, Jorgensen JT, Strobeck C (2002) Age-dependent sexual selection in bighorn rams. Proc R Soc Lond B 269:165–172CrossRefGoogle Scholar
  10. Darwin C (1871) The descent of man, and selection in relation to sex. John Murray, LondonCrossRefGoogle Scholar
  11. Dewsbury DA (1998) Robert Yerkes, sex research, and the problem of data simplification. Hist Psychol 1:116–129CrossRefGoogle Scholar
  12. Dewsbury DA (2005) The Darwin-Bateman paradigm in historical context. Integr Comp Biol 45:831–837CrossRefPubMedGoogle Scholar
  13. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, PrincetonGoogle Scholar
  14. Emlen JT (1958) Defended area?—a critique of the territory concept and of conventional thinking. Ibis 99:352Google Scholar
  15. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223CrossRefPubMedGoogle Scholar
  16. Evans LT (1936a) Social behavior of the normal and castrated lizard, Anolis carolinensis. Science 83:104CrossRefPubMedGoogle Scholar
  17. Evans LT (1936b) Territorial behavior of normal and castrated females of Anolis carolinensis. Pedagog Semin J Genet Psychol 49:49–60CrossRefGoogle Scholar
  18. Evans LT (1936c) A study of a social hierarchy in the lizard Anolis carolinensis. Pedagog Semin J Genet Psychol 48:88–111CrossRefGoogle Scholar
  19. Evans LT (1938a) Cuban field studies on the territoriality of the lizard Anolis sagrei. J Comp Psychol 25:97–125CrossRefGoogle Scholar
  20. Evans LT (1938b) Courtship behavior and sexual selection of Anolis. J Comp Zool 26:475–497Google Scholar
  21. Fisher HS, Hoekstra HE (2010) Competition drives cooperation among closely related sperm of deer mice. Nature 463:801–803CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fitzpatrick SM, Wellington WG (1982) Insect territoriality. Can J Zool 61:471–486CrossRefGoogle Scholar
  23. Flanagan SP, Bevier CR (2014) Do male activity level and territory quality affect female association time in the brown anole, Anolis sagrei? Ethology 120:365–374CrossRefGoogle Scholar
  24. Fleishman LJ (1988) The social behavior of Anolis auratus, a grass anole from Panama. J Herpetol 22:13–23CrossRefGoogle Scholar
  25. Gordon RE (1956) The biology and biodemography of Anolis carolinensis carolinensis Voight. Dissertation, Tulane UniversityGoogle Scholar
  26. Gowaty PA (2003) Sexual natures: how feminism changed evolutionary biology. Signs 28:901–921CrossRefGoogle Scholar
  27. Greenberg B, Noble GK (1944) Social behavior of the American chameleon (Anolis carolinensis Voight). Physiol Zool 17:392–439CrossRefGoogle Scholar
  28. Greene HW (2005) Organisms in nature as a central focus for biology. Trends Ecol Evol 20:23–27CrossRefPubMedGoogle Scholar
  29. Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212CrossRefPubMedGoogle Scholar
  30. Harrison AS (2014) The evolution and diversity of the Anolis dewlap. Dissertation, Harvard UniversityGoogle Scholar
  31. Hicks RM, Trivers RL (1983) The social behavior of Anolis valencienni. In: Rhodin GJ, Miyata K (eds) Recent advances in herpetology and evolutionary biology. Museum of Comparative Zoology, Cambridge, pp 570–595Google Scholar
  32. Hinde RA (1956) The biological significance of the territories of birds. Ibis 98:340–369CrossRefGoogle Scholar
  33. Hrdy SB (1986) Empathy, polyandry, and the myth of the “coy” female. In: Bleier R (ed) Feminist approaches to science. Pergamon Press, New York, pp 119–146Google Scholar
  34. Jenssen TA, Nunez SC (1998) Spatial and breeding relationships of the lizard, Anolis carolinensis: evidence of intrasexual selection. Behaviour 135:981–1003CrossRefGoogle Scholar
  35. Jenssen TA, Greenberg N, Hovde KA (1995) Behavioral profile of free-ranging male lizards, Anolis carolinensis, across breeding and post-breeding seasons. Herpetol Monogr 9:41–62CrossRefGoogle Scholar
  36. Jenssen TA, Orrell KS, Lovern MB (2000) Sexual dimorphism in aggressive signal structure and use by a polygynous lizard, Anolis carolinensis. Copeia 2000:140–149CrossRefGoogle Scholar
  37. Jenssen T, Lovern M, Congdon J (2001) Field-testing the protandry-based mating system for the lizard, Anolis carolinesis : does the model organism have the right model? Behav Ecol Sociobiol 50(2):162–172CrossRefGoogle Scholar
  38. Jenssen TA, Decourcy KR, Congdon JD (2005) Assessment in contests of male lizards (Anolis carolinensis): how should smaller males respond when size matters? Anim Behav 69:1325–1336CrossRefGoogle Scholar
  39. Johnson MA (2007) Behavioral ecology of Caribbean Anolis lizards: a comparative approach. Dissertation, Washington UniversityGoogle Scholar
  40. Kappeler PM, Barrett L, Blumstein DT, Clutton-Brock TH (2013) Constraints and flexibility in mammalian social behaviour: introduction and synthesis. Philos T Roy Soc B 368:0120337CrossRefGoogle Scholar
  41. Klug H (2011) Animal mating systems. eLS John Wiley and Sons Ltd, ChichesterCrossRefGoogle Scholar
  42. Losos JB (2009) Lizards in an evolutionary tree. University of California Press, BerkeleyGoogle Scholar
  43. Lott DF (1984) Intraspecific variation in the social systems of wild vertebrates. Behaviour 88:266–325CrossRefGoogle Scholar
  44. Maher CR, Lott DF (1995) Definitions of territoriality used in the study of variation in vertebrate spacing systems. Anim Behav 49:1581–1597CrossRefGoogle Scholar
  45. Martins EP (1994) Phylogenetic perspectives on the evolution of lizard territoriality. In: Vitt LJ, Pianka ER (eds) Lizard ecology: historical and experimental perspectives. Princeton University Press, Princeton, pp 117–144Google Scholar
  46. Milam EL (2010) Looking for a few good males. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  47. Noble GK, Bradley HT (1933) The mating behavior of lizards; its bearing on the theory of sexual selection. Ann N Y Acad Sci 35:25–100CrossRefGoogle Scholar
  48. Oliver JA (1948) The anoline lizards of Bimini, Bahamas. Am Mus Novit 1383:1–36Google Scholar
  49. Orians GH (1969) On the evolution of mating systems in birds and mammals. Am Nat 103:589–603CrossRefGoogle Scholar
  50. Orr TJ, Brennan PLR (2015) Sperm storage: distinguishing selective processes and evaluating criteria. Trends Ecol Evol 30:261–272CrossRefPubMedGoogle Scholar
  51. Passek KM (2002) Extra-pair paternity within the female-defense polygyny of the lizard, Anolis carolinensis: evidence of alternative mating strategies. Dissertation, Virginia Polytechnic InstituteGoogle Scholar
  52. Philibosian R (1975) Territorial behavior and population regulation in the lizards, Anolis acutus and A. cristatellus. Copeia 1975:428–444CrossRefGoogle Scholar
  53. Qualls CP, Jaeger RG (1991) Dear enemy recognition in Anolis carolinensis. J Herpetol 25:361–363CrossRefGoogle Scholar
  54. Rand AS (1967a) Ecology and social organization in the iguanid lizard Anolis lineatopus. Proc U S Natl Mus 122:1–79CrossRefGoogle Scholar
  55. Rand AS (1967b) The adaptive significance of territoriality in iguanid lizards. In: Milstead WW (ed) Lizard ecology: a symposium. University of Missouri Press, Columbia, pp 106–115Google Scholar
  56. Ruby DE (1984) Male breeding success and differential access to females in Anolis carolinensis. Herpetologica 40:272–280Google Scholar
  57. Schoener TW (1981) An empirically based estimate of home range. Theor Popul Biol 20:281–325CrossRefGoogle Scholar
  58. Schoener TW, Schoener A (1980) Densities, sex ratios, and population structure in four species of Bahamian Anolis lizards. J Anim Ecol 49:19–53CrossRefGoogle Scholar
  59. Schoener TW, Schoener A (1982) Intraspecific variation in home-range size in some Anolis lizards. Ecology 63:809–823CrossRefGoogle Scholar
  60. Simon VB (2011) Communication signal rates predict interaction outcome in the brown anole lizard, Anolis sagrei. Copeia 2011:38–45CrossRefGoogle Scholar
  61. Stamps JA (1977) Social behavior and spacing patterns in lizards. In: Gans C, Tinkle DW (eds) Biology of the reptilia, Ecology and Behaviour A, vol 7. Academic Press, New York, pp 265–334Google Scholar
  62. Stamps JA (1983) Sexual selection, sexual dimorphism, and territoriality. In: Huey R, Pianka ER, Schoener TW (eds) Lizard ecology. Harvard University Press, Cambridge, pp 169–204Google Scholar
  63. Stamps JA (1994) Territorial behavior: testing the assumptions. Adv Stud Behav 23:173–231CrossRefGoogle Scholar
  64. Stamps JA (1995) Using growth-based models to study behavioral factors affecting sexual size dimorphism. Herpetol Monogr 9:75–87CrossRefGoogle Scholar
  65. Tang-Martinez Z (2016) Rethinking Bateman’s principles: challenging persistent myths of sexually reluctant females and promiscuous males. J Sex Res 53:532–559CrossRefPubMedGoogle Scholar
  66. Tang-Martinez Z, Ryder TB (2005) The problem with paradigm: Bateman’s worldview as a case study. Integr Comp Biol 45:821–830CrossRefPubMedGoogle Scholar
  67. Tewksbury JJ, Anderson JGT, Bakker JD et al (2014) Natural history’s place in science and society. Bioscience 64:300–310CrossRefGoogle Scholar
  68. Thompson FG (1954) Notes on the behavior of the lizard Anolis carolinensis. Copeia 1954:299CrossRefGoogle Scholar
  69. Tinbergen N (1957) The functions of territory. Bird Study 4:14–27CrossRefGoogle Scholar
  70. Tokarz RR (1998) Mating pattern in the lizard Anolis sagrei: implications for mate choice and sperm competition. Herpetologica 54:388–394Google Scholar
  71. Tokarz RR (2008) Males distinguish between former female residents of their territories and unfamiliar nonresident females as preferred mating partners in the lizard Anolis sagrei. J Herpetol 42:260–264CrossRefGoogle Scholar
  72. Tokarz RR, McMann S, Seitz L, John-Alder H (1998) Plasma corticosterone and testosterone levels during the annual reproductive cycle of male brown anoles (Anolis sagrei). Physiol Zool 71:139–146CrossRefPubMedGoogle Scholar
  73. Trivers RL (1976) Sexual selection and resource-accruing abilities in Anolis garmani. Evolution 30:253–269CrossRefPubMedGoogle Scholar
  74. Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Mol Ecol 17:2566–2580CrossRefPubMedGoogle Scholar
  75. Webster R, Greenberg N (1988) Territoriality and social dominance in the green anole lizard. Am Zool 28:A73CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Organismic and Evolutionary Biology and the Museum of Comparative ZoologyHarvard UniversityCambridgeUSA

Personalised recommendations