Paceless life? A meta-analysis of the pace-of-life syndrome hypothesis

  • Raphaël Royauté
  • Monica Anderson Berdal
  • Courtney R. Garrison
  • Ned A. DochtermannEmail author
Original Article
Part of the following topical collections:
  1. Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life-history


The pace-of-life syndrome hypothesis predicts that individual differences in behavior should integrate with morphological, physiological, and life-history traits along a slow to fast pace-of-life continuum. For example, individuals with a “slow” pace-of-life are expected to exhibit a slower growth rate, delayed reproduction, longer lifespans, have stronger immune responses, and are expected to avoid risky situations relative to “fast” individuals. If supported, this hypothesis would help resolve ecological and evolutionary questions regarding the origin and maintenance of phenotypic variation. Support for the pace-of-life syndrome hypothesis has, however, been mixed. Here, we conducted a meta-analysis of 42 articles and 179 estimates testing the pace-of-life syndrome hypothesis as it applies to the integration of behaviors with physiological or life-history traits. We found little overall support for the pace-of-life syndrome hypothesis with the mean support estimated as r = 0.06. Support for the pace-of-life syndrome hypothesis was significantly higher in invertebrates (r = 0.23) than vertebrates (r = 0.02) and significantly higher when based on phenotypic (r = 0.10) versus genetic correlations (r = − 0.09). We also found that females exhibited correlations between behavior and life-history and physiology that were opposite the predictions of the pace-of-life syndrome hypothesis (r = − 0.16) and that these correlations significantly differed from those observed in males (r = 0.01) or males and females pooled (r = 0.12). It was also the case that there was little support for the hypothesis when life-history and physiological traits were independently analyzed (behavior × life-history: r = 0.12; behavior × physiology: r = 0.04). Exploratory post hoc analyses revealed that correlations of behavior with growth rate and hormone levels were more likely to show support for the predictions of the pace-of-life syndrome hypothesis. The lack of overall support found in our analyses suggests that general assertions regarding phenotypic integration due to “pace-of-life” should be re-evaluated.

Significance statement

The pace-of-life syndrome hypothesis has been proposed as an overall organizational framework for the integration of behavioral, life-history, and physiological traits. This hypothesis provides potentially profound insights into how and why phenotypic traits might covary and why phenotypic variation may be maintained within populations. Over the last 7 years, this organizational framework has been intensively investigated as it pertains to relationships between behavior and other traits. Here, we conducted an overall analysis of whether the hypothesis was supported. Despite considerable research investment across behavioral ecology, we did not find that available data supported the pace-of-life syndrome hypothesis. This suggests that either the hypothesis has been inappropriately tested or is not generally applicable.


Personality Behavioral syndrome Covariation Phenotypic integration 



We thank P.O. Montiglio and D. Réale for important discussions and for directing us to particular studies not identified by our searches. We also thank Julia Bowsher, M. Dammhahn, and three anonymous reviewers for comments provided on an earlier draft of this manuscript. RR was supported by a North Dakota EPSCoR grant to NAD. CRG and MAB were supported by the North Dakota State University Department of Biological Sciences.

Supplementary material

265_2018_2472_MOESM1_ESM.docx (672 kb)
ESM 1 (DOCX 671 kb)


  1. Adriaenssens B, Johnsson JI (2009) Personality and life-history productivity: consistent or variable association? Trends Ecol Evol 24:179–180CrossRefPubMedGoogle Scholar
  2. Adriaenssens B, Johnsson JI (2010) Shy trout grow faster: exploring links between personality and fitness-related traits in the wild. Behav Ecol 22:135–143CrossRefGoogle Scholar
  3. Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473CrossRefPubMedGoogle Scholar
  4. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834CrossRefPubMedGoogle Scholar
  5. Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368CrossRefPubMedGoogle Scholar
  6. Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25:653–659CrossRefPubMedGoogle Scholar
  7. Carducci JP, Jakob EM (2000) Rearing environment affects behaviour of jumping spiders. Anim Behav 59:39–46CrossRefPubMedGoogle Scholar
  8. Careau V, Bininda-Emonds O, Thomas D, Réale D, Humphries M (2009) Exploration strategies map along fast–slow metabolic and life-history continua in muroid rodents. Funct Ecol 23:150–156CrossRefGoogle Scholar
  9. Careau V, Garland T (2012) Performance, personality, and energetics: correlation, causation, and mechanism. Physiol Biochem Zool 85:543–571CrossRefPubMedGoogle Scholar
  10. Careau V, Montiglio P-O, Garant D, Pelletier F, Speakman JR, Humphries MM, Réale D (2015) Energy expenditure and personality in wild chipmunks. Behav Ecol Sociobiol 69:653–661CrossRefGoogle Scholar
  11. Careau V, Réale D, Humphries MM, Thomas DW (2010) The pace of life under artificial selection: personality, energy expenditure, and longevity are correlated in domestic dogs. Am Nat 175:753–758CrossRefPubMedGoogle Scholar
  12. Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117:641–653CrossRefGoogle Scholar
  13. Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R (2013) Animal personality: what are behavioural ecologists measuring? Biol Rev 88:465–475CrossRefPubMedGoogle Scholar
  14. Dammhahn M, Almeling L (2012) Is risk taking during foraging a personality trait? A field test for cross-context consistency in boldness. Anim Behav 84:1131–1139CrossRefGoogle Scholar
  15. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54CrossRefPubMedGoogle Scholar
  16. Dingemanse NJ, Dochtermann NA, Nakagawa S (2012) Defining behavioural syndromes and the role of ‘syndrome deviation’ in understanding their evolution. Behav Ecol Sociobiol 66:1543–1548CrossRefGoogle Scholar
  17. Dingemanse NJ, Wright J, Kazem AJ, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138CrossRefPubMedGoogle Scholar
  18. Dochtermann NA, Nelson AB (2014) Multiple facets of exploratory behavior in house crickets (Acheta domesticus): split personalities or simply different behaviors? Ethology 120:1110–1117CrossRefGoogle Scholar
  19. Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634Google Scholar
  20. Engqvist L, Cordes N, Reinhold K (2015) Evolution of risk-taking during conspicuous mating displays. Evolution 69:395–406CrossRefPubMedGoogle Scholar
  21. Galliard JF, Paquet M, Cisel M, Montes-Poloni L (2013) Personality and the pace-of-life syndrome: variation and selection on exploration, metabolism and locomotor performances. Funct Ecol 27:136–144CrossRefGoogle Scholar
  22. Hämäläinen A, Immonen E, Tarka M, Schuett W (2018) Evolution of sex-specific pace-of-life syndromes. Behav Ecol Sociobiol.
  23. Krams I, Kivleniece I, Kuusik A, Krama T, Freeberg TM, Mänd R, Sivacova L, Rantala MJ, Mänd M (2014a) High repeatability of anti-predator responses and resting metabolic rate in a beetle. J Insect Behav 27:57–66CrossRefGoogle Scholar
  24. Krams IA, Vrublevska J, Sepp T, Abolins-Abols M, Rantala MJ, Mierauskas P, Krama T (2014b) Sex-specific associations between nest defence, exploration and breathing rate in breeding pied flycatchers. Ethology 120:492–501CrossRefGoogle Scholar
  25. Letunic I (2015) phyloT : Phylogenetic Tree Generator. [online] Available at:
  26. Mathot KJ, Frankenhuis WE (2018) Models of pace-of-life syndromes (POLS): a systematic review. Behav Ecol Sociobiol.
  27. Mathot KJ, Nicolaus M, Araya-Ajoy YG, Dingemanse NJ, Kempenaers B (2015) Does metabolic rate predict risk-taking behaviour? A field experiment in a wild passerine bird. Funct Ecol 29:239–249CrossRefGoogle Scholar
  28. Montiglio PO, Dammhahn M, Dubuc Messier G, Réale D (2018) The pace-of-life syndrome hypothesis: evidence, limitations and future directions. Behav Ecol Sociobiol. (in press)Google Scholar
  29. Montiglio P-O, Garant D, Thomas D, Réale D (2010) Individual variation in temporal activity patterns in open-field tests. Anim Behav 80:905–912CrossRefGoogle Scholar
  30. Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605CrossRefPubMedGoogle Scholar
  31. Nakagawa S, Santos ES (2012) Methodological issues and advances in biological meta-analysis. Evol Ecol 26:1253–1274CrossRefGoogle Scholar
  32. Niemelä PT, Vainikka A, Hedrick AV, Kortet R (2012) Integrating behaviour with life history: boldness of the field cricket, Gryllus integer, during ontogeny. Funct Ecol 26:450–456CrossRefGoogle Scholar
  33. Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio P-O (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos T Roy Soc B 365:4051–4063CrossRefGoogle Scholar
  34. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318CrossRefPubMedGoogle Scholar
  35. Reznick DN, Butler MJ IV, Rodd FH, Ross P (1996) Life-history evolution in guppies (Poecilia reticulata) 6. Differential mortality as a mechanism for natural selection. Evolution 50:1651–1660PubMedGoogle Scholar
  36. Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468CrossRefGoogle Scholar
  37. Royauté R, Berdal MA, Garrison CR, Dochtermann NA (2018) Data from: Paceless life? A meta-analysis of the pace-of-life syndrome hypothesis. Dryad Digital Repository,
  38. Royauté R, Buddle CM, Vincent C (2015b) Under the influence: sublethal exposure to an insecticide affects personality expression in a jumping spider. Funct Ecol 29:962–970CrossRefGoogle Scholar
  39. Royauté R, Dochtermann NA (2017) When the mean no longer matters: developmental diet affects behavioral variation but not population averages in the house cricket (Acheta domesticus). Behav Ecol 28:337–345CrossRefGoogle Scholar
  40. Royauté R, Greenlee K, Baldwin M, Dochtermann NA (2015a) Behaviour, metabolism and size: phenotypic modularity or integration in Acheta domesticus? Anim Behav 110:163–169CrossRefGoogle Scholar
  41. Salzman TC, McLaughlin AL, Westneat DF, Crowley PH (2018) Energetic trade-offs and feedbacks between behavior and metabolism influence correlations between pace-of-life attributes. Behav Ecol Sociobiol.
  42. Santostefano F, Wilson AJ, Niemelä PT, Dingemanse NJ (2017) Behavioural mediators of genetic life-history trade-offs: a test of the pace-of-life syndrome hypothesis in field crickets. Proc R Soc B 284:20171567CrossRefPubMedGoogle Scholar
  43. Shearer TA, Pruitt JN (2014) Individual differences in boldness positively correlate with heart rate in orb-weaving spiders of genus Larinioides. Curr Zool 60:387–391CrossRefGoogle Scholar
  44. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an intergrative overiew. Q Rev Biol 79:241–277CrossRefPubMedGoogle Scholar
  45. Sinervo B, Svensson E (2002) Correlational selection and the evolution of genomic architecture. Heredity 89:329–338CrossRefPubMedGoogle Scholar
  46. Tieleman BI (2009) High and low, fast or slow: the complementary contributions of altitude and latitude to understand life-history variation. J Anim Ecol 78:293–295CrossRefPubMedGoogle Scholar
  47. Tieleman BI, Williams JB, Ricklefs RE, Klasing KC (2005) Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proc R Soc Lond B 272:1715–1720CrossRefGoogle Scholar
  48. Uher J (2011) Individual behavioral phenotypes: an integrative meta-theoretical framework. Why “behavioral syndromes” are not analogs of “personality”. Dev Psychobiol 53:521–548CrossRefPubMedGoogle Scholar
  49. van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142CrossRefGoogle Scholar
  50. Viechtbauer W (2010) Conducting meta-analyses in with the package. J Stat Softw 36(3):1–48Google Scholar
  51. Vincze E, Seress G, Lagisz M, Nakagawa S, Dingemanse N, Sprau P (2017) Does urbanization affect predation of bird nests? A meta-analysis. Front Ecol Evol 5:29CrossRefGoogle Scholar
  52. Wiersma P, Muñoz-Garcia A, Walker A, Williams JB (2007) Tropical birds have a slow pace of life. P Natl Acad Sci USA 104:9340–9345CrossRefGoogle Scholar
  53. Wikelski M, Spinney L, Schelsky W, Scheuerlein A, Gwinner E (2003) Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes. Proc R Soc Lond B 270:2383–2388CrossRefGoogle Scholar
  54. Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Raphaël Royauté
    • 1
  • Monica Anderson Berdal
    • 1
  • Courtney R. Garrison
    • 1
  • Ned A. Dochtermann
    • 1
    Email author
  1. 1.Department of Biological SciencesNorth Dakota State UniversityFargoUSA

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