Skip to main content
SpringerLink
Log in

Phenotypic correlations capture between-individual correlations underlying behavioral syndromes

  • Methods Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

The presence of variation in behavior on the between-individual level is considered the hallmark of personality. In contrast, behavioral syndromes are commonly recognized when documented on the phenotypic level, which is a mix of between-individual and residual (within-individual) correlations. Phenotypic and between-individual correlations need not align, and investigations on different levels of the same syndrome may hence lead to opposite inferences. Between-individual correlations, arguably, provide stronger evidence for an intrinsically determined behavioral syndrome than phenotypic correlations. We compiled 109 literature estimates of between-individual and phenotypic correlations between behaviors from 30 studies, performed on 22 species covering a wide range of taxa. Contrary to our expectation, the phenotypic correlation in behaviors was, on average, a reasonable predictor of the between-individual correlation in terms of magnitude and sign. Although our finding does not warrant the use of the phenotypic correlation as a suitable approximation of the between-individual correlation for any particular study, it does suggest that the phenotypic correlations used to infer the majority of behavioral syndromes to date have provided a reasonable characterization of syndrome associative strength.

Significance statement

Aspects of personality often correlate and are then said to form a behavioral syndrome. Syndromes are interesting because they signal that multiple behaviors may share causal drivers. Most syndromes to date are based on correlations of measured behaviors (phenotypes), but any pattern on the phenotypic level is likely influenced by uncontrolled associations between the focal behaviors which are expected to reduce the phenotypic correlation relative to the correlation on the underlying individual level. If so, behavioral ecologists may have underestimated the associative strength of behavioral syndromes. Based on over 100 published estimates of individual-level and phenotypic correlations between aspects of personality, we show that the phenotypic correlation provides a reasonable estimate of the magnitude and sign of individual-level correlations.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Araya-Ajoy YG, Dingemanse NJ (2014) Characterizing behavioural “characters”: an evolutionary framework. Proc R Soc B 281:20132645

    Article  PubMed  PubMed Central  Google Scholar 

  • Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behavior: a meta-analysis. Anim Behav 77:771–783

    Article  PubMed  PubMed Central  Google Scholar 

  • Bierbach D, Sommer-Trembo C, Hanisch J, Wolf M, Plath M (2015) Personality affects mate choice: bolder males show stronger audience effects under high competition. Behav Ecol 26:1314–1325

    Article  Google Scholar 

  • Blumstein DT, Lea AJ, Olson LE, Martin JGA (2010) Heritability of anti-predatory traits: vigilance and locomotor performance in marmots. J Evol Biol 23:879–887

    Article  CAS  PubMed  Google Scholar 

  • Boulton K, Couto E, Grimmer AJ, Early RL, Canario AVM, Wilson AJ, Walling CA (2015) How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model. Ecol Evol 5:618–633

    Article  PubMed  PubMed Central  Google Scholar 

  • Brommer JE (2013) On between-individual and residual (co) variances in the study of animal personality: are you willing to take the “individual gambit”? Behav Ecol Sociobiol 67:1027–1032

    Article  Google Scholar 

  • Careau V, Montiglio PO, Garant D, Pelletier F, Speakman JR, Humphries MM, Réale D (2015) Energy expenditure and personality in wild chipmunks. Behav Ecol Sociobiol 69:653–661

    Article  Google Scholar 

  • Cheverud JM (1988) A comparison of genetic and phenotypic correlations. Evolution 42:958–968

    Article  Google Scholar 

  • Class B, Kluen E, Brommer JE (2014) Evolutionary quantitative genetics of behavioral responses to handling in a wild passerine. Ecol Evol 4:427–440

    Article  PubMed  PubMed Central  Google Scholar 

  • Cordes N, Engqvist L, Schmoll T, Reinhold K (2014) Sexual signaling under predation: attractive moths take the greater risks. Behav Ecol 25:409–414

    Article  Google Scholar 

  • Diamond K, Trovillion D, Allen KE, Malela KM, Noble DA, Powell R, Eifler DA, Gifford ME (2014) Individual (co)variation of field behavior and locomotor performance in curly tailed lizards. J Zool 294:248–254

    Article  Google Scholar 

  • Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54

    Article  PubMed  Google Scholar 

  • Dingemanse NJ, Dochtermann NA (2014) Individual behaviour: behavioural ecology meets quantitative genetics. In: Charmantier A, Garant D, Kruuk LEB (eds) Quantitative genetics in the wild. Oxford University Press, Oxford, pp 54–65

    Chapter  Google Scholar 

  • Dingemanse NJ, Dochtermann NA, Nakagawa S (2012) Defining behavioural syndromes and the role of “syndrome deviation” in understanding their evolution. Behav Ecol Sociobiol 66:1543–1548

    Article  Google Scholar 

  • Dochtermann NA (2011) Testing Cheverud’s conjecture for behavioral correlations and behavioral syndromes. Evolution 65:1814–1820

    Article  PubMed  Google Scholar 

  • Dosmann AJ, Brooks KC, Mateo JM (2015) Within-individual correlations reveal link between a behavioral syndrome, condition, and cortisol in free-ranging Belding’s ground squirrels. Ethology 121:125–134

    Article  PubMed  Google Scholar 

  • Ferrari C, Pasquaretta C, Carere C, Cavallone E, von Hardenberg A, Réale D (2013) Testing for the presence of coping styles in a wild mammal. Anim Behav 85:1385–1396

    Article  Google Scholar 

  • Fisher DN, James A, Rodríguez-Muñoz R, Tregenza T (2015) Behaviour in captivity predicts some aspects of natural behaviour, but not others, in a wild cricket population. Proc R Soc B 282:20150708

    Article  PubMed  PubMed Central  Google Scholar 

  • Fresneau N, Kluen E, Brommer JE (2014) A sex-specific behavioral syndrome in a wild passerine. Behav Ecol 25:359–367

    Article  Google Scholar 

  • Garamszegi LZ, Eens M, Török J (2009) Behavioural syndromes and trappability in free-living collared flycatchers, Ficedula albicollis. Anim Behav 77:803–812

    Article  Google Scholar 

  • Garamszegi LZ, Markó G, Herczeg G (2012) A meta-analysis of correlated behaviours with implications for behavioural syndromes: mean effect size, publication bias, phylogenetic effects and the role of mediator variables. Evol Ecol 26:1213–1235

    Article  Google Scholar 

  • Garamszegi LZ, Markó G, Herczeg G (2013) A meta-analysis of correlated behaviors with implications for behavioral syndromes: relationships between particular behavioral traits. Behavioral Ecology 24:1068–1080

  • Geffroy B, Sadoul B, Bardonnet A (2015) Behavioural syndrome in juvenile eels and its ecological implications. Behaviour 152:147–166

    Article  Google Scholar 

  • Gifford ME, Clay TA, Careau V (2014) Individual (co)variation in standard metabolic rate, feeding rate, and exploratory behavior in wild-caught semiaquatic salamanders. Physiol Biochem Zool 87:384–396

    Article  PubMed  Google Scholar 

  • Gilmour AR, Gogel BJ, Cullis BR, Thompson R, Butler D (2009) ASReml user guide release 3.0. VSN International Ltd, Hemel Hempstead, UK

  • Grafen A (1984) Natural selection, kin selection and group selection. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Scientific, Oxford

    Google Scholar 

  • Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22

    Article  Google Scholar 

  • Hall ML, van Asten T, Katsis AC, Dingemanse NJ, Magrath MJ, Mulder RA (2015) Animal personality and pace-of-life syndromes: do fast-exploring fairy-wrens die young? Front Ecol Evol 3:28

    Google Scholar 

  • Han CS, Jäger HY, Dingemanse NJ (2016) Individuality in nutritional preferences: a multi-level approach in field crickets. Sci Rep 6:29071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison PM, Gutowsky LFG, Martins EG, Patterson DA, Cooke SJ, Power M (2015) Personality-dependent spatial ecology occurs independently from dispersal in wild burbot (Lota lota). Behav Ecol 26:483–492

    Article  Google Scholar 

  • Horváth G, Martín J, López P, Garamszegi LZ, Bertók P, Herczeg G (2016) Blood parasite infection intensity covaries with risk-taking personality in male Carpetan rock lizards (Iberolacerta cyreni). Ethology 122:355–363

    Article  Google Scholar 

  • Kim SY, Velando A (2015) Phenotypic integration between antipredator behavior and camouflage pattern in juvenile sticklebacks. Evolution 69:830–838

    Article  PubMed  Google Scholar 

  • Kluen E, Siitari H, Brommer JE (2014) Testing for between individual correlations of personality and physiological traits in a wild bird. Behav Ecol Sociobiol 68:205–213

    Article  Google Scholar 

  • Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neuroscience and Biobehavioral Reviews 23:925–935

  • Laskowski KL, Bell AM (2013) Competition avoidance drives individual differences in response to a changing food resource in sticklebacks. Ecol Lett 16:746–753

    Article  PubMed  PubMed Central  Google Scholar 

  • Lea AJ, Blumstein DT, Wey TW, Martin JGA (2010) Heritable victimization and the benefits of agonistic relationships. P Natl Acad Sci USA 107:21587–21592

    Article  CAS  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates

  • Mcevoy J, While GM, Sinn DL, Carver S, Wapstra E (2015) Behavioural syndromes and structural and temporal consistency of behavioural traits in a social lizard. J Zool 296:58–66

    Article  Google Scholar 

  • Niemelä PT, Lattenkamp EZ, Dingemanse NJ (2015) Personality-related survival and sampling bias in wild cricket nymphs. Behav Ecol 26:936–946

    Article  Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall P, Dingemanse NJ (2007) Integrating temperament in ecology and evolutionary biology. Biol Rev 82:291–318

    Article  PubMed  Google Scholar 

  • Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio PO (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos T Roy Soc B 365:4051–4063

    Article  Google Scholar 

  • Royauté R, Greenlee K, Baldwin M, Dochtermann NA (2015a) Behaviour, metabolism and size: phenotypic modularity or integration in Acheta domesticus? Anim Behav 110:163–169

    Article  Google Scholar 

  • Royauté R, Buddle CM, Vincent C (2015b) Under the influence: sublethal exposure to an insecticide affects personality expression in a jumping spider. Funct Ecol 29:962–970

    Article  Google Scholar 

  • Sanderson JL, Stott I, Young AJ, Vitikainen EI, Hodge SJ, Cant MA (2015) The origins of consistent individual differences in cooperation in wild banded mongooses, Mungos mungo. Anim Behav 107:193–200

    Article  Google Scholar 

  • Santostefano F, Wilson AJ, Araya-Ajoy YG, Dingemanse NJ (2016) Interacting with the enemy: indirect effects of personality on conspecific aggression in crickets. Behav Ecol 27:1235–1246

    Article  Google Scholar 

  • Searle SR (1961) Phenotypic, genetic, and environmental correlations. Biometrics 17:474–480

    Article  Google Scholar 

  • Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277

    Article  PubMed  Google Scholar 

  • Stein LR, Bell AM (2015) Consistent individual differences in paternal behavior: a field study of three-spined stickleback. Behav Ecol Sociobiol 69:227–236

    Article  PubMed  Google Scholar 

  • Urszán TJ, Garamszegi LZ, Nagy G, Hettyey A, Török J, Herczeg G (2015) No personality without experience? A test on Rana dalmatina tadpoles. Ecol Evol 5:5847–5856

    Article  PubMed  PubMed Central  Google Scholar 

  • Westneat DF, Wright J, Dingemanse NJ (2015) The biology hidden inside residual within-individual phenotypic variation. Biol Rev 90:729–743

    Article  PubMed  Google Scholar 

  • Zar JH (2010) Biostatistical analysis. Prenton Hall, Upper Saddle River, NJ

    Google Scholar 

Download references

Acknowledgements

We thank Alexander Weiss for an invitation which proved to be the initiation of this work. Two anonymous reviewers and the associate editor are thanked for constructive comments which clearly improved the paper.

Author information

Authors and Affiliations

  1. Department of Biology, University of Turku, University Hill, FI-20014, Turku, Finland

    Jon E. Brommer & Barbara Class

  2. Novia University of Applied Sciences, Campus Raseborg, Raseborgsvägen 9, FI-10600, Ekenäs, Finland

    Jon E. Brommer

Authors
  1. Jon E. Brommer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Barbara Class
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jon E. Brommer.

Ethics declarations

This work is a compilation of published work performed on animals, and the ethical considerations of working with experimental animals have been detailed in the original publications cited in this paper. This work does not include research on humans or primates.

Funding

The study was financially supported by funding from the Academy of Finland (to JEB) and the Graduate School in Biology, Geography and Geology (to BC).

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by N. A. Dochtermann

Electronic supplementary material

ESM 1

(XLSX 40 kb).

ESM 2

(DOCX 56 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brommer, J.E., Class, B. Phenotypic correlations capture between-individual correlations underlying behavioral syndromes. Behav Ecol Sociobiol 71, 50 (2017). https://doi.org/10.1007/s00265-017-2278-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-017-2278-4

Keywords

Search

Navigation