in

Selection and genetic variation in age-related plasticity drive the erosion of among-individual behavioural correlations in later life


Abstract

Among-individual correlations between labile traits stem from either shared genetic architectures or developmental processes that shape trait expression. While these correlations have been extensively studied in behavioural ecology over the past two decades, the specific mechanisms driving age-related changes in among-individual trait correlations remain unclear. Given that trait correlations can significantly constrain or facilitate evolutionary trajectories, identifying how these associations—and their underlying genetic basis—evolve with age is essential for accurately predicting evolutionary responses alongside age-specific selection. Here, using field cricket Gryllus bimaculatus males from a pedigreed population, we investigated how age-related changes in (1) genetic and (2) nongenetic bases of among-individual aggression-exploration correlations, as well as (3) survival selection, explain age-related variation in an aggression-exploration correlations. Our findings indicate that the magnitudes of both the positive among-individual and genetic correlations were maintained across nymph and young adult stages, but significantly decreased with age during adulthood. This decrease was due to both survival selection and genetic variation in age-related behavioural plasticity. Survival selection tended to favour less explorative males at the young adult stage, which may have eroded the genetic correlations. In addition, genetic variation in age-related plasticity in exploration contributed to a decrease in the magnitude of genetic correlations during the adult stage. The similarity of age-related changes in among-individual and genetic correlations resulted from the absence of short-term permanent environmental correlations. Therefore, the findings of this study suggest that age-related changes in among-individual behavioural correlations are not caused by a single mechanism, but rather a combination of mechanisms, such as genetic variation in age-related behavioural plasticity and survival selection.

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Different scenarios of age-related changes in genetic correlations between labile traits (e.g. behaviours).
Fig. 2: Age-related changes in behavioural variance components across three age categories.
Fig. 3: Age-related changes in correlations.

Similar content being viewed by others

Evolutionary genetics of ageing

Age- and trait-dependent breeding responses to environmental variation in a short-lived songbird

Signatures of repeated genomic selection associated with human-modified landscapes in genetically independent populations of Rhinella horribilis

Data availability

All data are available at https://doi.org/10.6084/m9.figshare.29950505.

References

  • Amat I, Desouhant E, Gomes E, Moreau J, Monceau K (2018) Insect personality: What can we learn from metamorphosis? Curr Opin Insect Sci 27:46–51

    Article 
    PubMed 

    Google Scholar 

  • Anderson BB, Scott A, Dukas R (2016) Social behavior and activity are decoupled in larval and adult fruit flies. Behav Ecol 27(3):820–828

    Article 

    Google Scholar 

  • Bailey NW, Moore AJ (2018) Evolutionary consequences of social isolation. Trends Ecol Evol 33(8):595–607

    Article 
    PubMed 

    Google Scholar 

  • Brommer J, Rattiste K, Wilson A (2010) The rate of ageing in a long-lived bird is not heritable. Heredity 104(4):363

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Brommer JE, Wilson AJ, Gustafsson L (2007) Exploring the genetics of aging in a wild passerine bird. Am Nat 170(4):643–650

    Article 
    PubMed 

    Google Scholar 

  • Campbell DR, Bischoff M, Raguso RA, Briggs HM, Sosenski P (2022) Selection of floral traits by pollinators and seed predators during sequential life history stages. Am Nat 199(6):808–823

    Article 
    PubMed 

    Google Scholar 

  • Chantepie S, Robert A, Sorci G, Hingrat Y, Charmantier A, Leveque G et al. (2015) Quantitative genetics of the aging of reproductive traits in the houbara bustard. PLoS ONE 10(7):e0133140

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Charlesworth B (2001) Patterns of age-specific means and genetic variances of mortality rates predicted by the mutation-accumulation theory of ageing. J Theor Biol 210(1):47–65

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Charmantier A, Perrins C, McCleery RH, Sheldon BC (2006) Quantitative genetics of age at reproduction in wild swans: support for antagonistic pleiotropy models of senescence. Proc Natl Acad Sci USA 103(17):6587–6592

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Class B, Brommer JE (2015) A strong genetic correlation underlying a behavioural syndrome disappears during development because of genotype–age interactions. Proc R Soc Lond B Biol Sci 282(1809):20142777

    Google Scholar 

  • Class B, Brommer JE (2016) Senescence of personality in a wild bird. Behav Ecol Sociobiol 70:733–744

    Article 

    Google Scholar 

  • Class B, Brommer JE, van Oers K (2019) Exploratory behavior undergoes genotype–age interactions in a wild bird. Ecol Evol 9(16):8987–8994

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Crean AJ, Monro K, Marshall DJ (2011) Fitness consequences of larval traits persist across the metamorphic boundary. Evolution 65(11):3079–3089.

    Article 
    PubMed 

    Google Scholar 

  • Dalos J, Royauté R, Hedrick AV, Dochtermann NA (2022) Phylogenetic conservation of behavioural variation and behavioural syndromes. J Evol Biol 35(2):311–321

    Article 
    PubMed 

    Google Scholar 

  • Dammhahn M, Dingemanse NJ, Niemelä PT, Réale D (2018) Pace-of-life syndromes: a framework for the adaptive integration of behaviour. Physiol Life Hist 72:62

    Google Scholar 

  • Dhellemmes F, Finger J-S, Laskowski KL, Guttridge TL, Krause J (2020) Comparing behavioural syndromes across time and ecological conditions in a free-ranging predator. Anim Behav 162:23–33

    Article 

    Google Scholar 

  • Dingemanse NJ, Araya-Ajoy YG, Westneat DF (2021) Most published selection gradients are underestimated: Why this is and how to fix it. Evolution 75(4):806–818

    Article 
    PubMed 

    Google Scholar 

  • Dingemanse NJ, Barber I, Dochtermann NA (2020) Non-consumptive effects of predation: Does perceived risk strengthen the genetic integration of behaviour and morphology in stickleback? Ecol Lett 23(1):107–118

    Article 
    PubMed 

    Google Scholar 

  • Dingemanse NJ, Dochtermann N, Wright J (2010) A method for exploring the structure of behavioural syndromes to allow formal comparison within and between data sets. Anim Behav 79(2):439–450

    Article 

    Google Scholar 

  • Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82(1):39–54

    Article 
    PubMed 

    Google Scholar 

  • Dingemanse NJ, Wolf M (2013) Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim Behav 85(5):1031–1039

    Article 

    Google Scholar 

  • Dochtermann NA, Dingemanse NJ (2013) Behavioral syndromes as evolutionary constraints. Behav Ecol 24(4):806–811

    Article 

    Google Scholar 

  • Edelsparre AH, Vesterberg A, Lim JH, Anwari M, Fitzpatrick MJ (2014) Alleles underlying larval foraging behaviour influence adult dispersal in nature. Ecol Lett 17(3):333–339

    Article 
    PubMed 

    Google Scholar 

  • Fraimout A, Li Z, Sillanpää MJ, Merilä J (2022) Age-dependent genetic architecture across ontogeny of body size in sticklebacks. Proc R Soc B 289(1975):20220352

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

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

    Google Scholar 

  • Han CS, Brooks RC (2014) Long-term effect of social interactions on behavioral plasticity and lifetime mating success. Am Nat 183(3):431–444

    Article 
    PubMed 

    Google Scholar 

  • Han CS, Tuni C, Ulcik J, Dingemanse NJ (2018) Increased developmental density decreases the magnitude of indirect genetic effects expressed during agonistic interactions in an insect. Evolution 72:2435–2448

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Han CS, Yang G (2021) Reproductive aging and pace-of-life syndromes: more active females age faster. Behav Ecol 32(5):926–931

    Article 

    Google Scholar 

  • Hansen, Wheat C, Fitzpatrick JL, Rogell B, Temrin H (2019) Behavioural correlations of the domestication syndrome are decoupled in modern dog breeds. Nat Commun 10(1):2422

    Article 

    Google Scholar 

  • Karlsson, Green K, Eroukhmanoff F, Harris S, Pettersson L, Svensson E (2016) Rapid changes in genetic architecture of behavioural syndromes following colonization of a novel environment. J Evol Biol 29(1):144–152

    Article 

    Google Scholar 

  • Kim SY, Metcalfe NB, Velando A (2016) A benign juvenile environment reduces the strength of antagonistic pleiotropy and genetic variation in the rate of senescence. J Anim Ecol 85(3):705–714

    Article 
    PubMed 

    Google Scholar 

  • Klingenberg CP (2008) Morphological integration and developmental modularity. Annu Rev Ecol Evol Syst 39:115–132

    Article 

    Google Scholar 

  • McGlothlin JW (2010) Combining selective episodes to estimate lifetime nonlinear selection. Evolution 64(5):1377–1385

    PubMed 

    Google Scholar 

  • Mitchell DJ, Houslay TM (2021) Context-dependent trait covariances: how plasticity shapes behavioral syndromes. Behav Ecol 32(1):25–29

    Article 
    PubMed 

    Google Scholar 

  • Nicolaus M, Piault R, Ubels R, Tinbergen JM, Dingemanse NJ (2016) The correlation between colouration and exploration behaviour varies across hierarchical levels in a wild passerine bird. J Evol Biol 29(9):1780–1792

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Niemelä PT, Dingemanse NJ (2017) Individual versus pseudo-repeatability in behaviour: lessons from translocation experiments in a wild insect. J Anim Ecol 86(5):1033–1043

    Article 
    PubMed 

    Google Scholar 

  • Park YH, Shin D, Han CS (2022) Polyandrous females but not monogamous females vary in reproductive ageing patterns in the bean bug Riptortus pedestris. BMC Ecol Evol 22(1):115

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pascoal S, Liu X, Fang Y, Paterson S, Ritchie MG, Rockliffe N et al. (2018) Increased socially mediated plasticity in gene expression accompanies rapid adaptive evolution. Ecol Lett 21(4):546–556

    Article 
    PubMed 

    Google Scholar 

  • Petelle MB, Martin JG, Blumstein DT (2015) Heritability and genetic correlations of personality traits in a wild population of yellow-bellied marmots (Marmota flaviventris). J Evol Biol 28(10):1840–1848

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Pigliucci M (2003) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecol Lett 6(3):265–272

    Article 

    Google Scholar 

  • Pigliucci M, Preston K (2004) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford University Press

  • Polverino G, Buchholz KM, Goulet CT, Michelangeli M, Chapple DG (2023) Temporal repeatability of behaviour in a lizard: implications for behavioural syndrome studies. Evol Ecol 37(3):401–418

    Article 

    Google Scholar 

  • 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 Trans R Soc B 365(1560):4051–4063

    Article 

    Google Scholar 

  • Royauté R, Hedrick A, Dochtermann NA (2020) Behavioural syndromes shape evolutionary trajectories via conserved genetic architecture. Proc R Soc B 287(1927):20200183

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sih A, Bell A, Johnson J, Ziemba R (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79(3):241–277.

    Article 
    PubMed 

    Google Scholar 

  • Sinervo B, Svensson E (2002) Correlational selection and the evolution of genomic architecture. Heredity 89(5):329–338

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Snell-Rood EC (2013) An overview of the evolutionary causes and consequences of behavioural plasticity. Anim Behav 85(8):1004–1011

    Article 

    Google Scholar 

  • Sniegula S, Golab MJ, Drobniak SM, Johansson F (2018) The genetic variance but not the genetic covariance of life-history traits changes towards the north in a time-constrained insect. J Evol Biol 31(6):853–865

    Article 
    PubMed 

    Google Scholar 

  • Styga JM, Houslay TM, Wilson AJ, Earley RL (2019) Development of G: a test in an amphibious fish. Heredity 122(5):696–708

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Tuni C, Han CS, Dingemanse NJ (2018) Multiple biological mechanisms result in correlations between pre- and post-mating traits that differ among versus within individuals and genotypes. Proc R Soc Lond B 285(1885):20180951

    Google Scholar 

  • Watanabe K, Stringer S, Frei O, Umićević Mirkov M, de Leeuw C, Polderman TJ et al. (2019) A global overview of pleiotropy and genetic architecture in complex traits. Nat Genet 51(9):1339–1348

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • White SJ, Pascall DJ, Wilson AJ (2020) Towards a comparative approach to the structure of animal personality variation. Behav Ecol 31(2):340–351

    Article 
    PubMed 

    Google Scholar 

  • Wilson A, Charmantier A, Hadfield J (2008) Evolutionary genetics of ageing in the wild: empirical patterns and future perspectives. Funct Ecol 22(3):431–442

    Article 

    Google Scholar 

  • Wilson AJ, Reale D, Clements MN, Morrissey MM, Postma E, Walling CA et al. (2010) An ecologist’s guide to the animal model. J Anim Ecol 79(1):13–26

    Article 
    PubMed 

    Google Scholar 

Download references

Acknowledgements

CSH is supported by the National Research Foundation of Korea (NRF) grants funded by the Korean government (NRF-2022R1C1C1004303, RS-2024-00405751, RS-2025-16067311, RS-2026-25589531 and RS-2025-25442355). CT and ND were funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation), grant TU 545/2-1 (CT), DI 1694 5–1 (ND), and DI 1694 1–2 (ND).

Author information

Authors and Affiliations

Authors

Contributions

CSH conceived the study, conducted the experiments, analysed the data, and wrote the manuscript; CT conceived the study, conducted the experiments, and wrote the manuscript; ND provided logistics and assisted with data analyses and interpretation and wrote the manuscript.

Corresponding author

Correspondence to
Chang S. Han.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Associate editor: Diala Abu Awad.

Supplementary information

Supplementary Material (download DOCX )

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Cite this article

Han, C.S., Tuni, C. & Dingemanse, N.J. Selection and genetic variation in age-related plasticity drive the erosion of among-individual behavioural correlations in later life.
Heredity (2026). https://doi.org/10.1038/s41437-026-00884-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Version of record:

  • DOI: https://doi.org/10.1038/s41437-026-00884-z


Source: Ecology - nature.com

Broad-scale shift in dominance of arbuscular mycorrhizal trees along the Japanese archipelago associated with tree diseases and climate warming

Biodiversity in deep time