Abstract
Behavioural ageing patterns can vary among individuals and can predict long-term changes in the extent of among-individual variation in behaviour, resulting in age-related changes in behavioural repeatability. Understanding how repeatability changes with age is important because it offers insight into the age-specific evolvability of a trait. However, age-related alterations in behavioural repeatability can also stem from changes in within-individual behavioural variation. Nevertheless, little is known about the roles of among- and within-individual behavioural variation in age-related changes in behavioural repeatability. In this study, we repeatedly measured mating attempts of individual male water striders (Gerris lacustris) at different times and estimated individual patterns of behavioural ageing as well as age-related changes in within- and among-individual behavioural variation. We found a decline in mating attempts with age in male water striders. Additionally, individual males exhibited diverse behavioural ageing patterns, resulting in varying ranks with age and consistent among-individual variation in mating attempts. Conversely, within-individual variation in mating attempts decreased with age, leading to increased repeatability. This increased repeatability may arise from reduced mating behaviour flexibility or a decline in the maximum number of mating attempts with age. Therefore, we emphasise the importance of within-individual behavioural variation in age-related changes in repeatability, independent of changes in among-individual behavioural variation.
Significance statement
Despite considerable research on age-related phenotypic changes, little attention has been given to individual-level analyses of behavioural changes with age. Here, we show that male water striders decrease their mating attempts with age and also exhibit variation in how their behaviour changes with age. The extent of individual differences in mating attempts was unchanged with age, but the extent of within-individual variation in mating attempts decreased. This pattern results in an age-related increase in behavioural repeatability. Thus, we suggest that age-related changes in behavioural variation should be considered when predicting behavioural evolution.
Similar content being viewed by others
Data availability
All data are available at https://shorturl.at/imqHZ.
References
Arnqvist G (1997) The evolution of water strider mating systems: causes and consequences of sexual conflicts. In: Choe JC, Crespi BJ (eds) The Evolution of Mating Systems in Insects and Arachnids. Cambridge University Press, Cambridge, pp 146–163
Atwell A, Wagner WE Jr (2014) Female mate choice plasticity is affected by the interaction between male density and female age in a field cricket. Anim Behav 98:177–183
Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368
Bonduriansky R, Brassil C (2005) Reproductive ageing and sexual selection on male body size in a wild population of antler flies (Protopiophila litigata). J Evol Biol 18:1332–1340
Bonner S, Kim H-N, Westneat D, Mutzel A, Wright J, Schofield M (2021) dalmatian: a package for fitting double hierarchical linear models in R via JAGS and nimble. J Stat Softw 100:1–25
Brand JA, Henry J, Melo GC, Wlodkowic D, Wong BB, Martin JM (2023) Sex differences in the predictability of risk-taking behavior. Behav Ecol 34:108–116
Briffa M, Bridger D, Biro PA (2013) How does temperature affect behaviour? Multilevel analysis of plasticity, personality and predictability in hermit crabs. Anim Behav 86:47–54
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
Brommer JE, Class B (2015) The importance of genotype-by-age interactions for the development of repeatable behavior and correlated behaviors over lifetime. Front Zool 12:1
Cain S, Solomon T, Leshem Y, Toledo S, Arnon E, Roulin A, Spiegel O (2023) Movement predictability of individual barn owls facilitates estimation of home range size and survival. Mov Ecol 11:10
Charmantier A, Brommer JE, Nussey DH (2014) The quantitative genetics of senescence in wild animals. In: Charmantier A, Garant D, Kruuk LEB (eds) Quantitative genetics in the wild. Oxford University Press, Oxford, pp 68–83
Churchill ER, Dytham C, Thom MD (2019) Differing effects of age and starvation on reproductive performance in Drosophila melanogaster. Sci Rep 9:1–8
Cleasby IR, Nakagawa S, Schielzeth H (2015) Quantifying the predictability of behaviour: statistical approaches for the study of between-individual variation in the within-individual variance. Methods Ecol Evol 6:27–37
Cotter SC, Ward RJ, Kilner RM (2011) Age-specific reproductive investment in female burying beetles: independent effects of state and risk of death. Funct Ecol 25:652–660
Danielsson I (2001) Antagonistic pre-and post-copulatory sexual selection on male body size in a water strider (Gerris lacustris). Proc R Soc Lond B 268:77–81
Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93
Dewsbury DA (1981) Effects of novelty of copulatory behavior: the Coolidge effect and related phenomena. Psychol Bull 89:464
Dochtermann NA, Schwab T, Sih A (2015) The contribution of additive genetic variation to personality variation: heritability of personality. Proc R Soc Lond B 282:20142201
Fairbairn DJ, Vermette R, Kapoor NN, Zahiri N (2003) Functional morphology of sexually selected genitalia in the water strider Aquarius remigis. Can J Zool 81:400–413
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Prentice Hall, London
Fischer B, van Doorn GS, Dieckmann U, Taborsky B (2014) The evolution of age-dependent plasticity. Am Nat 183:108–125
Gray DA (1999) Intrinsic factors affecting female choice in house crickets: time cost, female age, nutritional condition, body size, and size-relative reproductive investment. J Insect Behav 12:691–700
Han CS, Brooks RC (2013a) Correlational selection does not explain the evolution of a behavioral syndrome. J Evol Biol 26:2260–2270
Han CS, Brooks RC (2013b) Evolution of individual variation in behaviour and behavioural plasticity under scramble competition. Anim Behav 86:435–442
Han CS, Brooks RC (2014) Long-term effect of social interactions on behavioral plasticity and lifetime mating success. Am Nat 183:431–444
Han CS, Brooks RC (2015a) The interaction between genotype and juvenile and adult density environment in shaping multidimensional reaction norms of behaviour. Funct Ecol 29:78–87
Han CS, Brooks RC (2015b) Same-sex sexual behaviour as a by-product of reproductive strategy under male-male scramble competition. Anim Behav 108:193–197
Han CS, Jablonski PG, Kim B, Park F (2010) Size-assortative mating and sexual size dimorphism are predictable from simple mechanics of mate-grasping behavior. BMC Evol Biol 10:359
Han CS, Santostefano F, Dingemanse NJ (2016) Do social partners affect same-sex sexual behaviour in male water striders? Anim Behav 116:53–59
Hertel AG, Royauté R, Zedrosser A, Mueller T (2021) Biologging reveals individual variation in behavioural predictability in the wild. J Anim Ecol 90:723–737
Hooper AK, Lehtonen J, Schwanz LE, Bonduriansky R (2018) Sexual competition and the evolution of condition-dependent ageing. Evol Lett 2:37–48
Houslay TM, Kitchener PA, Royle NJ (2020) Are older parents less flexible? Testing age-dependent plasticity in Nicrophorus vespilloides burying beetles. Anim Behav 162:79–86
Houston AI, McNamara JM (1999) Models of adaptive behaviour: an approach based on state. Cambridge University Press
Hyun H, Han CS (2021) Morph-specific life-history correlations in a wing-dimorphic water strider. J Evol Biol 34:1340–1346
Jäger HY, Han CS, Dingemanse NJ (2019) Social experiences shape behavioral individuality and within-individual stability. Behav Ecol 30:1012–1019
Jolles JW, Briggs HD, Araya-Ajoy YG, Boogert NJ (2019) Personality, plasticity and predictability in sticklebacks: bold fish are less plastic and more predictable than shy fish. Anim Behav 154:193–202
Kasumovic MM, Hall MD, Brooks RC (2012) The juvenile social environment introduces variation in the choice and expression of sexually selected traits. Ecol Evol 2:1036–1047
Kok EM, Burant JB, Dekinga A, Manche P, Saintonge D, Piersma T, Mathot KJ (2019) Within-individual canalization contributes to age-related increases in trait repeatability: a longitudinal experiment in red knots. Am Nat 194:455–469
Laskowski KL, Moiron M, Niemelä P (2021) Integrating behavior in life-history theory: allocation versus acquisition? Trends Ecol Evol 36:132–138
Lauer MJ (1996) Effect of sperm depletion and starvation on female mating behavior in the water strider, Aquarius remigis. Behav Ecol Sociobiol 38:89–96
Lee Y, Nelder JA (2006) Double hierarchical generalized linear models (with discussion). J Roy Stat Soc Ser C (Appl Stat) 55:139–185
Mautz BS, Sakaluk SK (2008) The effects of age and previous mating experience on pre-and post-copulatory mate choice in female house crickets (Acheta domesticus L.). J Insect Behav 21:203–212
Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142
Niemelä PT, Niehoff PP, Gasparini C, Dingemanse NJ, Tuni C (2019) Crickets become behaviourally more stable when raised under higher temperatures. Behav Ecol Sociobiol 73:1–12
Nussey D, Wilson A, Brommer J (2007) The evolutionary ecology of individual phenotypic plasticity in wild populations. J Evol Biol 20:831–844
Nussey DH, Froy H, Lemaitre J-F, Gaillard J-M, Austad SN (2013) Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res Rev 12:214–225
O'Dea RE, Noble DW, Nakagawa S (2022) Unifying individual differences in personality, predictability and plasticity: a practical guide. Methods Ecol Evol 13:278–293
Occhiuto F, Vázquez-Diosdado JA, Carslake C, Kaler J (2022) Personality and predictability in farmed calves using movement and space-use behaviours quantified by ultra-wideband sensors. R Soc Open Sci 9:212019
Ortigosa A, Rowe L (2003) The effect of hunger on mating behaviour and sexual selection for male body size in Gerris buenoi. Anim Behav 64:369–375
Pervez A, Richmond AS (2004) The influence of age on reproductive performance of the predatory ladybird beetle, Propylea dissecta. J Insect Sci 4:22
Pinheiro J, Bates D (2006) Mixed-effects models in S and S-PLUS. Springer, New York
Polverino G, Cigliano C, Nakayama S, Mehner T (2016) Emergence and development of personality over the ontogeny of fish in absence of environmental stress factors. Behav Ecol Sociobiol 70:2027–2037
Preziosi RF, Fairbairn DJ (1997) Sexual size dimorphism and selection in the wild in the waterstrider Aquarius remigis: lifetime fecundity selection on female total length and its components. Evolution 51:467–474
Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267
Richard M, Lecomte J, De Fraipont M, Clobert J (2005) Age-specific mating strategies and reproductive senescence. Mol Ecol 14:3147–3155
Rodríguez-Muñoz R, Hopwood P, Fisher D, Skicko I, Tucker R, Woodcock K, Slate J, Walling C, Tregenza T (2019) Older males attract more females but get fewer matings in a wild field cricket. Anim Behav 153:1–14
Self SG, Liang K-Y (1987) Asymptotic properties of maximum likelihood estimators and likelihood ratio tests under nonstandard conditions. J Am Stat Assoc 82:605–610
Sih A, Watters J (2005) The mix matters: behavioural types and group dynamics in water striders. Behaviour 142(9):1417–1431
Sih A, Mathot KJ, Moirón M, Montiglio P-O, Wolf M, Dingemanse NJ (2015) Animal personality and state–behaviour feedbacks: a review and guide for empiricists. Trends Ecol Evol 30:50–60
Spence JR, Andersen NM (1994) Biology of water striders: interactions between systematics and ecology. Annu Rev Entomol 39:101–128
Stamps JA (2016) Individual differences in behavioural plasticities. Biol Rev 91:534–567
Stamps JA, Biro PA (2016) Personality and individual differences in plasticity. Curr Opin Behav Sci 12:18–23
Stamps JA, Briffa M, Biro PA (2012) Unpredictable animals: individual differences in intraindividual variability (IIV). Anim Behav 83:1325–1334
Thomas ML (2011) Detection of female mating status using chemical signals and cues. Biol Rev 86:1–13
Thys B, Pinxten R, Eens M (2021) Long-term repeatability and age-related plasticity of female behaviour in a free-living passerine. Anim Behav 172:45–54
van de Pol M, Verhulst S (2006) Age-dependent traits: a new statistical model to separate within- and between-individual effects. Am Nat 167:766–773
van de Pol M, Wright J (2009) A simple method for distinguishing within-versus between-subject effects using mixed models. Anim Behav 77:753–758
Visscher PM (2006) A note on the asymptotic distribution of likelihood ratio tests to test variance components. Twin Res Hum Genet 9:490–495
Westneat DF, Schofield M, Wright J (2013) Parental behavior exhibits among-individual variance, plasticity, and heterogeneous residual variance. Behav Ecol 24:598–604
Westneat DF, Wright J, Dingemanse NJ (2015) The biology hidden inside residual within-individual phenotypic variation. Biol Rev 90:729–743
Wilson AJ, Reale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LE, Nussey DH (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26
Winney IS, Schroeder J, Nakagawa S, Hsu YH, Simons MJ, Sánchez-Tójar A, Mannarelli ME, Burke T (2018) Heritability and social brood effects on personality in juvenile and adult life-history stages in a wild passerine. J Evol Biol 31:75–87
Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584
Acknowledgements
We thank two anonymous reviewers for improving earlier versions of the manuscript.
Funding
This work was supported by a Basic Science Research Program grant through the National Research Foundation of Korea (NRF-2022R1C1C1004303) to CSH.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
We declare that we have no competing interests.
Additional information
Communicated by D. J Hosken
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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.
About this article
Cite this article
Han, C.S., Dingemanse, N.J. Age-related reductions in within-individual variation increase the repeatability of mating behaviour. Behav Ecol Sociobiol 77, 94 (2023). https://doi.org/10.1007/s00265-023-03368-w
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-023-03368-w