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Adult bacterial exposure increases behavioral variation and drives higher repeatability in field crickets

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Abstract

Among-individual differences in behavior are now a widely studied research focus within the field of behavioral ecology. Furthermore, elements of an animal’s internal state, such as energy or fat reserves, and infection status can have large impacts on behaviors. Despite this, we still know little regarding how state may affect the expression of behavioral variation. Recent exposure to pathogens may have a particularly large impact on behavioral expression given that it likely activates costly immune pathways, potentially forcing organisms to make behavioral tradeoffs. In this study, we investigate how recent exposure to a common bacterial pathogen, Serratia marcescens, affects both the mean behavioral expression and the among-individual differences (i.e., variation) in boldness behavior in the field cricket, Gryllus integer. We find that recent pathogen exposure does not affect mean behavioral expression of the treatment groups, but instead affects behavioral variation and repeatability. Specifically, bacterial exposure drove large among-individual variation, resulting in high levels of repeatability in some aspects of boldness (willingness to emerge into a novel environment), but not others (latency to become active in novel environment), compared to non-infected crickets. Interestingly, sham injection resulted in a universal lack of among-individual differences. Our results highlight the sensitivity of among-individual variance and repeatability estimates to ecological and environmental factors that individuals face throughout their lives.

Significance statement

Animals are known to express consistent among-individual differences in behavior, also known as animal personalities, such that some individuals are always more bold, aggressive, or active relative to others. Yet it is relatively unknown how factors such as energy reserves and exposure to pathogens impact these differences in behavior. Here we investigated how exposure to a pathogenic bacteria as adults affects both the mean behavioral expression and the among-individual differences. Our results show that pathogen exposure results in large levels of among-individual differences in some aspects of boldness behavior (willingness to expose oneself to risk), but not others (latency to become active in a novel environment). These results highlight the sensitivity of behavioral differences to elements of state, such as infection status.

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References

  • Adamo S (1998) The specificity of behavioral fever in the cricket Acheta domesticus. J Parasitol:529–533

  • Adamo SA (2004) Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the cricket Gryllus texensis. J Insect Physiol 50:209–216

    Article  CAS  PubMed  Google Scholar 

  • Adamo SA, Kovalko I, Easy RH, Stoltz D (2014) A viral aphrodisiac in the cricket Gryllus texensis. J Exp Biol 217:1970–1976

    Article  PubMed  Google Scholar 

  • Ahtiainen JJ, Alatalo RV, Kortet R, Rantala MJ (2006) Immune function, dominance and mating success in drumming male wolf spiders Hygrolycosa rubrofasciata. Behav Ecol Sociobiol 60:826–832

    Article  Google Scholar 

  • Ardia DR, Gantz JE, Brent C, Strebel S (2012) Costs of immunity in insects: an induced immune response increases metabolic rate and decreases antimicrobial activity. Funct Ecol 26:732–739

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2013) lme4: linear mixed-effects models using Eigen and S4. R package version 1

  • Briffa M, Weiss A (2010) Animal personality. Curr Biol 20:R912–R914

    Article  CAS  PubMed  Google Scholar 

  • Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510

    Article  CAS  PubMed  Google Scholar 

  • Butler MW, Toomey MB, McGraw KJ, Rowe M (2012) Ontogenetic immune challenges shape adult personality in mallard ducks. Proc R Soc Lond B 279:326–333

    Article  Google Scholar 

  • Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R (2013) Animal personality: what are behavioural ecologists measuring? Biol Rev 88:465–475

    Article  PubMed  Google Scholar 

  • Coats J, Poulin R, Nakagawa S (2010) The consequences of parasitic infections for host behavioural correlations and repeatability. Behaviour 147:367–382

    Article  Google Scholar 

  • David M, Auclair Y, Giraldeau LA, Cézilly F (2012) Personality and body condition have additive effects on motivation to feed in zebra finches Taeniopygia guttata. Ibis 154:372–378

    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 

  • DiRienzo N, Montiglio PO (2016) The contribution of developmental experience vs. condition to life history, trait variation and individual differences. J Anim Ecol 85(4):915–926

  • DiRienzo N, Niemelä PT, Skog A, Vainikka A, Kortet R (2015) Juvenile pathogen exposure affects the presence of personality in adult field crickets. Front Ecol Evol 3:36

    Google Scholar 

  • DiRienzo N, Pruitt JN, Hedrick AV (2012) Juvenile exposure to acoustic sexual signals from conspecifics alters growth trajectory and an adult personality trait. Anim Behav 84:861–868

    Article  Google Scholar 

  • DiRienzo N, Pruitt JN, Hedrick AV (2013) The combined behavioural tendencies of predator and prey mediate the outcome of their interaction. Anim Behav 86:317–322

    Article  Google Scholar 

  • Fisher DN, David M, Tregenza, Tom, Rodríguez-Muñoz R (2015) Dynamics of among-individual behavioral variation over adult lifespan in a wild insect. Behav Ecol 26(4):975–985

  • Freeman-Gallant CR, Taff CC, Morin DF, Dunn PO, Whittingham LA, Tsang SM (2010) Sexual selection, multiple male ornaments, and age-and condition-dependent signaling in the common yellowthroat. Evolution 64:1007–1017

    Article  PubMed  Google Scholar 

  • Grimont PA, Grimont F (1978) The genus Serratia. Annu Rev Microbiol 32:221–248

    Article  CAS  PubMed  Google Scholar 

  • Groothuis TG, Trillmich F (2011) Unfolding personalities: the importance of studying ontogeny. Dev Psychobiol 53:641–655

    Article  PubMed  Google Scholar 

  • Hedrick AV (2000) Crickets with extravagant mating songs compensate for predation risk with extra caution. Proc R Soc Lond B 267:671–675

    Article  CAS  Google Scholar 

  • Hedrick AV, Kortet R (2006) Hiding behaviour in two cricket populations that differ in predation pressure. Anim Behav 72:1111–1118

    Article  Google Scholar 

  • Holzer B, Jacot A, Brinkhof MW (2003) Condition-dependent signaling affects male sexual attractiveness in field crickets, Gryllus campestris. Behav Ecol 14:353–359

    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

  • Janssens L, Stoks R (2014) Reinforcing effects of non-pathogenic bacteria and predation risk: from physiology to life history. Oecologia 176:323–332

    Article  PubMed  Google Scholar 

  • Kekäläinen J, Lai Y-T, Vainikka A, Sirkka I, Kortet R (2014) Do brain parasites alter host personality?—experimental study in minnows. Behav Ecol Sociobiol 68:197–204

    Article  Google Scholar 

  • Kortet R, Hedrick A (2007) A behavioural syndrome in the field cricket Gryllus integer: intrasexual aggression is correlated with activity in a novel environment. Biol J Linn Soc 91:475–482

    Article  Google Scholar 

  • Kortet R, Hedrick AV, Vainikka A (2010) Parasitism, predation and the evolution of animal personalities. Ecol Lett 13:1449–1458

    Article  PubMed  Google Scholar 

  • Kortet R, Rantala MJ, Hedrick A (2007) Boldness in anti-predator behaviour and immune defence in field crickets. Evol Ecol Res 9:185–197

    Google Scholar 

  • Kortet R, Niemelä PT, Vainikka A, Laakso J (2012). Females prefer bold males; an analysis of boldness, mate choice, and bacterial resistance in the field cricket Gryllus integer. Ecological Parasitology and Immunology 1:1–6

  • Kotiaho JS (2000) Testing the assumptions of conditional handicap theory: costs and condition dependence of a sexually selected trait. Behav Ecol Sociobiol 48:188–194

    Article  Google Scholar 

  • Liedtke J, Redekop D, Schneider JM, Schuett W (2015) Early environmental conditions shape personality types in a jumping spider. Front Ecol Evol 3:134

    Article  Google Scholar 

  • Louis C, Jourdan M, Cabanac M (1986) Behavioral fever and therapy in a rickettsia-infected Orthoptera. Am J Physiol-Reg I 250:R991–R995

    CAS  Google Scholar 

  • Luttbeg B, Sih A (2010) Risk, resources and state-dependent adaptive behavioural syndromes. Philos T R Soc B 365:3977–3990

    Article  Google Scholar 

  • Mappes J, Alatalo RV, Kotiaho J, Parri S (1996) Viability costs of condition-dependent sexual male display in a drumming wolf spider. Proc R Soc B 263:785–789

    Article  Google Scholar 

  • Márkus R, Kurucz É, Rus F, Andó I (2005) Sterile wounding is a minimal and sufficient trigger for a cellular immune response in Drosophila melanogaster. Immunol Lett 101:108–111

    Article  PubMed  Google Scholar 

  • Martin JG, Réale D (2008) Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. Anim Behav 75:309–318

    Article  Google Scholar 

  • McElreath R, Luttbeg B, Fogarty SP, Brodin T, Sih A (2007) Evolution of animal personalities. Nature 450:E5–E5

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  • Niemelä PT, Vainikka A, Hedrick AV, Kortet R (2012b) Integrating behaviour with life history: boldness of the field cricket, Gryllus integer, during ontogeny. Funct Ecol 26(2):450–456

  • Niemelä PT, Vainikka A, Lahdenperä S, Kortet R (2012c) Nymphal density, behavioral development, and life history in a field cricket. Behav Ecol Sociobiol 66:645–652

    Article  Google Scholar 

  • Niemelä PT, DiRienzo N, Hedrick AV (2012a) Predator-induced changes in the boldness of naïve field crickets, Gryllus integer, depends on behavioural type. Anim Behav 84:129–135

    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 

  • Pinheiro JC, Bates DM (2000) Linear mixed-effects models: basic concepts and examples. Mixed-Effects Models in S and S-Plus:3–56

  • Poulin R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Adv Stud Behav 41:151–186

    Article  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. The R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.R-project.org/

  • Rantala M, Roff D (2005) An analysis of trade-offs in immune function, body size and development time in the Mediterranean field cricket, Gryllus bimaculatus. Funct Ecol 19:323–330

    Article  Google Scholar 

  • Rantala MJ, Kortet R (2003) Courtship song and immune function in the field cricket Gryllus bimaculatus. Biol J Linn Soc 79(3):503–510

  • Rantala MJ, Kortet R (2004) Male dominance and immunocompetence in a field cricket. Behav Ecol 15:187–191

    Article  Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    Article  PubMed  Google Scholar 

  • Rigby MC, Jokela J (2000) Predator avoidance and immune defence: costs and trade-offs in snails. Proc R Soc Lond B 267:171–176

    Article  CAS  Google Scholar 

  • Seaman B, Briffa M (2015) Parasites and personality in periwinkles (Littorina littorea): infection status is associated with mean-level boldness but not repeatability. Behav Process 115:132–134

    Article  Google Scholar 

  • Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289

    Article  PubMed  Google Scholar 

  • Sinn DL, Gosling SD, Moltschaniwskyj NA (2008) Development of shy/bold behaviour in squid: context-specific phenotypes associated with developmental plasticity. Anim Behav 75:433–442

    Article  Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press

  • Westneat DF, Hatch MI, Wetzel DP, Ensminger AL (2011) Individual variation in parental care reaction norms: integration of personality and plasticity. Am Nat 178:652–667

    Article  PubMed  Google Scholar 

  • Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the University of Oulu and UEF for hosting ND while conducting this research. We also thank the National Science Foundation Nordic Research Opportunity, the Orthopterists’ Society Theodore J. Cohn Research Fund, the Emil Aaltonen foundation, Academy of Finland (project 127398), and Tekes: The Finnish Funding Agency for Innovation for their support in this project. ND was supported by an NSF Graduate Research Fellowship. RK and PTN were supported by the Academy of Finland. We also thank Jouni Laakso and Lauri Mikonranta for providing the bacterial culture of Serratia marcescens used in this experiment.

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Arizona, PO Box 210088, Tucson, AZ, 85721, USA

    Nicholas DiRienzo

  2. Department of Neurobiology Physiology and Behavior, University of California—Davis, One Shields Ave, Davis, CA, 95616, USA

    Nicholas DiRienzo & Ann V. Hedrick

  3. Department Biology II, Ludwig-Maximilians University of Munich, Planegg-Martinsried, Germany

    Petri T. Niemelä

  4. Department of Environmental and Biological Sciences, University of Eastern Finland, Joensuu, Finland

    Raine Kortet

  5. Department of Biology, Biological and Geological Sciences, University of Western Ontario, 1151 Richmond St N, London, ON, N6A 5B7, Canada

    Raine Kortet

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  1. Nicholas DiRienzo
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Correspondence to Nicholas DiRienzo.

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Communicated by S. Cremer

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DiRienzo, N., Niemelä, P.T., Hedrick, A.V. et al. Adult bacterial exposure increases behavioral variation and drives higher repeatability in field crickets. Behav Ecol Sociobiol 70, 1941–1947 (2016). https://doi.org/10.1007/s00265-016-2200-5

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