When the mean no longer matters: Developmental diet affects behavioral variation but not population averages in the house cricket (Acheta domesticus)

Behavioral Ecology

Volumn 28, Issue 1, 2017, Pages 337-345

  Royauté, Raphaël ^a   Dochtermann, Ned A ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

activity; animal personality; antipredator response; behavioral syndromes; behavioral variation; developmental conditions; diet quality; house crickets; permanent environment

Indexed keywords

ACTIVITY PATTERN; ANTIPREDATOR DEFENSE; BEHAVIORAL RESPONSE; BIOLOGICAL DEVELOPMENT; BODY SIZE; DIET; ENVIRONMENTAL CUE; GROWTH RATE; NUTRITIONAL STATUS;

ACHETA DOMESTICUS; ANIMALIA; GRYLLIDAE;

EID: 85008647708     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/arw164     Document Type: Article

References (88)

1. Akman C, Zhao Q, Liu X, Holmes GL. 2004. Effect of food deprivation during early development on cognition and neurogenesis in the rat. Epilepsy Behav. 5:446-454.
2. Bell AM. 2005. Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol. 18:464-473.
3. Bell AM, Sih A. 2007. Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett. 10:828-834.
4. Bengston SE, Jandt JM. 2014. The development of collective personality: the ontogenetic drivers of behavioral variation across groups. Front Ecol Evol. 2:81.
5. Bergeron P, Montiglio PO, Réale D, Humphries MM, Gimenez O, Garant D. 2013. Disruptive viability selection on adult exploratory behaviour in eastern chipmunks. J Evol Biol. 26:766-774.
6. Bertram SM, Whattam EM, Visanuvimol L, Bennett R, Lauzon C. 2009. Phosphorus availability influences cricket mate attraction displays. Anim Behav 77:525-530.
7. Braendle C, Davis GK, Brisson JA, Stern DL. 2006. Wing dimorphism in aphids. Heredity (Edinb). 97:192-199.
8. Brodin T. 2009. Behavioral syndrome over the boundaries of life-carryovers from larvae to adult damselfly. Behav Ecol. 20:30-37.
9. Buss DM, Greiling H. 1999. Adaptive individual differences. J Personality. 67:209-243.
10. Butler MW, Toomey MB, McGraw KJ, Rowe M. 2012. Ontogenetic immune challenges shape adult personality in mallard ducks. Proc Biol Sci. 279:326-333.
11. Carere C, Drent PJ, Privitera L, Koolhaas JM, Groothuis TG. 2005. Personalities in great tits, Parus major: stability and consistency. Anim Behav. 70:795-805.
12. Clark CW. 1994. Antipredator behavior and the asset-protection principle. Behav Ecol. 5:159-170.
13. Clark CW, Mangel M. 2000. Dynamic state variable models in ecology: methods and applications. New York: Oxford University Press.
14. Cruz, x, Neto A, xa P, Bozinovic F. 2004. The Relationship between Diet Quality and Basal Metabolic Rate in Endotherms: Insights from Intraspecific Analysis. Physiol Biochem Zool. 77:877-889.
15. Dall SRX, Houston AI, McNamara JM. 2004. The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett. 7:734-739.
16. Dingemanse NJ, Dochtermann NA. 2013. Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol. 82:39-54.
17. Dingemanse NJ, Dochtermann NA. 2014. Individual behaviour: behavioural ecology meets quantitative genetics. In: Charmantier A, Garant D, Kruuk LE, editors. Quantitative genetics in the wild. Oxford, UK: Oxford University Press. p. 54-67.
18. 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.
19. 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. 76:1128-1138.
20. 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.
21. 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.
22. Dochtermann NA. 2011. Testing Cheverud's conjecture for behavioral correlations and behavioral syndromes. Evolution. 65:1814-1820.
23. Dochtermann NA, Dingemanse NJ. 2013. Behavioral syndromes as evolutionary constraints. Behav Ecol. 24:806-811.
24. Dochtermann NA, Jenkins SH, Swartz MJ, Hargett AC. 2012. The roles of competition and environmental heterogeneity in the maintenance of behavioral variation and covariation. Ecology. 93:1330-1339.
25. Dochtermann NA, Nelson AB. 2014. Multiple Facets of Exploratory Behavior in House Crickets (Acheta domesticus): Split Personalities or Simply Different Behaviors? Ethology. 120:1110-1117.
26. Dochtermann NA, Roff DA. 2010. Applying a quantitative genetics framework to behavioural syndrome research. Philos Trans R Soc Lond B Biol Sci. 365:4013-4020.
27. Dochtermann NA, Schwab T, Sih A. 2015. The contribution of additive genetic variation to personality variation: heritability of personality. Proc Biol Sci. 282:20142201.
28. Duckworth RA. 2010. Evolution of personality: developmental constraints on behavioral flexibility. Auk. 127:752-758.
29. Groothuis TG, Trillmich F. 2011. Unfolding personalities: the importance of studying ontogeny. Dev Psychobiol. 53:641-655.
30. Hadfield JD. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Soft. 33:1-22.
31. Han CS, Dingemanse NJ. 2015. Effect of diet on the structure of animal personality. Front Zool. 12(1 Suppl):S5.
32. Han CS, Jäger HY, Dingemanse NJ. 2016. Individuality in nutritional preferences: a multi-level approach in field crickets. Sci Rep. 6:29071.
33. Hedrick AV. 2000. Crickets with extravagant mating songs compensate for predation risk with extra caution. Proc Biol Sci. 267:671-675.
34. Hedrick AV, Kortet R. 2012. Sex differences in the repeatability of boldness over metamorphosis. Behav Ecol Sociobiol. 66:407-412.
35. Herman CS, Valone TJ. 2000. The effect of mammalian predator scent on the foraging behavior of Dipodomys merriami. Oikos. 91:139-145.
36. Houslay TM, Hunt J, Tinsley MC, Bussière LF. 2015. Sex differences in the effects of juvenile and adult diet on age-dependent reproductive effort. J Evol Biol. 28:1067-1079.
37. Houston A, McNamara J. 1999. Models of adaptive behaviour. Cambridge (UK): Cambridge University Press.
38. Hunt J, Brooks R, Jennions MD. 2005. Female mate choice as a conditiondependent life-history trait. Am Nat. 166:79-92.
39. Hunt J, Brooks R, Jennions MD, Smith MJ, Bentsen CL, Bussière LF. 2004. High-quality male field crickets invest heavily in sexual display but die young. Nature. 432:1024-1027.
40. Hunt J, Jennions MD, Spyrou N, Brooks R. 2006. Artificial selection on male longevity influences age-dependent reproductive effort in the black field cricket Teleogryllus commodus. Am Nat. 168:E72-E86.
41. Iwasaki M, Katagiri C. 2008. Cuticular lipids and odors induce sex-specific behaviors in the male cricket Gryllus bimaculatus. Comp Biochem Physiol A Mol Integr Physiol. 149:306-313.
42. Jandt JM, Bengston S, Pinter-Wollman N, Pruitt JN, Raine NE, Dornhaus A, Sih A. 2014. Behavioural syndromes and social insects: personality at multiple levels. Biol Rev Camb Philos Soc. 89:48-67.
43. Kasumovic MM. 2013. The multidimensional consequences of the juvenile environment: towards an integrative view of the adult phenotype. Anim Behav. 85:1049-1059.
44. Kortet R, Hedrick A. 2004. Detection of the spider predator, Hololena nedra by naive juvenile field crickets (Gryllus integer) using indirect cues. Behaviour. 141:1189-1196.
45. Kortet R, Hedrick A. 2005. The scent of dominance: female field crickets use odour to predict the outcome of male competition. Behav Ecol Sociobiol. 59:77-83.
46. 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 Linnean Soc. 91:475-482.
47. Ledón-Rettig CC, Richards CL, Martin LB. 2012. Epigenetics for behavioral ecologists. Behav Ecol. ars145.
48. Lee WS, Monaghan P, Metcalfe NB. 2015. Perturbations in growth trajectory due to early diet affect age-related deterioration in performance. Funct Ecol. 30:625-635.
49. Liedtke J, Redekop D, Schneider JM, Schuett W. 2015. Early environmental conditions shape personality types in a jumping spider. Front Ecol Evol. 3:134.
50. Luttbeg B, Sih A. 2010. Risk, resources and state-dependent adaptive behavioural syndromes. Philos Trans R Soc Lond B Biol Sci. 365:3977-3990.
51. Mathot KJ, van den Hout PJ, Piersma T, Kempenaers B, Réale D, Dingemanse NJ. 2011. Disentangling the roles of frequency-vs. statedependence in generating individual differences in behavioural plasticity. Ecol Lett. 14:1254-1262.
52. Metcalfe NB, Monaghan P. 2001. Compensation for a bad start: grow now, pay later? Trends Ecol Evol. 16:254-260.
53. Montiglio PO, Royauté R. 2014. Contaminants as a neglected source of behavioural variation. Anim Behav. 88:29-35.
54. Nakagawa S, Schielzeth H. 2010. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev Camb Philos Soc. 85:935-956.
55. Nelson AB, Alemadi SD, Wisenden BD. 2013. Learned recognition of novel predator odour by convict cichlid embryos. Behav Ecol Sociobiol. 67:1269-1273.
56. Niemelä P, Lattenkamp EZ, Dingemanse NJ. 2015. Personality-related survival and sampling bias in wild cricket nymphs. Behav Ecol. 26:936-946.
57. Niemelä P, Vainikka A, Lahdenperä S, Kortet R. 2012a. Nymphal density, behavioral development, and life history in a field cricket. Behav Ecol Sociobiol. 66:645-652.
58. 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. 26:450-456.
59. Noguera JC, Metcalfe NB, Surai PF, Monaghan P. 2015. Are you what you eat? Micronutritional deficiencies during development influence adult personality-related traits. Anim Behav. 101:129-140.
60. Paterson RA, Pritchard DW, Dick JT, Alexander ME, Hatcher MJ, Dunn AM. 2013. Predator cue studies reveal strong trait-mediated effects in communities despite variation in experimental designs. Anim Behav. 86:1301-1313.
61. van de Pol M, Wright J. 2009. A simple method for distinguishing withinversus between-subject effects using mixed models. Anim Behav. 77:753-758.
62. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. 2007. Integrating animal temperament within ecology and evolution. Biol Rev Camb Philos Soc. 82:291-318.
63. Royauté R, Buddle CM, Vincent C. 2014. Interpopulation variations in behavioral syndromes of a jumping spider from insecticide-treated and insecticide-free orchards. Ethology. 120:127-139.
64. Royauté R, Buddle CM, Vincent C. 2015a. Under the influence: sublethal exposure to an insecticide affects personality expression in a jumping spider. Funct Ecol. 29:962-970.
65. Royauté R, Dochtermann N. 2016. Data from: When the mean no longer matters: developmental diet affects behavioral variation but not population averages in the house cricket (Acheta domesticus). Dryad Digital Repository. http://dx.doi.org/10.5061/dryad.nv835
66. Royauté R, Greenlee K, Baldwin M, Dochtermann NA. 2015b. Behaviour, metabolism and size: phenotypic modularity or integration in Acheta domesticus? Anim Behav. 110:163-169.
67. Sih A, Bell A, Johnson JC. 2004a. Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol. 19:372-378.
68. Sih A, Bell AM, Johnson JC, Ziemba RE. 2004b. Behavioral syndromes: an intergrative overiew. Q Rev Biol. 79:241-277.
69. Sih A, Mathot KJ, Moirón M, Montiglio PO, Wolf M, Dingemanse NJ. 2015. Animal personality and state-behaviour feedbacks: a review and guide for empiricists. Trends Ecol Evol. 30:50-60.
70. 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.
71. Snell-Rood EC. 2013. An overview of the evolutionary causes and consequences of behavioural plasticity. Anim Behav. 85:1004-1011.
72. Stamps J, Groothuis TG. 2010. The development of animal personality: relevance, concepts and perspectives. Biol Rev Camb Philos Soc. 85:301-325.
73. Storm JJ, Lima SL. 2008. Predator-naïve fall field crickets respond to the chemical cues of wolf spiders. Can J Zool. 86:1259-1263.
74. Storm JJ, Lima SL. 2010. Mothers forewarn offspring about predators: a transgenerational maternal effect on behavior. Am Nat. 175:382-390.
75. Tatar M, Carey J. 1995. Nutrition mediates reproductive trade-offs with age-specific mortality in the beetle Callosobruchus maculatus. Ecology. 76:2066-2073.
76. Taylor RW, Boon AK, Dantzer B, Réale D, Humphries MM, Boutin S, Gorrell JC, Coltman DW, McAdam AG. 2012. Low heritabilities, but genetic and maternal correlations between red squirrel behaviours. J Evol Biol. 25:614-624.
77. Tremmel M, Muller C. 2013. Insect personality depends on environmental conditions. Behav Ecol. 24:386-392.
78. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. 2004. Epigenetic programming by maternal behavior. Nat Neurosci. 7:847-854.
79. Weddle CB, Steiger S, Hamaker CG, Ower GD, Mitchell C, Sakaluk SK, Hunt J. 2013. Cuticular hydrocarbons as a basis for chemosensory selfreferencing in crickets: a potentially universal mechanism facilitating polyandry in insects. Ecol Lett. 16:346-353.
80. West-Eberhard MJ. 2003. Developmental plasticity and evolution. Oxford, UK: Oxford University Press.
81. 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.
82. Westneat DF, Wright J, Dingemanse NJ. 2015. The biology hidden inside residual within-individual phenotypic variation. Biol Rev Camb Philos Soc. 90:729-743.
83. Wilder S, Rypstra A. 2008. Diet quality affects mating behaviour and egg production in a wolf spider. Anim Behav. 76:439-445.
84. Wilson ADM, Krause J. 2012. Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav Ecol. 23:1316-1323.
85. Wolf M, van Doorn GS, Leimar O, Weissing FJ. 2007. Life-history tradeoffs favour the evolution of animal personalities. Nature. 447:581-584.
86. Zajitschek F, Hunt J, Jennions M, Hall M, Brooks R. 2009. Effects of juvenile and adult diet on ageing and reproductive effort of male and female black field crickets Teleogryllus commodus. Funct Ecol. 23:602-611.
87. Zajitschek F, Lailvaux SP, Dessmann J, Brooks R. 2012. Diet, sex, and death in field crickets. Ecol Evol. 2:1627-1636.
88. Zuur AF. 2009. Mixed effects models and extensions in ecology with R. New York: Springer.