You are what you eat: Diet shapes body composition, personality and behavioural stability

BMC Evolutionary Biology

Volumn 17, Issue 1, 2017, Pages

  Han, Chang S ^a,b   Dingemanse, Niels J ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Behavioural stability; Developmental plasticity; Diet; Heterogeneous residual within individual variance; Personality; Repeatability

Indexed keywords

ADULT; BEHAVIORAL ECOLOGY; BODY CONDITION; CONSPECIFIC; CRICKET; DIET; ENVIRONMENTAL FACTOR; INDIVIDUAL VARIATION; JUVENILE; PHENOTYPE; PHENOTYPIC PLASTICITY; SEX-RELATED DIFFERENCE;

GRYLLINAE; GRYLLUS BIMACULATUS;

CARBOHYDRATE DIET; PROTEIN INTAKE;

AGGRESSION; ANIMAL; ANIMAL BEHAVIOR; BODY COMPOSITION; BODY WEIGHT; CARBOHYDRATE DIET; DIET; DRUG EFFECTS; FEEDING BEHAVIOR; FEMALE; GRYLLIDAE; MALE; PERSONALITY; PHARMACOLOGY; PHENOTYPE; PHYSIOLOGY; PROTEIN INTAKE; SEXUAL BEHAVIOR;

AGGRESSION; ANIMALS; BEHAVIOR, ANIMAL; BODY COMPOSITION; BODY WEIGHT; DIET; DIETARY CARBOHYDRATES; DIETARY PROTEINS; FEEDING BEHAVIOR; FEMALE; GRYLLIDAE; MALE; PERSONALITY; PHENOTYPE; SEXUAL BEHAVIOR, ANIMAL;

EID: 85008690132     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-016-0852-4     Document Type: Article

References (95)

1. Dingemanse NJ, Kazem AJN, Réale D, Wright J. Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol. 2010;25(2):81-9.
2. Dingemanse NJ, Wolf M. Recent models for adaptive personality differences: a review. Phil Trans R Soc B. 2010;365(1560):3947-58.
3. Westneat DF, Wright J, Dingemanse NJ. The biology hidden inside residual within-individual phenotypic variation. Biol Rev. 2014;90(3):729-43.
4. Dochtermann NA, Schwab T, Sih A. The contribution of additive genetic variation to personality variation: heritability of personality. Proc R Soc Lond B Biol Sci. 2015;282(1798):20142201.
5. Kasumovic MM, Brooks RC. It's all who you know: the evolution of socially cued anticipatory plasticity as a mating strategy. Q Rev Biol. 2011;86(3):181-97.
6. Snell-Rood EC. An overview of the evolutionary causes and consequences of behavioural plasticity. Anim Behav. 2013;85(8):1004-11.
7. West-Eberhard MJ. Developmental plasticity and evolution. Oxford: Oxford University Press; 2003.
8. Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci. 2001;24(1):1161-92.
9. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. Epigenetic programming by maternal behavior. Nat Neurosci. 2004;7(8):847-54.
10. Carere C, Drent PJ, Koolhaas JM, Groothuis TGG: Epigenetic effects on personality traits: early food provisioning and sibling competition. Behaviour, 142 2005;9(10):1329-55.
11. Dingemanse NJ, Dochtermann NA. Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol. 2013;82(1):39-54.
12. Jenkins SH. Sex differences in repeatability of food-hoarding behaviour of kangaroo rats. Anim Behav. 2011;81(6):1155-62.
13. Briffa M. Plastic proteans: reduced predictability in the face of predation risk in hermit crabs. Biol Lett. 2013;9(5):20130592.
14. Careau V, Buttemer WA, Buchanan KL. Early-developmental stress, repeatability, and canalization in a suite of physiological and behavioral traits in female zebra finches. Integr Comp Biol. 2014;54(4):539-54.
15. DiRienzo N, Niemelä PT, Skog A, Vainikka A, Kortet R. Juvenile pathogen exposure affects the presence of personality in adult field crickets. Front Ecol Evol. 2015;3:36.
16. Royaute R, Dochtermann NA: When the mean no longer matters: Developmental diet affects behavioral variation but not population averages in the house cricket (Acheta domesticus). Behav Ecol 2017:in press.
17. Westneat DF, Schofield M, Wright J. Parental behavior exhibits among-individual variance, plasticity, and heterogeneous residual variance. Behav Ecol. 2013;24(3):598-604.
18. Wood CW, Brodie ED. Environmental effects on the structure of the G-matrix. Evolution. 2015;69(11):2927-40.
19. Charmantier A, Garant D. Environmental quality and evolutionary potential: lessons from wild populations. Proc R Soc Lond B. 2005;272(1571):1415-25.
20. Hoffmann AA, Merilä J. Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol. 1999;14(3):96-101.
21. Han CS, Dingemanse NJ. Effect of diet on the structure of animal personality. Front Zool. 2015;12 Suppl 1:S5.
22. Zajitschek F, Lailvaux SP, Dessmann J, Brooks R. Diet, sex, and death in field crickets. Ecol Evol. 2012;2(7):1627-36.
23. Blay S, Yuval B. Nutritional correlates of reproductive success of male Mediterranean fruit flies (Diptera: Tephritidae). Anim Behav. 1997;54(1):59-66.
24. Droney DC. Environmental influences on male courtship and implications for female choice in a lekking HawaiianDrosophila. Anim Behav. 1996;51(4):821-30.
25. Hunt J, Brooks R, Jennions MD, Smith MJ, Bentsen CL, Bussiere LF. High-quality male field crickets invest heavily in sexual display but die young. Nature. 2004;432(7020):1024-7.
26. Maklakov AA, Simpson SJ, Zajitschek F, Hall MD, Dessmann J, Clissold F, Raubenheimer D, Bonduriansky R, Brooks RC. Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Curr Biol. 2008;18(14):1062-6.
27. Wilder SM, Rypstra AL. Diet quality affects mating behaviour and egg production in a wolf spider. Anim Behav. 2008;76(2):439-45.
28. Lichtenstein JL, DiRienzo N, Knutson K, Kuo C, Zhao KC, Brittingham HA, Geary SE, Ministero S, Rice HK, David Z. Prolonged food restriction decreases body condition and reduces repeatability in personality traits in web-building spiders. Behav Ecol Sociobiol. 2016;70(11):1793-803.
29. Paaby AB, Rockman MV. Cryptic genetic variation: evolution's hidden substrate. Nat Rev Genet. 2014;15(4):247-58.
30. Senior A, Nakagawa S, Lihoreau M, Simpson S, Raubenheimer D. An Overlooked Consequence of Dietary Mixing: A Varied Diet Reduces Interindividual Variance in Fitness. Am Nat. 2015;186(5):649-59.
31. Bunning H, Bassett L, Clowser C, Rapkin J, Jensen K, House CM, Archer CR, Hunt J. Dietary choice for a balanced nutrient intake increases the mean and reduces the variance in the reproductive performance of male and female cockroaches. Ecol Evol. 2016;6(14):4711-30.
32. DeWitt TJ, Sih A, Wilson DS. Costs and limits of phenotypic plasticity. Trends Ecol Evol. 1998;13(2):77-81.
33. Wilson A, Morrissey M, Adams M, Walling C, Guinness F, Pemberton J, Clutton-Brock T, Kruuk L. Indirect genetics effects and evolutionary constraint: an analysis of social dominance in red deer. Cervus elaphus J Evol Biol. 2011;24(4):772-83.
34. Wilson AJ, Gelin U, Perron M-C, Réale D. Indirect genetic effects and the evolution of aggression in a vertebrate system. Proc R Soc Lond B Biol Sci. 2009;276(1656):533-41.
35. Houle D. Comparing evolvability and variability of quantitative traits. Genetics. 1992;130(1):195-204.
36. Lee KP. Sex-specific differences in nutrient regulation in a capital breeding caterpillar, Spodoptera litura (Fabricius). J Insect Physiol. 2010;56(11):1685-95.
37. Lee KP, Kim J-S, Min K-J. Sexual dimorphism in nutrient intake and life span is mediated by mating in Drosophila melanogaster. Anim Behav. 2013;86(5):987-92.
38. Morehouse NI, Nakazawa T, Booher CM, Jeyasingh PD, Hall MD. Sex in a material world: why the study of sexual reproduction and sex-specific traits should become more nutritionally-explicit. Oikos. 2010;119(5):766-78.
39. Harrison SJ, Raubenheimer D, Simpson SJ, Godin J-GJ, Bertram SM. Towards a synthesis of frameworks in nutritional ecology: interacting effects of protein, carbohydrate and phosphorus on field cricket fitness. Proc R Soc Lond B Biol Sci. 2014;281(1792):20140539.
40. Simpson SJ, Raubenheimer D: The nature of nutrition: a unifying framework from animal adaptation to human obesity: Princeton: Princeton University Press; 2012
41. Adler MI, Cassidy EJ, Fricke C, Bonduriansky R. The lifespan-reproduction trade-off under dietary restriction is sex-specific and context-dependent. Exp Gerontol. 2013;48(6):539-48.
42. Bauerfeind SS, Fischer K. Effects of food stress and density in different life stages on reproduction in a butterfly. Oikos. 2005;111(3):514-24.
43. Dmitriew C, Rowe L. The effects of larval nutrition on reproductive performance in a food-limited adult environment. PLoS One. 2011;6(3):e17399.
44. Zajitschek F, Hunt J, Jennions MD, Hall MD, Brooks RC. Effects of juvenile and adult diet on ageing and reproductive effort of male and female black field crickets. Teleogryllus commodus Funct Ecol. 2009;23(3):602-11.
45. Maklakov AA, Hall MD, Simpson SJ, Dessmann J, Clissold FJ, Zajitschek F, Lailvaux SP, Raubenheimer D, Bonduriansky R, Brooks RC. Sex differences in nutrient-dependent reproductive ageing. Aging Cell. 2009;8(3):324-30.
46. Kasumovic MM, Hall MD, Try H, Brooks RC. Socially cued developmental plasticity affects condition-dependent trait expression. Behav Ecol. 2013;24(2):429-34.
47. Matos M. Maternal effects can inflate rate of adaptation to captivity. Proc Natl Acad Sci. 2012;109(36):E2380.
48. Wolf JB, Wade MJ. What are maternal effects (and what are they not)? Phil Trans R Soc B. 2009;364(1520):1107-15.
49. Niemelä PT, Dingemanse NJ. Artificial environments and the study of 'adaptive'personalities. Trends Ecol Evol. 2014;29(5):245-7.
50. Simpson S, Abisgold J. Compensation by locusts for changes in dietary nutrients: behavioural mechanisms. Physiol Entomol. 1985;10(4):443-52.
51. Raubenheimer D, Simpson SJ. Integrative models of nutrient balancing: application to insects and vertebrates. Nutr Res Rev. 1997;10:151-79.
52. Dingemanse NJ, Wright J, Kazem AJN, Thomas DK, Hickling R, Dawnay N. Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol. 2007;76(6):1128-38.
53. Dochtermann N. Behavioral syndromes: carryover effects, false discovery rates, and a priori hypotheses. Behav Ecol. 2010;21(5):919-26.
54. Dingemanse NJ, Araya-Ajoy YG. Interacting personalities: behavioural ecology meets quantitative genetics. Trends Ecol Evol. 2015;30(2):88-97.
55. Santostefano F, Wilson AJ, Araya-Ajoy YG, Dingemanse NJ. Interacting with the enemy: indirect effects of personality on conspecific aggression in crickets. Behav Ecol. 2016;27:1235-46.
56. Wilson AJ, Grimmer A, Rosenthal GG. Causes and consequences of contest outcome: aggressiveness, dominance and growth in the sheepshead swordtail, Xiphophorus birchmanni. Behav Ecol Sociobiol. 2013;67(7):1151-61.
57. McGlothlin JW, Moore AJ, Wolf JB, Brodie III ED. Interacting phenotypes and the evolutionary process. III Social evolution. Evolution. 2010;64(9):2558-74.
58. Wolf JB, Brodie III ED, Cheverud JM, Moore AJ, Wade MJ. Evolutionary consequences of indirect genetic effects. Trends Ecol Evol. 1998;13(2):64-9.
59. Wolf JB, Brodie III ED, Moore AJ. Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. Am Nat. 1999;153(3):254-66.
60. Han CS, Jäger H, Dingemanse NJ. Individuality in nutritional preferences: a multi-level approach in field crickets. Sci Rep. 2016;6:29071.
61. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. Integrating animal temperament within ecology and evolution. Biol Rev. 2007;82(2):291-318.
62. Adamo S, Linn C, Hoy R. The role of neurohormonal octopamine during 'fight or flight' behaviour in the field cricket Gryllus bimaculatus. J Exp Biol. 1995;198(8):1691-700.
63. Simmons L. Female choice in the field cricket Gryllus bimaculatus (De Geer). Anim Behav. 1986;34(5):1463-70.
64. Alexander RD, Otte D: The evolution of genitalia and mating behavior in crickets (Gryllidae): Misc Publ Mus Zool Univ Mich 1967;133: 1-62.
65. Simmons L. Sperm competition as a mechanism of female choice in the field cricket, Gryllus bimaculatus. Behav Ecol Sociobiol. 1987;21(3):197-202.
66. Wynn H, Vahed K. Male Gryllus bimaculatus guard females to delay them from mating with rival males and to obtain repeated copulations. J Insect Behav. 2004;17(1):53-66.
67. Sakaluk SK. Post-copulatory mate guarding in decorated crickets. Anim Behav. 1991;41(2):207-16.
68. Loveridge J. Age and the changes in water and fat content of adult laboratory-reared Locusta migratoria migratorioides R. and F. Rhodesian J Agric Res. 1973;11:131-44.
69. Pinheiro J, Bates D. Mixed-effects models in S and S-PLUS. New York: Springer; 2006.
70. Self SG, Liang K-Y. Asymptotic properties of maximum likelihood estimators and likelihood ratio tests under nonstandard conditions. J Am Stat Assoc. 1987;82(398):605-10.
71. Visscher PM. A note on the asymptotic distribution of likelihood ratio tests to test variance components. Twin Res Hum Genet. 2006;9(04):490-5.
72. Akaike H. Maximum likelihood identification of Gaussian autoregressive moving average models. Biometrika. 1973;60(2):255-65.
73. Burnham K, Anderson D: Model selection and inference. 2nd edition. New York: Springer; 1998.
74. Westneat DF, Hatch MI, Wetzel DP, Ensminger AL. Individual variation in parental care reaction norms: integration of personality and plasticity. Am Nat. 2011;178(5):652-67.
75. Westneat DF, Stewart IR, Hatch MI. Complex interactions among temporal variables affect the plasticity of clutch size in a multi-brooded bird. Ecology. 2009;90(5):1162-74.
76. McNeill S. The dynamics of a population of Leptopterna dolabrata (Heteroptera: Miridae) in relation to its food resources. J Anim Ecol. 1973;42:495-507.
77. Iversen T. Ingestion and growth in Sericostoma personatum (Trichoptera) in relation to the nitrogen content of ingested leaves. Oikos. 1974;25:278-82.
78. Merkel G. The effects of temperature and food quality on the larval development of Gryllus bimaculatus (Orthoptera, Gryllidae). Oecologia. 1977;30(2):129-40.
79. Gebhardt MD, Stearns SC. Reaction norms for developmental time and weight at eclosion in Drosophila mercatorum. J Evol Biol. 1988;1(4):335-54.
80. Tu MP, Tatar M. Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell. 2003;2(6):327-33.
81. Colasurdo N, Gélinas Y, Despland E. Larval nutrition affects life history traits in a capital breeding moth. J Exp Biol. 2009;212(12):1794-800.
82. Stoks R, Block MD, McPeek MA. Physiological costs of compensatory growth in a damselfly. Ecology. 2006;87(6):1566-74.
83. Monaghan P. Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc Lond B. 2008;363(1497):1635-45.
84. Niemelä PT, Santostefano F. Social carry-over effects on non-social behavioral variation: mechanisms and consequences. Front Ecol Evol. 2015;3:49.
85. Hsu Y, Earley RL, Wolf LL. Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes. Biol Rev. 2006;81(1):33-74.
86. Hsu Y, Wolf LL. The winner and loser effect: integrating multiple experiences. Anim Behav. 1999;57(4):903-10.
87. Kasumovic MM, Elias DO, Sivalinghem S, Mason AC, Andrade MC: Examination of prior contest experience and the retention of winner and loser effects. Behav Ecol. 2010;21(2):404-409.
88. Diaz-Uriarte R. Incorrect analysis of crossover trials in animal behaviour research. Anim Behav. 2002;63:815-22.
89. Senn S. Cross-over trials in clinical research, vol. 5. Chichester: Wiley; 1993.
90. Adamo SA, Hoy RR. Agonistic behaviour in male and female field crickets, Gryllus bimaculatus, and how behavioural context influences its expression. Anim Behav. 1995;49(6):1491-501.
91. Sakura M, Aonuma H. Aggressive behavior in the antennectomized male cricket Gryllus bimaculatus. J Exp Biol. 2013;216(12):2221-8.
92. Hofmann HA, Stevenson PA. Flight restores fight in crickets. Nature. 2000;403(6770):613.
93. Stearns SC. The evolution of life histories. New York: Oxford University Press; 1992.
94. Nakagawa S, Schielzeth H. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev. 2010;85(4):935-56.
95. Wyman M, Stinchcombe J, Rowe L. A multivariate view of the evolution of sexual dimorphism. J Evol Biol. 2013;26(10):2070-80.