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Genotype-by-sex-by-diet interactions for nutritional preference, dietary consumption, and lipid deposition in a field cricket

Heredityvolume 121pages361373 (2018) | Download Citation


Changes in feeding behaviour, especially the overconsumption of calories, has led to a rise in the rates of obesity, diabetes, and other associated disorders in humans and a range of animals inhabiting human-influenced environments. However, understanding the relative contribution of genes, the nutritional environment, and their interaction to dietary intake and lipid deposition in the sexes still remains a major challenge. By combining nutritional geometry with quantitative genetics, we determined the effect of genes, the nutritional environment, and their interaction on the total nutritional preference (TP), total diet eaten (TE), and lipid mass (LM) of male and female black field crickets (Teleogryllus commodus) fed one of four diet pairs (DPs) differing in the ratio of protein to carbohydrate and total nutritional content. We found abundant additive genetic variance for TP, TE, and LM in both sexes and across all four DPs, with significant genetic correlations between TE and TP and between TP and LM in males. We also found significant genotype-by-DP and genotype-by-sex-by-DP interactions for each trait and significant genotype-by-sex interactions for TE and LM. Complex interactions between genes, sex, and the nutritional environment, therefore, play an important role in nutrient regulation and lipid deposition in T. commodus. This finding may also help explain the increasing rate of obesity and the maintenance of sex differences in obesity observed across many animal species, including humans.

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  1. Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225

  2. Barreto RE, Moreira PSA, Carvalho RF (2003) Sex-specific compensatory growth in food-deprived Nile tilapia. Braz J Med Biol Res 36:477–483

  3. Barsh GS, Farooqi IS, O’Rahilly S (2000) Genetics of body-weight regulation. Nature 404:644–651

  4. Bentsen CL, Hunt J, Jennions MD, Brooks R (2006) Complex multivariate sexual selection on male acoustic signaling in a wild population of Teleogryllus commodus. Am Nat 167:E102–E116

  5. Brooks RC, Simpson SJ, Raubenheimer D (2010) The price of protein: combining evolutionary and economic analysis to understand excessive energy consumption. Obes Rev 11:887–894

  6. Bunning H, Bassett L, Clowser C, Rapkin J, Jensen K, House CM, Archer CR, Hunt J (2016) 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 6:4711–4730

  7. Bunning H, Rapkin J, Belcher L, Archer CR, Jensen K, Hunt J (2015) Protein and carbohydrate intake influence sperm number and fertility in male cockroaches, but not sperm viability. Proc R Soc B Biol Sci 282:20142144

  8. Cheverud JM, Lawson HA, Fawcett GL, Wang B, Pletscher LS, Fox AR et al. (2011) Diet‐dependent genetic and genomic imprinting effects on obesity in mice. Obesity 19:160–170

  9. Coatmellec-Taglioni G, Dausse J-P, Giudicelli Y, Ribière C (2003) Sexual dimorphism in cafeteria diet-induced hypertension is associated with gender-related difference in renal leptin receptor down-regulation. J Pharmacol Exp Ther 305:362–367

  10. Faith MS, Rha SS, Neale MC, Allison DB (1999) Evidence for genetic influences on human energy intake: results from a twin study using measured observations. Behav Genet 29:145–154

  11. Felton AM, Felton A, Raubenheimer D, Simpson SJ, Foley WJ, Wood JT et al. (2009) Protein content of diets dictates the daily energy intake of a free-ranging primate. Behav Ecol 20:685–690

  12. Gilmour AR, Gogel BJ, Cullis BR, Thompson R, Butler D (2009) ASReml user guide release 3.0. VSN Int. Ltd., Hemel Hempstead

  13. Gordon RR, Hunter KW, Sørensen P, Pomp D (2008) Genotype× diet interactions in mice predisposed to mammary cancer. I. Body weight and fat Mamm Genome 19:163–178

  14. Gosby AK, Conigrave AD, Lau NS, Iglesias MA, Hall RM, Jebb SA et al. (2011) Testing protein leverage in lean humans: a randomised controlled experimental study. PLoS ONE 6:e25929

  15. Gosby AK, Conigrave AD, Raubenheimer D, Simpson SJ (2014) Protein leverage and energy intake. Obes Rev 15:183–191

  16. Goudeau J, Bellemin S, Toselli-Mollereau E, Shamalnasab M, Chen Y, Aguilaniu H (2011) Fatty acid desaturation links germ cell loss to longevity through NHR-80/HNF4 in C. elegans. PLoS Biol 9:e1000599

  17. Hansen M, Flatt T, Aguilaniu H (2013) Reproduction, fat metabolism, and life span: what is the connection? Cell Metab 17:10–19

  18. Harrison S, Raubenheimer D, Simpson S, Godin G, Bertram S (2014) Towards a synthesis of frameworks in nutritional ecology: interacting effects of protein, carbohydrate and phosphorus on field cricket fitness. Proc R Soc B Biol Sci 281:20140539

  19. Hasselbalch AL, Heitmann BL, Kyvik KO, Sørensen TIA (2010) Associations between dietary intake and body fat independent of genetic and familial environmental background. Int J Obes 34:892

  20. Heianza Y, Qi L (2017) Gene-diet interaction and precision nutrition in obesity. Int J Mol Sci 18:787

  21. Henson SM, Hallam TG (1995) Optimal feeding via constrained processes. J Theor Biol 176:33–37

  22. Horne I, Haritos VS, Oakeshott JG (2009) Comparative and functional genomics of lipases in holometabolous insects. Insect Biochem Mol Biol 39:547–567

  23. Jensen K, McClure C, Priest NK, Hunt J (2015) Sex-specific effects of protein and carbohydrate intake on reproduction but not lifespan in Drosophila melanogaster. Aging Cell 14:605–615

  24. Kanter R, Caballero B (2012) Global gender disparities in obesity: a review. Adv Nutr 3:491–498

  25. Kapahi P, Chen D, Rogers AN, Katewa SD, Li PW-L, Thomas EL et al. (2010) With TOR, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab 11:453–465

  26. Kavanagh MW (1987) The efficiency of sound production in two cricket species, Gryllotalpa australis and Teleogryllus commodus (Orthoptera: Grylloidea). J Exp Biol 130:107–119

  27. van der Klaauw AA, Farooqi IS (2015) The hunger genes: pathways to obesity. Cell 161:119–132

  28. Klimentidis YC, Beasley TM, Lin H-Y, Murati G, Glass GE, Guyton M et al. (2011) Canaries in the coal mine: a cross-species analysis of the plurality of obesity epidemics. Proc R Soc B Biol Sci 278:1626–1632

  29. Lande R (1979) Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution 33:402–416

  30. Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–305

  31. Lee KP (2010) Sex-specific differences in nutrient regulation in a capital breeding caterpillar, Spodoptera litura (Fabricius). J Insect Physiol 56:1685–1695

  32. Lee KP, Simpson SJ, Clissold FJ, Brooks R, Ballard JW, Taylor PW et al. (2008) Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proc Natl Acad Sci USA 105:2498–2503

  33. Lihoreau M, Buhl J, Charleston MA, Sword GA, Raubenheimer D, Simpson SJ (2015) Nutritional ecology beyond the individual: a conceptual framework for integrating nutrition and social interactions. Ecol Lett 18:273–286

  34. Link JC, Reue K (2017) Genetic basis for sex differences in obesity and lipid metabolism. Annu Rev Nutr 37:225–245

  35. Liu J, Lloyd SG (2013) High-fat, low-carbohydrate diet alters myocardial oxidative stress and impairs recovery of cardiac function after ischemia and reperfusion in obese rats. Nutr Res 33:311–321

  36. Maklakov AA, Simpson SJ, Zajitschek F, Hall MD, Dessmann J, Clissold F et al. (2008) Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Curr Biol 18:1062–1066

  37. Marie LS, Miura GI, Marsh DJ, Yagaloff K, Palmiter RD (2000) A metabolic defect promotes obesity in mice lacking melanocortin-4 receptors. Proc Natl Acad Sci USA 97:12339–12344

  38. Martens EA, Lemmens SG, Westerterp-Plantenga MS (2013) Protein leverage affects energy intake of high-protein diets in humans. Am J Clin Nutr 97:86–93

  39. Mathes WF, Kelly SA, Pomp D (2011) Advances in comparative genetics: influence of genetics on obesity. Br J Nutr 106:S1–S10

  40. Medrikova D, Jilkova ZM, Bardova K, Janovska P, Rossmeisl M, Kopecky J (2012) Sex differences during the course of diet-induced obesity in mice: adipose tissue expandability and glycemic control. Int J Obes 36:262

  41. Musselman LP, Fink JL, Narzinski K, Ramachandran PV, Hathiramani SS, Cagan RL et al. (2011) A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis Model Mech 4:842–849

  42. Na J, Musselman LP, Pendse J, Baranski TJ, Bodmer R, Ocorr K et al. (2013) A Drosophila model of high sugar diet-induced cardiomyopathy. PLoS Genet 9:e1003175

  43. Nanoth Vellichirammal N, Zera AJ, Schilder RJ, Wehrkamp C, Riethoven J-JM, Brisson JA (2014) De novo transcriptome assembly from fat body and flight muscles transcripts to identify morph-specific gene expression profiles in Gryllus firmus. PLoS ONE 9:e82129

  44. Neel JV (1962) Diabetes mellitus: a ‘thrifty’ genotype rendered detrimental by ‘progress’? Am J Hum Genet 14:353–362

  45. Nestel D, Papadopoulos NT, Liedo P, Gonzales-Ceron L, Carey JR (2005) Trends in lipid and protein contents during medfly aging: an harmonic path to death. Arch Insect Biochem Physiol 60:130–139

  46. Ordovas JM (2008) Genotype–phenotype associations: modulation by diet and obesity. Obesity 16:S40–S46

  47. Post S, Tatar M (2016) Nutritional geometric profiles of insulin/IGF expression in Drosophila melanogaster. PLoS ONE 11:e0155628

  48. Qi L, Cho YA (2008) Gene-environment interaction and obesity. Nutr Rev 66:684–694

  49. Rapkin J, Archer CR, Grant CE, Jensen K, House CM, Wilson AJ et al. (2017) Little evidence for intralocus sexual conflict over the optimal intake of nutrients for life span and reproduction in the black field cricket Teleogryllus commodus. Evolution 77:2159–2177

  50. Rapkin J, Jensen K, Archer CR, House CM, Sakaluk SK, Castillo ED, Hunt J (2018) The Geometry of Nutrient Space–Based Life-History Trade-Offs: Sex-Specific Effects of Macronutrient Intake on the Trade-Off between Encapsulation Ability and Reproductive Effort in Decorated Crickets Am Nat 191:452–474

  51. Raubenheimer D, Machovsky-Capuska GE, Gosby AK, Simpson SJ (2015) Nutritional ecology of obesity: from humans to companion animals. Br J Nutr 113:S26–S39

  52. Raubenheimer D, Simpson SJ (1997) Integrative models of nutrient balancing: application to insects and vertebrates. Nutr Res Rev 10:151–179

  53. Reddiex AJ, Gosden TP, Bonduriansky R, Chenoweth SF (2013) Sex-specific fitness consequences of nutrient intake and the evolvability of diet preferences Am Nat 182:91–102

  54. Reed LK, Williams S, Springston M, Brown J, Freeman K, DesRoches CE, Sokolowski MB, Gibson G (2010) Genotype-by-diet interactions drive metabolic phenotype variation in Drosophila melanogaster . Genetics 185:1009–1019

  55. Robbins AL, Savage DB (2015) The genetics of lipid storage and human lipodystrophies. Trends Mol Med 21:433–438

  56. Schilder RJ, Marden JH (2006) Metabolic syndrome and obesity in an insect. Proc Natl Acad Sci USA 103:18805–18809

  57. Schilder RJ, Zera AJ, Black C, Hoidal M, Wehrkamp C (2011) The biochemical basis of life history adaptation: molecular and enzymological causes of NADP+-isocitrate dehydrogenase activity differences between morphs of Gryllus firmus that differ in lipid biosynthesis and life history. Mol Biol Evol 28:3381–3393

  58. Simpson SJ, Raubenheimer D (2005) Obesity: the protein leverage hypothesis. Obes Rev 6:133–142

  59. Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press, Princeton, NJ

  60. Skorupa DA, Dervisefendic A, Zwiener J, Pletcher SD (2008) Dietary composition specifies consumption, obesity and lifespan in Drosophila melanogaster. Aging Cell 7:478–490

  61. Smith BK, Andrews PK, West DB (2000) Macronutrient diet selection in thirteen mouse strains. Am J Physiol Integr Comp Physiol 278:R797–R805

  62. Song Y, Wang H-J, Dong B, Ma J, Wang Z, Agardh A (2016) 25-year trends in gender disparity for obesity and overweight by using WHO and IOTF definitions among Chinese school-aged children: a multiple cross-sectional study. BMJ Open 6:e011904

  63. Sørensen A, Mayntz D, Raubenheimer D, Simpson SJ (2008) Protein-leverage in mice: the geometry of macronutrient balancing and consequences for fat deposition. Obesity 16:566–571

  64. South SH, House CM, Moore AJ, Simpson SJ, Hunt J (2011) Male cockroaches prefer a high carbohydrate diet that makes them more attractive to females: implications for the study of condition dependence. Evolution 65:1594–1606

  65. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton, NJ

  66. Sutton GM, Trevaskis JL, Hulver MW, McMillan RP, Markward NJ, Babin MJ, Meyer EA, Butler AA (2006) Diet-genotype interactions in the development of the obese, insulin-resistant phenotype of C57BL/6J micelacking melanocortin-3 or-4 receptors Endocrinology 147:2183–2196

  67. Tanaka T (2014) Genetics of energy and macronutrient intake in humans. Curr Nutr Rep 3:170–177

  68. Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871-1971. Aldine Publishing Company, Chicago, IL, pp 136–179

  69. Warbrick-Smith J, Behmer ST, Lee KP, Raubenheimer D, Simpson SJ (2006) Evolving resistance to obesity in an insect. Proc Natl Acad Sci USA 103:14045–14049

  70. 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 79:13–26

  71. Wolf KJ, Lorenz RG (2012) Gut microbiota and obesity. Curr Obes Rep 1:1–8

  72. Yuan C, Gaskins AJ, Blaine AI, Zhang C, Gillman MW, Missmer SA et al. (2016) Association between cesarean birth and risk of obesity in offspring in childhood, adolescence, and early adulthood. JAMA Pediatr 170:e162385–e162385

  73. Zera AJ (2005) Intermediary metabolism and life history trade-offs: lipid metabolism in lines of the wing-polymorphic cricket, Gryllus firmus, selected for flight capability vs. early age reproduction. Integr Comp Biol 45:511–524

  74. Ziegler R, Van Antwerpen R (2006) Lipid uptake by insect oocytes. Insect Biochem Mol Biol 36:264–272

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JH was funded by a University Royal Society Fellowship and Equipment Grant and by NERC (NE/G00949X/1) and AJW by a BBSRC Fellowship. JR was funded by a NERC studentship (NERC/1200242) awarded to JH.

Author information


  1. Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Penryn, Cornwall, TR10 9FE, UK

    • James Rapkin
    • , Clarissa M. House
    • , Alastair J. Wilson
    •  & John Hunt
  2. Department of Bioscience, Terrestrial Ecology, Aarhus University, Vejlsøvej 25, 8600, Silkeborg, Denmark

    • Kim Jensen
  3. School of Science and Health, Western Sydney University, Locked Bag 1797, Penrith, NSW, 2751, Australia

    • Clarissa M. House
    •  & John Hunt
  4. Hawkesbury Institute for the Environment, University of Western Sydney, Locked Bay 1797, Penrith, NSW, 2751, Australia

    • Clarissa M. House
    •  & John Hunt


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The authors declare that they have no conflict of interest.

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Correspondence to John Hunt.

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