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Immune Priming, Fat Reserves, Muscle Mass and Body Weight of the House Cricket is Affected by Diet Composition

  • Systematics, Morphology and Physiology
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Abstract

Some insect species are capable of producing an enhanced immune response after a first pathogenic encounter, a process called immune priming. However, whether and how such ability is driven by particular diet components (protein/carbohydrate) have not been explored. Such questions are sound given that, in general, immune response is dietary dependent. We have used adults of the house cricket Acheta domesticus L. (Orthoptera: Gryllidae) and exposed them to the bacteria Serratia marcescens. We first addressed whether survival rate after priming and nonpriming treatments is dietary dependent based on access/no access to proteins and carbohydrates. Second, we investigated how these dietary components affected fat reserves, muscle mass, and body weight, three key traits in insect fitness. Thus, we exposed adult house crickets to either a protein or a carbohydrate diet and measured the three traits. After being provided with protein, primed animals survived longer compared to the other diet treatments. Interestingly, this effect was also sex dependent with primed males having a higher survival than primed females when protein was supplemented. For the second experiment, protein-fed animals had more fat, muscle mass, and body weight than carbohydrate-fed animals. Although we are not aware of the immune component underlying immune priming, our results suggest that its energetic demand for its functioning and/or consequent survival requires a higher demand of protein with respect to carbohydrate. Thus, protein shortage can impair key survival-related traits related to immune and energetic condition. Further studies varying nutrient ratios should verify our results.

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References

  • Adamo S (1999) Evidence for adaptive changes in egg laying in crickets exposed to bacteria and parasites. Anim Behav 57:117–124

    Article  PubMed  Google Scholar 

  • Adamo SA, Jensen M, Younger M (2001) Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G. integer): trade-offs between immunity and reproduction. Anim Behav 62:417–425

    Article  Google Scholar 

  • Alaux C, Ducloz F, Crauser D, Le Conte Y (2010) Diet effects on honeybee immunocompetence. Biol Lett 6:562–565

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey RC, Byrnes J (1990) A new old method for assessing measurement error in both univariate and multivariate morphometric studies. Syst Zool 39:124–130

    Article  Google Scholar 

  • Barnes H, Blackstock J (1973) Estimations of lipids in marine animals and tissues: detailed investigation on the sulpho phospho vanillin method for total lipids. J Exp Mar Biol Ecol 12:103–118

    Article  CAS  Google Scholar 

  • Bascuñan-García P, Lara C, Córdoba-Aguilar A (2010) Immune investment impairs growth, female reproduction and survival in the house cricket, Acheta domesticus. J Insect Physiol 56:204–211

    Article  PubMed  Google Scholar 

  • Behmer ST, Raubenheimer D, Simpson SJ (2001) Frequency-dependent food selection in locusts: a geometric analysis of the role of nutrient balancing. Anim Behav 61:995–1005

    Article  Google Scholar 

  • Best A, Tidbury H, White A, Boots M (2012) The evolutionary dynamics of within-generation immune priming in invertebrate hosts. J R Soc Interface 10:20120887

    Article  PubMed  Google Scholar 

  • Carroll NV, Longley RW, Roe JH (1956) Determination of glycogen in liver and muscle by use of anthrone reagent. J Biol Chem 220:583–593

    CAS  PubMed  Google Scholar 

  • Chapman RF (2012) The insects: structure and function. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Cisarovsky G, Schmid-Hempel P, Sadd BM (2012) Robustness of the outcome of adult bumblebee infection with a trypanosome parasite after varied parasite exposures during larval development. J Evol Biol 25:1053–1059

    Article  CAS  PubMed  Google Scholar 

  • Contreras Garduño J, Buzatto BA, Serrano-Meneses MA, Nájera-Cordero K, Córdoba-Aguilar A (2008) The size of the red wing spot of the American rubyspot as a heightened condition dependent ornament. Behav Ecol 19:724–732

    Article  Google Scholar 

  • Contreras Garduño J, Rodríguez MC, Rodríguez MH, Alvarado-Delgado A, Lanz-Mendoza H (2013) Cost of immune priming within generations: trade-off between infections and reproduction. Microbes Infect 16:261–267

    Article  PubMed  Google Scholar 

  • Cotter SC, Kruuk LEB, Wilson K (2003) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J Evol Biol 17:421–429

    Article  Google Scholar 

  • Cotter SC, Simpson SJ, Raubenheimer D, Wilson K (2011) Macronutrient balance mediates trade-offs between immune function and life history traits. Funct Ecol 25:186–198

    Article  Google Scholar 

  • Dadd RH (1960) The nutritional requirements of locusts—I. Development of synthetic diets and lipid requirements. J Insect Physiol 4:319–347

    Article  CAS  Google Scholar 

  • Daukste J, Kivleniece I, Krama T, Rantala MJ, Krams I (2012) Senescence in immune priming and attractiveness in a beetle. J Evol Biol 25:1298–1304

    Article  CAS  PubMed  Google Scholar 

  • Dong Y, Taylor HE, Dimopoulos G (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 4(7), e229. doi:10.1371/journal.pbio.0040229

    Article  PubMed  PubMed Central  Google Scholar 

  • Gómez-Díaz E, Jordá M, Peinado MA, Rivero A (2012) Epigenetics of host-pathogen interactions: the road ahead and the road behind. PLoS Pathog 8(11), e1003007

    Article  PubMed  PubMed Central  Google Scholar 

  • González-Santoyo I, Córdoba-Aguilar A (2012) Phenoloxidase: a key component of the insect immune system. Entomol Exp Appl 142:1–16

    Article  Google Scholar 

  • González-Tokman DM, González-Santoyo I, Lanz-Mendoza H, Córdoba Aguilar A (2010) Territorial damselflies do not show immunological priming in the wild. Physiol Entomol 35:364–372

    Article  Google Scholar 

  • Humphries MW, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179

    Article  PubMed  Google Scholar 

  • Jervis MA, Boggs CL, Ferns PN (2005) Egg maturation strategy and its associated trade offs: a synthesis focusing on Lepidoptera. Ecol Entomol 30:359–375

    Article  Google Scholar 

  • Jiménez-Cortés JG, Córdoba-Aguilar A (2013) Condition dependence and trade offs of sexual versus non-sexual traits in an insect. J Ethol 31:275–284

    Article  Google Scholar 

  • Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    Article  PubMed  Google Scholar 

  • Jokela J (2010) Transgenerational immune priming as cryptic parental care. J Anim Ecol 79:305–307

    Article  PubMed  Google Scholar 

  • Lailvaux SP, Irschick DJ (2006) A functional perspective on sexual selection: insights and future prospects. Anim Behav 72:263–273

    Article  Google Scholar 

  • Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc R Soc Lond B 273:823–829

    Article  CAS  Google Scholar 

  • Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697–743

    Article  CAS  PubMed  Google Scholar 

  • Little TJ, Connor BO, Colegrave N, Watt K, Read AF (2003) Maternal transfer of strain-specific immunity in an invertebrate. Curr Biol 13:489–492

    Article  CAS  PubMed  Google Scholar 

  • Lyn JC, Naikkhwah W, Aksenov V, Rollo CD (2011) Influence of two methods of dietary restrictions on life history features and aging of the cricket Acheta domesticus. Age 33:509–522

    Article  PubMed  Google Scholar 

  • MacLeod R, Lind J, Clark J, Creswell W (2007) Mass regulation in response to predation risk can indicate population declines. Ecol Lett 10:945–955

    Article  PubMed  Google Scholar 

  • McWilliams SR, Guglicimo C, Pierce B, Klaasen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393

    Article  Google Scholar 

  • Miller MR, White A, Boots M (2007) Host life span and the evolution of resistance characteristics. Evolution 61:2–14

    Article  PubMed  Google Scholar 

  • Mukherjee K, Twyman RM, Vilcinskas A (2015) Insects as models to study the epigenetic basis of disease. Prog Biophys Mol Biol 118:69–78

    Article  CAS  PubMed  Google Scholar 

  • Nation JL (2016) Insect physiology and biochemistry. CRC, Boca Raton

    Google Scholar 

  • Nava-Sánchez A, Munguía-Steyer R, González-Tokman D, Córdoba-Aguilar A (2015) Does mating activity impair phagocytosis-mediated priming immune response? A test using the house cricket, Acheta domesticus. Acta Ethol 18:295–299

    Article  Google Scholar 

  • Neville PF, Luckey TD (1962) Carbohydrate and roughage requirement of the cricket, Acheta domesticus. J Nutr 78:139–146

    CAS  PubMed  Google Scholar 

  • Nowosielski JW, Patton RL (1965) Life-tables for the house cricket, Acheta domesticus L and the effect of intra-specific factors on longevity. J Insect Physiol 11:201–209

    Article  Google Scholar 

  • Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS (2007) A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 3(3), e26. doi:10.1371/journal.ppat.0030026

    Article  PubMed  PubMed Central  Google Scholar 

  • Plaistow S, Siva-Jothy MT (1996) Energetic constraints and male mate-securing tactics in the damselfly Calopteryx splendens xanthostoma (Charpentier). Proc R Soc Lond 263:1233–1239

    Article  Google Scholar 

  • Ponton F, Lalubin F, Fromont C, Wilson K, Behm C, Simpson SJ (2011) Hosts use altered macronutrient intake to circumvent parasite-induced reduction in fecundity. Int J Parasitol 41:43–50

    Article  CAS  PubMed  Google Scholar 

  • Ponton F, Wilson K, Holmes AJ, Cotter SC, Raubenheimer D, Simpson SJ (2013) Integrating nutrition and immunology: a new frontier. J Insect Physiol 59:130–137

    Article  CAS  PubMed  Google Scholar 

  • Povey S, Cotter SC, Simpson SJ, Lee KP, Wilson K (2009) Can the protein costs of bacterial resistance be offset by altered feeding behaviour? J Anim Ecol 78:437–446

    Article  PubMed  Google Scholar 

  • Povey S, Cotter SC, Simpson SJ, Wilson K (2014) Dynamics of macronutrient self-medication and illness-induced anorexia in virally infected insects. J Anim Ecol 88:245–255

    Article  Google Scholar 

  • R Core Development Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reber A, Chapuisat M (2012) No evidence for immune priming in ants exposed to a fungal pathogen. PLoS One 7(4), e35372. doi:10.1371/journal.pone.0035372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roeder A, Behmer ST (2014) Lifetime consequences of food protein-carbohydrate content for an insect herbivore. Funct Ecol 28:1135–1143

    Article  Google Scholar 

  • Roth O, Kurtz J (2009) Phagocytosis mediates specificity in the immune defence of an invertebrate, the woodlouse Porcellio scaber (Crustacea: Isopoda). Dev Comp Immunol 33:1151–1155

    Article  CAS  PubMed  Google Scholar 

  • Roth O, Joop G, Eggert H, Hilbert J, Daniel J, Schmid-Hempel P, Kurtz J (2010) Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. J Anim Ecol 79:403–413

    Article  PubMed  Google Scholar 

  • Ryder JJ, Siva-Jothy MT (2000) Male calling song provides a reliable signal of immune function in a cricket. Proc R Soc B 267:1171–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50:529–551

    Article  CAS  PubMed  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  CAS  PubMed  Google Scholar 

  • Simmons LW (1986) Female choice in the field cricket Gryllus bimaculatus (De Geer). Anim Behav 34:1463–1470

    Article  Google Scholar 

  • Simpson SJ, Sword GA, Lorch PD, Couzin ID (2006) Cannibal crickets on a forced march for protein and salt. Proc Natl Acad Sci U S A 103:4152–4156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srygley RB, Lorch PD (2011) Weakness in the band: nutrient mediated trade-offs between migration and immunity of Mormon crickets, Anabrus simplex. Anim Behav 81:395–400

    Article  Google Scholar 

  • Srygley RB, Lorch PD (2013) Coping with uncertainty: nutrient deficiencies motivate insect migration at a cost to immunity. Integr Comp Biol 53:1–12

    Article  Google Scholar 

  • Srygley RB, Lorch PD, Simpson SJ, Sword GA (2009) Immediate protein dietary effects on movement and the generalised immunocompetence of migrating Mormon crickets Anabrus simplex (Orthoptera: Tettigoniidae). Ecol Entomol 34:663–668

    Article  Google Scholar 

  • Triggs A, Knell RJ (2011) Interactions between environmental variables determine immunity in the Indian meal moth Plodia interpunctella. J Anim Ecol 81:386–394

    Article  PubMed  Google Scholar 

  • Triggs A, Knell RJ (2012) Parental diet has strong transgenerational effects on offspring immunity. Funct Ecol 26:1409–1417

    Article  Google Scholar 

  • Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M, Kondo M, Rebel VI, Schmucker D (2005) Extensive diversity of lg-superfamily proteins in the immune system of insects. Science 309:1874–1878

    Article  CAS  PubMed  Google Scholar 

  • Yezerinac SM, Lougheed SC, Handford P (1992) Measurement error and morphometric studies: statistical power and observer experience. Syst Biol 41:471–482

    Article  Google Scholar 

  • Zanchi C, Troussard JP, Martinaud G, Moreau J, Moret Y (2011) Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect. J Anim Ecol 80:1174–1183

    Article  PubMed  Google Scholar 

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Acknowledgments

This paper is a partial fulfillment of the requirement for the doctoral degree of A. Nava-Sánchez at the graduate program Doctorado en Ciencias Biomédicas of the Universidad Nacional Autónoma de México. Thanks to L. Cordero Méndez (Facultad de Estudios Superiores Iztacala) who provided the crickets, R. I. Martínez-Becerril for logistic support, and M. A. Moreno-García and M. Tapia R. for key assistance in the laboratory.

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Correspondence to A Córdoba-Aguilar.

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Edited by Guilherme D Rossi – UNESP

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Córdoba-Aguilar, A., Nava-Sánchez, A., González-Tokman, D.M. et al. Immune Priming, Fat Reserves, Muscle Mass and Body Weight of the House Cricket is Affected by Diet Composition. Neotrop Entomol 45, 404–410 (2016). https://doi.org/10.1007/s13744-016-0391-0

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