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Sex-specific effects of glucose deprivation on cell-mediated immunity and reproduction in Siberian hamsters (Phodopus sungorus)

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Abstract

In most species, sexes differ in levels of parasitism. These differences have traditionally been believed to be static, but a capacity for adjusting anti-parasite investments would allow sexes to allocate resources adaptively contingent on environmental conditions. During stressful periods, such as a food shortage, allocation decisions would be mandated in males and females, but the biasing of resources may differ depending on the value of various physiological alternatives to the fitness of each sex. To determine whether sexes sacrifice immune or reproductive capacity when stressed, male and female Siberian hamsters (Phodopus sungorus) were pharmacologically deprived of glucose. Glucose deprivation was expected to compromise immune activity (delayed-type hypersensitivity) more than reproductive capacity in males because male fitness is limited by reproductive opportunities. The opposite was predicted for females because of the greater value of surviving to breed in favorable conditions. Contrary to expectations, glucoprivation compromised immune activity in female, but not male, hamsters. Conversely, glucoprivation reduced male, but not female, reproductive organ masses. These results may reflect the adjustments made by wild hamsters during food shortages, or they may be influenced by the study design; neither sex was permitted to incur other behavioral and physiological costs, such as lactation and parental care. Regardless, our results indicate that sex differences in parasitism are likely to be plastic in many circumstances, but further work in free-living animals is critical to ascertain whether results of the present study are naturally representative.

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References

  • Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368

    Article  PubMed  CAS  Google Scholar 

  • Bilbo SD, Nelson RJ (2003) Sex differences in photoperiodic and stress-induced enhancement of immune function in Siberian hamsters. Brain Behav Immun 17:462–472

    Article  PubMed  CAS  Google Scholar 

  • Bilbo SD, Dhabhar FS, Viswanathan K, Saul A, Yellon SM, Nelson RJ (2002) Short day lengths augment stress-induced leukocyte trafficking and stress-induced enhancement of skin immune function. Proc Natl Acad Sci USA 99:4067–4072

    Article  PubMed  CAS  Google Scholar 

  • Bronson FH (1985) Mammalian reproduction—an ecological perspective. Biol Reprod 32:1–26

    Article  PubMed  CAS  Google Scholar 

  • Chou SH, Kojic LD, Messingham KN, Cunnick JE (1996) Characterization of the effect of 2-deoxy-d-glucose (2-DG) on the immune system. Brain Behav Immun 10:399–416

    Article  PubMed  CAS  Google Scholar 

  • Dark J, Miller DR, Zucker I (1994) Reduced glucose availability induces torpor in Siberian hamsters. Am J Physiol 267:R496–R501

    PubMed  CAS  Google Scholar 

  • Demas GE, DeVries AC, Nelson RJ (1997) Effects of photoperiod and 2-deoxy-d-glucose-induced metabolic stress on immune function in female deer mice. Am J Physiol Regul Integr Comp Physiol 41:R1762–R1767

    Google Scholar 

  • Demas GE, Drazen DL, Nelson RJ (2003) Reductions in total body fat decrease humoral immunity. Proc R Soc Lond B Biol Sci 270:905–911

    Article  Google Scholar 

  • Dhabhar FS, Miller AH, McEwen BS, Spencer RL (1995) Effects of stress on immune cell distribution—dynamics and hormonal mechanisms. J Immunol 154:5511–5527

    PubMed  CAS  Google Scholar 

  • Dreau D, Morton DS, Foster M, Swiggett JP, Sonnenfeld G (1997) Immune alterations in male and female mice after 2-deoxy-d-glucose administration. Physiol Behav 62:1325–1331

    Article  PubMed  CAS  Google Scholar 

  • Dreau D, Morton DS, Foster M, Fowler N, Sonnenfeld G (1998) Effects of 2-deoxy-d-glucose administration on immune parameters in mice. Immunopharmacology 39:201–213

    Article  PubMed  CAS  Google Scholar 

  • Forbes MR (2007) On sex differences in optimal immunity. Trends Ecol Evol 22:111–113

    Article  PubMed  Google Scholar 

  • Furuta I, Porkkaheiskanen T, Scarbrough K, Tapanainen J, Turek FW, Hsueh AJW (1994) Photoperiod regulates testis cell apoptosis in Djungarian hamsters. Biol Reprod 51:1315–1321

    Article  PubMed  CAS  Google Scholar 

  • Geiser F, Heldmaier G (1995) The impact of dietary fats, photoperiod, temperature and season on morphological variables, torpor patterns, and brown adipose-tissue fatty-acid composition of hamsters, Phodopus sungorus. J Comp Physiol B 165:406–415

    Article  PubMed  CAS  Google Scholar 

  • Lee KA (2006) Linking immune defenses and life history at the levels of the individual and species. Integr Comp Biol 46:1000–1015

    Article  CAS  Google Scholar 

  • Martin LB, Han P, Kwong J, Hau M (2006) Cutaneous immune activity varies with physiological state in female house sparrows (Passer domesticus). Physiol Biochem Zool 79:775–783

    Article  PubMed  Google Scholar 

  • Martin LB, Navara KJ, Weil ZM, Nelson RJ (2007) Immunological memory is compromised by food restriction in deer mice, Peromyscus maniculatus. Am J Physiol Regul Integr Comp Physiol 292:R316–R320

    PubMed  CAS  Google Scholar 

  • Martin LB, Weil ZM, Nelson RJ (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philos Trans R Soc Lond B Biol Sci 363:321–339

    Article  PubMed  Google Scholar 

  • McKean KA, Nunney L (2005) Bateman’s principle and immunity: phenotypically plastic reproductive strategies predict changes in immunological sex differences. Evolution 59:1510–1517

    PubMed  Google Scholar 

  • Nagatani S, Bucholtz DC, Murahashi K, Estacio MAC, Tsukamura H, Foster DL, Maeda KI (1996) Reduction of glucose availability suppresses pulsatile luteinizing hormone release in female and male rats. Endocrinology 137:1166–1170

    Article  PubMed  CAS  Google Scholar 

  • Nelson RJ, Demas GE (1996) Seasonal changes in immune function. Q Rev Biol 71:511–548

    Article  PubMed  CAS  Google Scholar 

  • Niklowitz P, Khan S, Bergmann M, Hoffmann K, Nieschlag E (1989) Differential effects of follicle stimulating hormone and luteinizing hormone on Leydig cell function and restoration of spermatogenesis in hypophysectomized and photoinhibited Djungarian hamsters (Phodopus sungorus). Biol Reprod 41:871–880

    Article  PubMed  CAS  Google Scholar 

  • Rolff J (2002) Bateman’s principle and immunity. Proc R Soc Lond B Biol Sci 269:867–872

    Article  Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89

    Article  PubMed  CAS  Google Scholar 

  • Schmid-Hempel P, Ebert D (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18:27–32

    Article  Google Scholar 

  • Schneider JE, Friedenson DG, Hall AJ, Wade GN (1993) Glucoprivation induces anestrus and lipoprivation may induce hibernation in Syrian hamsters. Am J Physiol 264:R573–R577

    PubMed  CAS  Google Scholar 

  • Speakman JR (2000) The cost of living: field metabolic rates of small mammals. Adv Ecol Res 30:177–297

    Google Scholar 

  • Stoehr AM, Kokko H (2006) Sexual dimorphism in immunocompetence: what does life-history theory predict? Behav Ecol 17:751–756

    Article  Google Scholar 

  • Weil ZM, Pyter LM, Martin LB, Nelson RJ (2006) Perinatal photoperiod organizes adult immune responses in Siberian hamsters (Phodopus sungorus). Am J Physiol Regul Integr Comp Physiol 290:R1714–R1719

    PubMed  CAS  Google Scholar 

  • Wynne-Edwards KE (1998) Evolution of parental care in Phodopus: conflict between adaptations for survival and adaptations for rapid reproduction. Am Zool 38:238–250

    Google Scholar 

  • Zuk M (1990) Reproductive strategies and disease susceptibility—an evolutionary viewpoint. Parasitol Today 6:231–233

    Article  PubMed  CAS  Google Scholar 

  • Zuk M, Simmons LW, Rotenberry JT, Stoehr AM (2004) Sex differences in immunity in two species of field crickets. Can J Zool 82:627–634

    Article  Google Scholar 

  • Zysling DA, Demas GE (2007) Metabolic stress suppresses humoral immune function in long day, but not short day, Siberian hamsters (Phodopus sungorus). J Comp Physiol B 177:339–347

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors thank Kristen Navara and Brian Trainor for comments on a previous draft. Funding for this study came from NSF IBN04-16897.

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Correspondence to Lynn B. Martin.

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Communicated by G. Heldmaier.

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Martin, L.B., Weil, Z.M., Bowers, S.L. et al. Sex-specific effects of glucose deprivation on cell-mediated immunity and reproduction in Siberian hamsters (Phodopus sungorus). J Comp Physiol B 178, 623–628 (2008). https://doi.org/10.1007/s00360-008-0253-0

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  • DOI: https://doi.org/10.1007/s00360-008-0253-0

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