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Life History Features and Aging Rates: Insights from Intra-specific Patterns in the Cricket Acheta domesticus

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Abstract

We carried out 42 lifetime studies of male and female crickets (Acheta domesticus) treated with different diets, nutritional supplements and dietary restriction (84 groups). Maximal longevity of controls averaged ~118 days and various treatments obtained lifespans of 86–257 days. Overall, greater longevity was most strongly associated with slower growth and delayed maturation. Early nymphal mortality and early fasting stress were also associated with life extension. The opposite associations of growth rate and stress resistance with maximal life span are consistent with modulation of aging by the target of rapamycin (growth) and forkhead transcription factors (stress resistance). Unlike inter-specific comparisons or intra-specific comparisons of species differentiated into strains or breeds, body size did not emerge as a strong predictor of cricket longevity. Rather, targeted body size was strongly compensated for in crickets whereas most genetically differentiated breeds of mice, rats, horses and dogs express breed-specific sizes and growth rates. Both extension of the juvenile period and adult lifetime contributed to increases in maximal longevity of crickets, although for extreme life extension, extended immaturity was a greater factor than adult life span. We discuss the inter- and intra-specific allometry of life histories from a perspective of aging and suggest that inter-specific variance may particularly reflect exogenous mortality risks whereas intra-specific aging is dominated by constraints on productivity.

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References

  • Aksenov, V., Long, J., Liu, J., Szechtman, H., Khanna, P., & Matravadia, S. (2011). A complex dietary supplement augments spatial learning, brain mass, and mitochondrial electron transport chain activity in aging mice. Age. doi:10.1007/s11357-011-9325-2 (Ahead of print).

  • Aksenov, V., Long, J., Lokuge, S., Foster, J. A., Liu, J., & Rollo, C. D. (2010). A dietary supplement ameliorates locomotor, neurotransmitter and mitochondrial aging. Experimental Biology and Medicine, 335, 66–76.

    Article  Google Scholar 

  • Archer, C. R., Royle, N., South, S., Selman, C., & Hunt, J. (2009). Nutritional geometry provides food for thought. Journals of Gerontology A Biological Science and Medical Science, 64A, 956–959.

    Article  Google Scholar 

  • Austad, S. N. (2010). Animal size, metabolic rate, and survival, among and within species. In N. S. Wolf (Ed.), The comparative biology of aging (Vol. 27, pp. 27–41). New York: Springer.

  • Bateman, P. W., Ferguson, J. W. H., & Yetman, C. A. (2005). Courtship and copulation, but not ejaculates, reduce the longevity of female field crickets (Gryllus bimaculatus). Journal of Zoology,. doi:10.1111/j.1469-7998.2006.00054.x.

    Google Scholar 

  • Behmer, S. T. (2009). Insect herbivore nutrient regulation. Annual Review of Entomology, 54, 165–187.

    Article  PubMed  CAS  Google Scholar 

  • Booth, D. T., & Kiddell, K. (2007). Temperature and the energetics of development in the house cricket (Acheta domesticus). Journal of Insect Physiology, 53, 950–953.

    Article  PubMed  CAS  Google Scholar 

  • Bowen, R. L., & Atwood, C. S. (2004). Living and dying for sex. Gerontology, 50, 265–290.

    Article  PubMed  Google Scholar 

  • Burpee, D. M., & Sakaluk, S. K. (1993). Repeated matings offset costs of reproduction in female crickets. Evolutionary Ecology, 7, 240–250.

    Article  Google Scholar 

  • Calder, W. A. (1984). Size, function, and life history. Cambridge: Harvard University Press.

    Google Scholar 

  • Carey, J. R., Harshman, L., Liedo, P., Muller, H. G., Wang, J. L., & Zhang, Z. (2008). Longevity-fertility trade-offs in the Tephritid fruit fly, Anastrepha ludens, across dietary-restriction gradients. Aging Cell, 7, 470–477.

    Article  PubMed  CAS  Google Scholar 

  • Case, T. J. (1978). On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. Quarterly Review of Biology, 53, 243–276.

    Article  PubMed  CAS  Google Scholar 

  • Castrillo, J. I., Zeef, L. A., Hoyle, D. C., Zhang, N., Hayes, A., Gardner, D. C. J., et al. (2007). Growth control of the eukaryote cell: A systems biology study in yeast. Journal of Biology, 6, 4. doi:10.1186/jbiol54.

    Article  PubMed  Google Scholar 

  • Charnov, E. L. (1993). Life history invariants. Oxford: Oxford University Press.

    Google Scholar 

  • Cutler, R. G. (1984a). Antioxidants, aging and longevity. In W. A. Pryor (Ed.), Free radicals in biology (Vol. VI, pp. 371–428). New York: Academic Press.

    Google Scholar 

  • Cutler, R. G. (1984b). Evolutionary biology of aging and longevity in mammalian species. In J. E. Johnson (Ed.), Aging and cell function (pp. 1–147). New York: Plenum Press.

    Google Scholar 

  • Dabour, N., Bando, T., Nakamura, T., Miyawaki, K., Mito, T., Ohuchi, H., et al. (2011). Cricket body size is altered by systemic RNAi against insulin signaling components and epidermal growth factor receptor. Development Growth and Differentiation, 53, 857–869.

    Article  CAS  Google Scholar 

  • de Magalhaes, J. P., & Church, G. M. (2005). Genomes optimize reproduction: Aging as a consequence of the developmental program. Physiology, 20, 252–259.

    Article  PubMed  Google Scholar 

  • de Magalhaes, J. P., Costa, J., & Church, G. M. (2007). An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. Journals of Gerontology, 62A, 149–160.

    Google Scholar 

  • Dobson, F. S. (2007). A life-style view of life history variation. Proceedings of the National Academy of the United States of America, 104, 17565–17566.

    Article  CAS  Google Scholar 

  • Esperk, T., Tammaru, T., & Nylin, S. (2007). Intraspecific variability in number of larval instars in insects. Journal of Economic Entomology, 100, 627–645.

    Article  PubMed  Google Scholar 

  • Fanson, B. G., Weldon, C. W., Perez-Staples, D., Simpson, S. J., & Taylor, P. W. (2009). Nutrients, not caloric restriction, extend lifespan in Queensland fruit flies (Bactrocera tryoni). Aging Cell, 8, 514–523.

    Article  PubMed  CAS  Google Scholar 

  • Finch, C. E. (1976). The regulation of physiological changes during mammalian aging. Quarterly Review of Biology, 51, 49–83.

    Article  PubMed  CAS  Google Scholar 

  • Galis, F., Sluijs, I. V. D., Dooren, T. J. M. V., Metz, J. A. J., & Nussbaumer, M. (2007). Do large dogs die young? Journal of Experimental Zoology, 308B, 119–126.

    Article  Google Scholar 

  • Glazier, D. S. (1999). Trade-offs between reproductive and somatic (storage) investments in animals: A comparative test of the Van Noodwijk and De Jong model. Evolutionary Ecology, 13, 539–555.

    Article  Google Scholar 

  • Glazier, D. S. (2010). A unifying explanation for diverse metabolic scaling in animals and plants. Biological Reviews, 85, 111–138.

    Article  PubMed  Google Scholar 

  • Grandison, R. C., Piper, M. D. W., & Partridge, L. (2009). Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature, 462, 1061–1064.

    Article  PubMed  CAS  Google Scholar 

  • Hamilton, M. J., Davidson, A. D., Sibly, R. M., & Brown, J. H. (2011). Universal scaling of production rates across mammalian lineages. Proceedings of the Royal Society B, 278, 560–566.

    Article  PubMed  Google Scholar 

  • Hunt, J., Brooks, R., Jennions, M. D., Smith, M. J., Bentsen, C. L., & Bussiere, L. F. (2004). High-quality male field crickets invest heavily in sexual display but die young. Nature, 432, 1024–1027.

    Article  PubMed  CAS  Google Scholar 

  • Hunt, J., Jennions, M. D., Spyrou, N., & Brooks, R. (2006). Artificial selection on male longevity influences age-dependent reproductive effort in the black field cricket Teleogryllus commodus. American Naturalist, 168, E72–E86.

    Article  PubMed  Google Scholar 

  • Ja, W. W., Carvalho, G. B., Zid, B. M., Mak, E. M., Brummel, T., & Benzer, S. (2009). Water- and nutrient-dependent effects of dietary restriction on Drosophila lifespan. Proceedings National Academy of Sciences of the United States of America, 106, 18633–18637.

    Article  CAS  Google Scholar 

  • Kearney, M., Simpson, S. J., Raubenheimer, D., & Helmuth, B. (2010). Modelling the ecological niche from functional traits. Proceedings of the Royal Society of London B Biological Sciences, 365, 3469–3483.

    Google Scholar 

  • Kirkwood, J. K. (1985). The influence of size on the biology of the dog. Journal of Small Animal Practice, 26, 97–110.

    Article  Google Scholar 

  • Kirkwood, T. B. L. (2008). A systematic look at an old problem. Nature, 451, 644–647.

    Article  PubMed  CAS  Google Scholar 

  • Kirkwood, T. B. L., & Holliday, R. (1979). The evolution of ageing and longevity. Proceedings of the Royal Society of London B, 205, 531–546.

    Article  CAS  Google Scholar 

  • Lee, K. P., Simpson, S. J., Clissold, F. J., Brooks, R., Ballard, J. W. O., Taylor, P. W., et al. (2008). Lifespan and reproduction in Drosophila: New insights from nutritional geometry. Proceedings of the National Academy of the United States of America, 105, 2498–2503.

    Article  CAS  Google Scholar 

  • Lemon, J. A., Boreham, D. R., & Rollo, C. D. (2003). A dietary supplement abolishes age-related cognitive decline in transgenic mice expressing elevated free radical processes. Experimental Biology and Medicine, 228, 800–810.

    PubMed  CAS  Google Scholar 

  • Lemon, J. A., Boreham, D. R., & Rollo, C. D. (2005). A complex dietary supplement extends longevity of mice. Journals of Gerontology, 60A, 275–279.

    CAS  Google Scholar 

  • Lemon, J. A., Rollo, C. D., & Boreham, D. R. (2008a). Elevated DNA damage in a mouse model of oxidative stress: Impacts of ionizing radiation and a protective dietary supplement. Mutagenesis, 23, 473–482.

    Article  PubMed  CAS  Google Scholar 

  • Lemon, J. A., Rollo, C. D., McFarlane, N. M., & Boreham, D. R. (2008b). Radiation-induced apoptosis in mouse lymphocytes is modified by a complex dietary supplement: The effect of genotype and gender. Mutagenesis, 23, 465–472.

    Article  PubMed  CAS  Google Scholar 

  • Lyn, J., Naik, W., Aksenov, V., & Rollo, C. D. (2011). Development of the cricket Acheta domesticus as a model of aging. AGE, 33, 509–522.

    Article  PubMed  Google Scholar 

  • Maklakov, A. A., Hall, M. D., Simpson, S. J., Dessmann, J., Clissold, F. J., Zajitschek, F., et al. (2009). Sex differences in nutrient-dependent reproductive ageing. Aging Cell, 8, 324–330.

    Article  PubMed  CAS  Google Scholar 

  • Maklakov, A. A., Simpson, S. J., Zajitschek, F., Hall, M. D., Dessmann, J., Clissold, F., et al. (2008). Sex-specific fitness effects of nutrient intake on reproduction and lifespan. Current Biology, 18, 1062–1066.

    Article  PubMed  CAS  Google Scholar 

  • McCay, C. M., Pope, F., & Lunsford, W. (1956). Experimental prolongation of the life span. Bulletin of the New York Academy of Medicine, 32, 91–101.

    Article  PubMed  CAS  Google Scholar 

  • McFarlane, J. E., Amit, I., & Sixeves, E. (1984). Studies on the group effect in Acheta domesticus (L.) using artificial diets. Journal of Insect Physiology, 30, 103–107.

    Article  CAS  Google Scholar 

  • Miller, R. A., Harper, J. M., Dysko, R. C., Durkee, S. J., & Austad, S. N. (2002). Longer life spans and delayed maturation in wild-derived mice. Experimental Biology and Medicine, 227, 500–508.

    PubMed  CAS  Google Scholar 

  • Okada, K., Pitchers, W. R., Sharma, M. D., Hunt, J., & Hosken, D. J. (2010). Longevity, calling effort, and metabolic rate in two populations of cricket. Behavioral Ecology and Sociobiology, 65, 1773–1778.

    Article  Google Scholar 

  • Ooka, H., Segall, P. E., & Timiras, P. S. (1988). Histology and survival in age-delayed low-tryptophan-fed rats. Mechanisms of Ageing and Development, 43, 79–98.

    Article  PubMed  CAS  Google Scholar 

  • Ophir, A. G., Schrader, S. B., & Gilooly, J. F. (2010). Energetic cost of calling: General constraints and species-specific differences. Journal of Evolutionary Ecology, 23, 1564–1569.

    CAS  Google Scholar 

  • Partridge, L., Piper, M. D. W., & Mair, W. (2005). Dietary restriction in Drosophila. Mechanisms of Ageing and Development, 126, 938–950.

    Article  PubMed  CAS  Google Scholar 

  • Patronek, G. J., Waters, D. J., & Glickman, L. T. (1997). Comparative longevity of pet dogs and humans: Implications for gerontology research. Journals of Gerontolology A Biological Sciences and Medical Sciences, 52A, B171–B178.

    Article  Google Scholar 

  • Pearl, R. (1928). The rate of living. London: University of London Press.

    Google Scholar 

  • Peters, R. H. (1983). The ecological implications of body size. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Pletcher, S. D., Khazaeli, A. A., & Curtsinger, J. W. (2000). Why do life spans differ? Partitioning mean longevity differences in terms of age-specific mortality parameters. Journals of Gerontology, 55A, B381–B389.

    Google Scholar 

  • Price, P. W. (1974). Strategies for egg production. Evolution, 28, 76–84.

    Article  Google Scholar 

  • Renucci, M., Strambi, C., Strambi, A., Augier, R., & Charpin, P. (1990). Ovaries and regulation of juvenile hormone titer in Acheta domesticus L. (Orthoptera). General and Comparative Endocrinology, 78, 137–149.

    Article  PubMed  CAS  Google Scholar 

  • Ricklefs, R. E. (2000). Intrinsic aging-related mortality in birds. Journal of Avian Biology, 31, 103–111.

    Article  Google Scholar 

  • Ricklefs, R. E. (2010). Life-history connections to rates of aging in terrestrial vertebrates. Proceedings of the National Academy of the United States of America, 107, 10314–10319.

    Article  CAS  Google Scholar 

  • Rollo, C. D. (1994). Phenotypes: Their epigenetics, ecology and evolution. London: Chapman and Hall.

    Google Scholar 

  • Rollo, C. D. (2002). Growth negatively impacts the life span of mammals. Evolution and Development, 4, 55–61.

    Article  PubMed  Google Scholar 

  • Rollo, C. D. (2007a). The evolutionary ecology of body size with special reference to allometry and survivorship. In T. Samaras (Ed.), Human body size and the laws of scaling (pp. 213–234). New York: Nova Scientific Publishing.

    Google Scholar 

  • Rollo, C. D. (2007b). Multidisciplinary aspects of regulatory systems relevant to multiple stressors: Aging, xenobiotics and radiation. In C. Mothersill (Ed.), Multiple stressors: A challenge for the future (pp. 185–224). New York: Springer.

    Chapter  Google Scholar 

  • Rollo, C. D. (2010). Aging and the mammalian regulatory triumvirate. Aging and Disease, 1, 105–138. http://www.aginganddisease.org/issue-2.html.

  • Rollo, C. D. (2011). Circadian redox regulation. In K. Pantopoulos & H. M. Schipper (Eds.), Principles of free radical biomedicine. New York: Nova Scientific Publishing.

    Google Scholar 

  • Samaras, T. (Ed.). (2007). Human body size and the laws of scaling. New York: Nova Scientific Publishing.

    Google Scholar 

  • Schmaulhausen, I. I. (1949). Factors of evolution: The theory of stabilizing selection. Philadelphia: Blakiston.

    Google Scholar 

  • Schmidt-Nielson, K. (1984). Scaling: Why is animal size so important?. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Sibly, J. R., & Brown, J. H. (2007). Effects of body size and lifestyle on evolution of mammal life histories. Proceedings of the National Academy of Sciences, 104, 17707–17712.

    Article  CAS  Google Scholar 

  • Simpson, S. J., & Raubenheimer, D. (2010). The nutritional geometry of aging. In A. V. Everitt, S. I. S. Rattan, D. G. Le Couteur, & R. de Cabo (Eds.), Calorie restriction, aging and longevity (pp. 111–122). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Skorupa, D. A., Dervisefendic, A., Zwiener, J., & Pletcher, S. D. (2008). Dietary composition specifies consumption, obesity, and lifespan in Drosophila melanogaster. Aging Cell, 7, 478–490.

    Article  PubMed  CAS  Google Scholar 

  • Sutter, N. B., Bustamante, C. D., Chase, K., Gray, M. M., Zhao, K., Zhu, L., et al. (2007). A single IGF1 allele is a major determinant of small size in dogs. Science, 316, 112–115.

    Article  PubMed  CAS  Google Scholar 

  • Tanaka, S. (2001). Effects of suppressed oviposition activity and flight muscle histolysis on food consumption and ovarian development in a wing-dimorphic cricket: An explanation for sporadic conclusions related to physiological trade-offs. Journal of Insect Physiology, 47, 83–94.

    Article  PubMed  CAS  Google Scholar 

  • Tu, M. P., & Tatar, M. (2003). Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell, 2, 327–333.

    Article  PubMed  CAS  Google Scholar 

  • Van Noordwijk, A. J., & de Jong, G. (1986). Acquisition and allocation of resources: Their influence on variation in life history tactics. American Naturalist, 128, 137–142.

    Article  Google Scholar 

  • Wagner, W. E., Jr, & Harper, C. J. (2003). Female life span and fertility are increased by the ejaculates of preferred males. Evolution, 57, 2054–2066.

    PubMed  Google Scholar 

  • Wagner, W. E., Jr, Kelley, R. J., Tucker, K. R., & Harper, C. J. (2001). Females receive a life-span benefit from male ejaculates in a field cricket. Evolution, 55, 994–1001.

    Article  PubMed  Google Scholar 

  • Wedell, N., Tregenza, T., & Simmons, L. W. (2008). Nuptial gifts fail to resolve a sexual conflict in an insect. BMC Evolutionary Biology, 8, 204. doi:10.1186/1471-2148-8-204.

    Article  PubMed  Google Scholar 

  • Williams, G. C. (1957). Pleiotropy, natural selection and the evolution of senescence. Evolution, 11, 398–411.

    Article  Google Scholar 

  • Woodring, J. P. (1983). Control of moulting in the house cricket, Acheta domesticus. Journal Insect Physiology, 29, 461–464.

    Article  CAS  Google Scholar 

  • Woodring, J. P., Roe, R. M., & Clifford, C. W. (1977). Relation of feeding, growth, and metabolism to age in the larval, female house cricket. Journal of Insect Physiology, 23, 207–212.

    Article  PubMed  CAS  Google Scholar 

  • Yu, B. B. (1996). Aging and oxidative stress: Modulation by dietary restriction. Free Radical Biology and Medicine, 21, 651–668.

    Article  PubMed  CAS  Google Scholar 

  • Zajitschek, F., Bonduriansky, R., Zajitschek, S. R. K., & Brooks, R. C. (2009a). Sexual dimorphism in life history: Age, survival, and reproduction in male and female field crickets Teleogryllus commodus under seminatural conditions. American Naturalist, 173, 792–802.

    Article  PubMed  Google Scholar 

  • Zajitschek, F., Hunt, J., Jennions, M. D., Hall, M. D., & Brooks, R. C. (2009b). Effects of juvenile and adult diet on ageing and reproductive effort of male and female black field crickets, Teleogryllus commodus. Functional Ecology, 23, 602–611.

    Article  Google Scholar 

  • Zwaan, B., Bijlsma, R., & Hoekstra, R. F. (1995). Direct selection on life span in Drosophila melanogaster. Evolution, 49, 649–659.

    Article  Google Scholar 

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Acknowledgments

We thank Warren Fingrut, Sherif Yani, Alaif Naima, Sonya Sidhu, and Wida Naikkhwah for contributions to our research program related to this analysis. We also thank two anonymous reviewers for their very constructive direction. This research was funded by a grant to CDR from the Natural Sciences and Engineering Research Council of Canada.

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  1. Deptartment of Biology, McMaster University, 1280 Main St W., Hamilton, ON, L8S 4K1, Canada

    Janice Lyn, Vadim Aksenov, Zillon LeBlanc & C. David Rollo

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Correspondence to C. David Rollo.

Appendix I: Composition of diets

Appendix I: Composition of diets

  • Guinea pig diet Living World ® Extrusion Guinea Pig Diet: Protein 16%, Fat 3.5%, Fibre 12.5%, Ash 6%, Calcium 0.8%, Phosphorus 0.6%, Copper sulphate 15 mg/kg, Vitamin A 6000 IU/kg, Vitamin C 300 mg/kg, Vitamin D3 520 IU/kg, Vitamin E 24 IU/kg

  • Cricket Gutload © Repashy Superfoods: Protein 20%; Fat 4.5%; Fiber 10%; Calcium 8%; Phosphorous 0.5%; Vitamin D3 20 IU/g; Vitamin A 200 IU/g; Beta carotene 5 mg/g; Choline 6 mg/g; Vitamin C 2.5 mg/g; Vitamin E 0.1 mg/g; B vitamins (B1, B2, B3, B5, B6, B7, B12) 0.83 mg/g; Vitamin K 0.03 mg/g).

  • Cat food Petcurean Go! Natural ® Cat Food: Protein 32%, Fat 20%, Fibre 3%, Moisture 9%, Ash 5.9%, Omega −6 5.8%, Omega 3 0.86%, Taurine 0.19%, Magnesium 0.09%, Vitamin E 200 IU/Kg

  • Kitten food Purina Kitten Chow: Protein (Min) 40%, Fat 12.5%, Fibre 4%, Moisture 12%, Calcium 1.2%, Phosphorus 1.1%, Taurine 0.125%

  • Whey protein diet Whey protein mixed with Cricket Gutload© to achieve an overall level of 40% protein.

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Lyn, J., Aksenov, V., LeBlanc, Z. et al. Life History Features and Aging Rates: Insights from Intra-specific Patterns in the Cricket Acheta domesticus . Evol Biol 39, 371–387 (2012). https://doi.org/10.1007/s11692-012-9160-0

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