Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-24T02:32:32.355Z Has data issue: false hasContentIssue false

Thermal developmental plasticity affects body size and water conservation of Drosophila nepalensis from the Western Himalayas

Published online by Cambridge University Press:  13 June 2014

R. Parkash
Affiliation:
Department of Genetics, Maharshi Dayanand University, Rohtak 124001, India
C. Lambhod*
Affiliation:
Department of Genetics, Maharshi Dayanand University, Rohtak 124001, India
D. Singh
Affiliation:
Department of Genetics, Maharshi Dayanand University, Rohtak 124001, India
*
*Author for correspondence Phone: +91-9996074219 E-mail: chanda.malik071@gmail.com

Abstract

In the Western Himalayas, Drosophila nepalensis is more abundant during the colder and drier winter than the warmer rainy season but the mechanistic bases of such adaptations are largely unknown. We tested effects of developmental plasticity on desiccation-related traits (body size, body melanization and water balance traits) that may be consistent with changes in seasonal abundance of this species. D. nepalensis grown at 15°C has shown twofold higher body size, greater melanization (∼15-fold), higher desiccation resistance (∼55 h), hemolymph as well as carbohydrate content (twofold higher) as compared with corresponding values at 25°C. Water loss before succumbing to death was much higher (∼16%) at 15°C than 25°C. Developmental plastic effects on body size are associated with changes in water balance-related traits (bulk water, hemolymph and dehydration tolerance). The role of body melanization was evident from the analysis of assorted darker and lighter flies (from a mass culture of D. nepalensis reared at 21°C) which lacked differences in dry mass but showed differences in desiccation survival hours and rate of water loss. For adult acclimation, we found a slight increase in desiccation resistance of flies reared at lower growth temperature, whereas in flies reared at 25°C such a response was lacking. In D. nepalensis, greater developmental plasticity is consistent with its contrasting levels of seasonal abundance. Finally, in the context of global climate change in the Western Himalayas, D. nepalensis seems vulnerable in the warmer season due to lower adult as well as developmental acclimation potential at higher growth temperature (25°C).

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Angilletta, M.J. (2009) Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford, UK, Oxford University Press.Google Scholar
Atkinson, D. (1994) Temperature and organism size – a biological law for ectotherms? Advances in Ecological Research 25, 158.CrossRefGoogle Scholar
Bale, J.S. (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Philosophical Transactions of the Royal Society London B 357, 849862.Google Scholar
Bazinet, A.L., Marshall, K.E., MacMillan, H.A., Williams, C.M. & Sinclair, B.J. (2010) Rapid changes in desiccation resistance in Drosophila melanogaster are facilitated by changes in cuticular permeability. Journal of Insect Physiology 56, 20062012.Google Scholar
Benoit, J.B., Yoder, J.A., Rellinger, E.J., Ark, J.T. & Keeney, G.D. (2005) Prolonged maintenance of water balance by adult females of the American spider beetle, Mezium affine Boieldieu, in the absence of food and water resources. Journal of Insect Physiology 51, 565573.Google Scholar
Chapman, R.F. (1998) The Insects: Structure and Function. Cambridge, UK, Cambridge University Press.Google Scholar
Chippindale, A.K., Gibbs, A.G., Sheik, M., Yee, K.J., Djawdan, M., Bradley, T.J. & Rose, M.R. (1998) Resource allocation and the evolution of desiccation resistance in laboratory selected Drosophila melanogaster . Evolution 52, 13421352.Google Scholar
Chown, S.L. & Klok, C.J. (2003) Water-balance characteristics respond to changes in body size in subantarctic weevils. Physiological and Biochemical Zoology 76, 634643.Google Scholar
Chown, S.L. & Nicolson, S.W. (2004) Insect Physiological Ecology: Mechanisms and Patterns. Oxford, Oxford University Press.Google Scholar
Chown, S.L., Scholtz, C.H., Klok, C.J., Joubert, F.J. & Coles, K.S. (1995) Ecophysiology, range contraction and survival of a geographically restricted African dung-beetle (Coleoptera: Scarabaeidae). Functional Ecology 9, 3039.Google Scholar
Chown, S.L., Le Lagadec, M.D. & Scholtz, C.H. (1999) Partitioning variance in a physiological trait: desiccation resistance in keratin beetles (Coleoptera, Trogidae). Functional Ecology 13, 838844.Google Scholar
Cohen, A.C., March, R.B. & Pinto, J.D. (1986) Effects of water stress and rehydration in hemolymph volume and amino acid content in the blister beetle Cysteodemus armatus . Comparative Biochemistry and Physiology A 85, 743746.Google Scholar
Djawdan, M., Chippindale, A.K., Rose, M.R. & Bradley, T.J. (1998) Metabolic reserves and evolved stress resistance in Drosophila melanogaster . Physiological and Biochemical Zoology 71, 584594.Google Scholar
Edney, E.B. (1977) Water Balance in Land Arthropods. Berlin, Springer.Google Scholar
Folk, D.G. & Bradley, T.J. (2005) Adaptive evolution in the lab: unique phenotypes in the fruit flies comprise a fertile field of study. Integrative and Comparative Biology 45, 492499.Google Scholar
Folk, D.G., Han, C. & Bradley, T.J. (2001) Water acquisition and partitioning in Drosophila melanogaster: effects of selection for desiccation resistance. Journal of Experimental Biology 204, 33233331.Google Scholar
Gibbs, A.G. (2002) Water balance in desert Drosophila: lessons from non-charismatic microfauna. Comparative Biochemistry and Physiology A 133, 781789.Google Scholar
Gibbs, A.G. & Matzkin, L.M. (2001) Evolution of water balance in the genus Drosophila . Journal of Experimental Biology 204, 23312338.Google Scholar
Gibbs, A.G., Chippindale, A.K. & Rose, M.R. (1997) Physiological mechanisms of evolved desiccation resistance in Drosophila melanogaster . Journal of Experimental Biology 200, 18211832.CrossRefGoogle ScholarPubMed
Gibbs, A.G., Fukuzato, F. & Matzkin, L.M. (2003) Evolution of water conservation mechanisms in desert Drosophila . Journal of Experimental Biology 206, 11831192.Google Scholar
Graves, J.L., Toolson, E.C., Jeong, C., Vu, L.N. & Rose, M.R. (1992) Desiccation, flight, glycogen, and postponed senescence in Drosophila melanogaster . Physiological and Biochemical Zoology 65, 268286.Google Scholar
Hadley, N.F. (1994) Water Relations of Terrestrial Arthropods. San Diego, CA, Academic Press.Google Scholar
Hoffmann, A.A. (1990) Acclimation for desiccation resistance in Drosophila melanogaster and the association between acclimation responses and genetic variation. Journal of Insect Physiology 36, 885891.Google Scholar
Hoffmann, A.A. (1991) Acclimation for desiccation resistance in Drosophila: species and population comparisons. Journal of Insect Physiology 37, 757762.Google Scholar
Hoffmann, A.A. & Harshman, L.G. (1999) Desiccation and starvation resistance in Drosophila: patterns of variation at the species, population and intrapopulation levels. Heredity 83, 637643.Google Scholar
Hoffmann, A.A. & Parsons, P.A. (1989) Selection for increased desiccation resistance in Drosophila melanogaster: additive genetic control and correlated responses for other stresses. Genetics 122, 837845.Google Scholar
Hoffmann, A.A., Sørensen, J.G. & Loeschcke, V. (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. Journal of Thermal Biology 28, 175216.CrossRefGoogle Scholar
Marron, M.T., Markow, T.A., Kain, K.J. & Gibbs, A.G. (2003) Effects of starvation and desiccation on energy metabolism in desert and mesic Drosophila . Journal of Insect Physiology 49, 261270.Google Scholar
Matzkin, L.M., Watts, T.D. & Markow, T.A. (2007) Desiccation resistance in four Drosophila species: sex and population effects. Fly 1, 268273.Google Scholar
Mousseau, T.A., Sinervo, B. & Endler, J.A. (2000) Adaptive Genetic Variation in the Wild. New York, Oxford University Press.CrossRefGoogle Scholar
Okada, T. (1955) Fauna and flora of Nepal Himalaya. I. Drosophila . pp. 387390 in Kihara, H. (Ed.) Scientific Results of the Japanese Expeditions to Nepal Himalaya, 1952–1953. Vol. 1. Kyoto, Fauna and Flora Research Society.Google Scholar
Parkash, R., Rajpurohit, S. & Ramniwas, S. (2008 a) Changes in body melanisation and desiccation resistance in highland vs. lowland populations of Drosophila melanogaster . Journal of Insect Physiology 54, 10501056.Google Scholar
Parkash, R., Ramniwas, S., Rajpurohit, S. & Sharma, V. (2008 b) Variations in body melanization impact desiccation resistance in Drosophila immigrans from western Himalayas. Journal of Zoology 276, 219227.Google Scholar
Parkash, R., Singh, S. & Ramniwas, S. (2009) Seasonal changes in humidity level in the tropics impact body color polymorphism and desiccation resistance in Drosophila jambulina – evidence for melanism-desiccation hypothesis. Journal of Insect Physiology 55, 358368.Google Scholar
Parkash, R., Kalra, B. & Sharma, V. (2010) Impact of body melanisation on contrasting levels of desiccation resistance in a circumtropical and a generalist Drosophila species. Evolutionary Ecology 24, 207225.Google Scholar
Parkash, R., Aggarwal, D.D., Singh, D., Lambhod, C. & Ranga, P. (2013) Divergence of water balance mechanisms in two sibling species (Drosophila simulans and D. melanogaster): effects of growth temperatures. Journal of Comparative Physiology B 183, 359378.Google Scholar
Parshad, R. & Paika, I.J. (1964) Drosophilid survey of India. II. Taxonomy and cytology of the subgenus Sophophora (Drosophila). Research Bulletin of Punjab University 15, 225252.Google Scholar
Rajpurohit, S., Parkash, R. & Ramniwas, S. (2008) Climatic changes and shifting species boundaries of drosophilids in the Western Himalaya. Acta Entomologica Sinica 51, 328335.Google Scholar
Rajpurohit, S., Nedved, O. & Gibbs, A.G. (2013) Meta-analysis of geographical clines in desiccation tolerance of Indian drosophilids. Comparative Biochemistry and Physiology A 164, 391398.Google Scholar
Ramniwas, S., Kajla, B., Dev, K. & Parkash, R. (2013) Direct and correlated responses to laboratory selection for body melanisation in Drosophila melanogaster: support for the melanisation-desiccation resistance hypothesis. Journal of Experimental Biology 216, 12441254.Google Scholar
Rourke, B.C. (2000) Geographical and altitudinal variation in water balance and metabolic rate in a California grasshopper, Melanoplus sanguinipes . Journal of Experimental Biology 203, 26992712.Google Scholar
Schmidt-Nielsen, K. (1990) Animal Physiology: Adaptation and Environment. 4th edn. New York, Cambridge University Press.Google Scholar
Toolson, E.C. (1984) Inter individual variations in epicuticular hydrocarbon composition and water loss rates of the cicada, Tibicen dealbatus (Homoptera: Cicadidae). Physiological Zoology 57, 550556.Google Scholar
Wharton, G.W. (1985) Water balance of insects. pp. 565603 in Kerkut, G.A. & Gilbert, L.I. (Eds) Comprehensive Insect Physiology, Biochemistry and Pharmacology. Vol. 4. Oxford, Pergamon Press.Google Scholar
Willmer, P., Stone, G. & Johnston, I. (2000) Environmental Physiology of Animals. Oxford, Blackwell Science.Google Scholar
Willott, S.J. & Hassall, M. (1998) Life history responses of British grasshoppers (Orthoptera: Acrididae) to temperature change. Functional Ecology 12, 232241.Google Scholar