Adaptive Evolution in the Lab: Unique Phenotypes in Fruit Flies Comprise a Fertile Field of Study1

Abstract Laboratory selection for desiccation resistance, which has been imposed on five replicate populations of Drosophila melanogaster for >200 generations, has resulted in enhanced survivability during periods of extreme water stress. The ability of these populations to persistently resist the fatal effects of desiccation is correlated with evolved physiological traits, namely preferential storage of carbohydrates (associated with reduced lipid reserves) and a dramatic increase in blood volume, which has led to a significant increase in extracellular sodium and chloride content, as well as body mass. When compared to other populations of this drosophilid species, these adaptive traits are unique. While some may argue against the value of evolved traits that have not been found in natural populations, we counter that such traits are of considerable value to the analyses of physiological functions, as well as the underlying mechanisms and evolutionary trajectories of these functions. We propose that multiple physiological consequences almost certainly derive from the evolution of these singular traits; and, furthermore, we discuss future directions for the elucidation of such consequences.

[1]  T. Bradley,et al.  Water acquisition and partitioning in Drosophila melanogaster: effects of selection for desiccation-resistance. , 2001, The Journal of experimental biology.

[2]  H. Wieczorek,et al.  A vacuolar-type proton pump energizes K+/H+ antiport in an animal plasma membrane. , 1991, The Journal of biological chemistry.

[3]  K E Weber,et al.  Aerial performance of Drosophila melanogaster from populations selected for upwind flight ability. , 1997, The Journal of experimental biology.

[4]  K. Zierold,et al.  Stellate cells in the Malpighian tubules of Drosophila hydei and D. melanogaster larvae (Insecta, Diptera) , 1999, Zoomorphology.

[5]  T. Bradley,et al.  Analyses of Physiological Evolutionary Response , 2004, Physiological and Biochemical Zoology.

[6]  J. Nation Insect Physiology and Biochemistry , 2001 .

[7]  L. Matzkin,et al.  Evolution of water balance in the genus Drosophila. , 2001, The Journal of experimental biology.

[8]  J. Phillips,et al.  The secretion of hyperosmotic fluid by the rectum of a saline-water mosquito larva, Aedes taeniorhynchus. , 1975, The Journal of experimental biology.

[9]  M. Rose,et al.  The Effects of Evolution are Local: Evidence from Experimental Evolution in Drosophila1 , 2005, Integrative and comparative biology.

[10]  A. Hoffmann,et al.  Selection for adult desiccation resistance in Drosophila melanogaster: fitness components, larval resistance and stress correlations , 1993 .

[11]  K. Kaiser,et al.  Molecular genetic analysis of V-ATPase function in Drosophila melanogaster. , 1997, The Journal of experimental biology.

[12]  B. Heinrich,et al.  Metabolic rates related to muscle activity in bumblebees. , 1974, The Journal of experimental biology.

[13]  L. Margaritis,et al.  The egg-shell of Drosophila melanogaster. VI, Structural analysis of the wax layer in laid eggs. , 1991, Tissue & cell.

[14]  M. Florkin,et al.  Chapter 6 – HEMOLYMPH: COMPOSITION , 1974 .

[15]  A. F. Bennett,et al.  Experimental tests of the roles of adaptation, chance, and history in evolution. , 1995, Science.

[16]  D. Riddle,et al.  Positive selection of Caenorhabditis elegans mutants with increased stress resistance and longevity. , 2003, Genetics.

[17]  L. Partridge,et al.  Another set of responses and correlated responses to selection on age at reproduction in Drosophila melanogaster , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[18]  H. Schweikl,et al.  A vacuolar-type ATPase, partially purified from potassium transporting plasma membranes of tobacco hornworm midgut. , 1989, The Journal of biological chemistry.

[19]  Michael R. Rose,et al.  Metabolic Aspects of the Trade-Off between Fecundity and Longevity in Drosophila melanogaster , 1996, Physiological Zoology.

[20]  M. Dickinson,et al.  The scaling of carbon dioxide release and respiratory water loss in flying fruit flies (Drosophila spp.). , 2000, The Journal of experimental biology.

[21]  A. Gibbs,et al.  Osmoregulation in Drosophila melanogaster selected for urea tolerance. , 1999, The Journal of experimental biology.

[22]  D. Mullins 9 – Chemistry and Physiology of the Hemolymph , 1985 .

[23]  T. Pannabecker,et al.  Central role of the apical membrane H+-ATPase in electrogenesis and epithelial transport in Malpighian tubules. , 2000, The Journal of experimental biology.

[24]  L. Partridge,et al.  A delayed wave of death from reproduction in Drosophila. , 1999, Science.

[25]  N. F. Hadley Water Relations of Terrestrial Arthropods , 1994 .

[26]  J. Veenstra,et al.  The Dh gene of Drosophila melanogaster encodes a diuretic peptide that acts through cyclic AMP. , 2002, The Journal of experimental biology.

[27]  Fritz-Olaf Lehmann,et al.  The constraints of body size on aerodynamics and energetics in flying fruit flies: an integrative view. , 2002, Zoology.

[28]  Bernd Heinrich,et al.  The Hot-Blooded Insects , 2012, Springer Berlin Heidelberg.

[29]  T. Bradley 10 – The Excretory System: Structure and Physiology , 1985 .

[30]  S. Maddrell,et al.  Secretion by the Malpighian tubules of Rhodnius prolixus stal: electrical events. , 1984, The Journal of experimental biology.

[31]  A. Gibbs,et al.  OSMOREGULATION IN DROSOPHILA MELANOGASTERSELECTED FOR UREA TOLERANCE , 1999 .

[32]  T. Bradley,et al.  Osmotic regulation in adult Drosophila melanogaster during dehydration and rehydration , 2004, Journal of Experimental Biology.

[33]  L. Luckinbill,et al.  SELECTION FOR DELAYED SENESCENCE IN DROSOPHILA MELANOGASTER , 1984, Evolution; international journal of organic evolution.

[34]  J. Dow,et al.  Separate control of anion and cation transport in malpighian tubules of Drosophila Melanogaster. , 1996, The Journal of experimental biology.

[35]  R. Kliman,et al.  Selection Conflicts, Gene Expression, and Codon Usage Trends in Yeast , 2003, Journal of Molecular Evolution.

[36]  A. Gibbs,et al.  Laboratory selection for the comparative physiologist. , 1999, The Journal of experimental biology.

[37]  G. Gäde,et al.  Hormonal regulation in insects: facts, gaps, and future directions. , 1997, Physiological reviews.

[38]  T. Awasaki,et al.  Seasonal changes in glycogen and trehalose content in relation to winter survival of four temperate species of Drosophila , 1992 .

[39]  T. Bradley,et al.  Evolved patterns and rates of water loss and ion regulation in laboratory-selected populations of Drosophila melanogaster , 2003, Journal of Experimental Biology.

[40]  R. Chapman The Insects: Structure and Function , 1969 .

[41]  LIFE‐HISTORY EVOLUTION AND THE MICROEVOLUTION OF INTERMEDIARY METABOLISM: ACTIVITIES OF LIPID‐METABOLIZING ENZYMES IN LIFE‐HISTORY MORPHS OF A WING‐DIMORPHIC CRICKET , 2003, Evolution; international journal of organic evolution.

[42]  A. F. Bennett Experimental Evolution and the Krogh Principle: Generating Biological Novelty for Functional and Genetic Analyses1 , 2003, Physiological and Biochemical Zoology.

[43]  The Principles of Insect Physiology. , 1966 .

[44]  T. Garland,et al.  Selection experiments: an under-utilized tool in biomechanics and organismal biology , 2002 .

[45]  V B WIGGLESWORTH,et al.  INSECT HORMONES. , 1965, Endeavour.

[46]  T. Bradley,et al.  Regulation of rectal secretion in saline-water mosquito larvae living in waters of diverse ionic composition. , 1977, The Journal of experimental biology.

[47]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[48]  Anthony D Long,et al.  Evolutionary changes in heat-inducible gene expression in lines of Escherichia coli adapted to high temperature. , 2003, Physiological genomics.

[49]  G. A. Kerkut,et al.  Comprehensive insect physiology, biochemistry, and pharmacology , 1985 .

[50]  D. Roff The evolution of life histories : theory and analysis , 1992 .

[51]  W. J. Bell,et al.  Comprehensive Insect Physiology, Biochemistry and Pharmacology , 1985 .

[52]  A. Gibbs,et al.  RESOURCE ACQUISITION AND THE EVOLUTION OF STRESS RESISTANCE IN DROSOPHILA MELANOGASTER , 1998, Evolution; international journal of organic evolution.

[53]  A. Zera,et al.  Differential lipid biosynthesis underlies a tradeoff between reproduction and flight capability in a wing-polymorphic cricket , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[54]  D. Sutcliffe The chemical composition of haemolymph in insects and some other arthropods, in relation to their phylogeny , 1963 .

[55]  J. H. Law,et al.  Role of lipophorin in lipid transport to the insect egg. , 1988, The Journal of biological chemistry.

[56]  Hoffmann,et al.  Laboratory selection experiments using Drosophila: what do they really tell us? , 2000, Trends in ecology & evolution.

[57]  M. Dickinson,et al.  The changes in power requirements and muscle efficiency during elevated force production in the fruit fly Drosophila melanogaster. , 1997, The Journal of experimental biology.

[58]  S. Maddrell,et al.  H + V-ATPases Energize Animal Plasma Membranes for Secretion and Absorption of Ions and Fluids' , 1998 .

[59]  M. Rose,et al.  Evolutionary physiology of the cost of reproduction , 1998 .

[60]  T. Markow,et al.  Effects of starvation and desiccation on energy metabolism in desert and mesic Drosophila. , 2003, Journal of insect physiology.

[61]  A. Zera,et al.  LIFE-HISTORY EVOLUTION AND THE MICROEVOLUTION OF INTERMEDIARY METABOLISM: ACTIVITIES OF LIPID-METABOLIZING ENZYMES IN LIFE-HISTORY MORPHS OF A WING-DIMORPHIC CRICKET , 2003, Evolution; international journal of organic evolution.

[62]  S. Applebaum Regulation : digestion, nutrition, excretion , 1985 .

[63]  M. Rockstein The physiology of Insecta , 1964 .

[64]  K. Siegert Locust corpora cardiaca contain an inactive adipokinetic hormone , 1999, FEBS letters.

[65]  M. Rose,et al.  Physiological mechanisms of evolved desiccation resistance in Drosophila melanogaster. , 1997, The Journal of experimental biology.

[66]  M. Dickinson,et al.  The production of elevated flight force compromises manoeuvrability in the fruit fly Drosophila melanogaster. , 2001, The Journal of experimental biology.

[67]  T. Bradley,et al.  The evolution of recovery from desiccation stress in laboratory-selected populations of Drosophila melanogaster , 2004, Journal of Experimental Biology.

[68]  G. Gäde The adipokinetic hormone/red pigment-concentrating hormone peptide family: structures, interrelationships and functions. , 1990 .

[69]  J. Marden,et al.  Dropping like Flies: Environmentally Induced Impairment and Protection of Locomotor Performance in Adult Drosophila melanogaster , 2003, Physiological and Biochemical Zoology.

[70]  Michael R Rose,et al.  LABORATORY EVOLUTION OF POSTPONED SENESCENCE IN DROSOPHILA MELANOGASTER , 1984, Evolution; international journal of organic evolution.