Abstract
Body size is an integral feature of an organism that influences many aspects of life such as fecundity, life span and mating success. Size of individual organs and the entire body size represent quantitative traits with a large reaction norm, which are influenced by various environmental factors. In the model system Drosophila melanogaster, pupal size and adult traits, such as tibia and thorax length or wing size, accurately estimate the overall body size. However, it is unclear whether these traits can be used in other flies. Therefore, we studied changes in size of pupae and adult organs in response to different rearing temperatures and densities for D. melanogaster, Ceratitis capitata and Musca domestica. We confirm a clear sexual size dimorphism (SSD) for Drosophila and show that the SSD is less uniform in the other species. Moreover, the size response to changing growth conditions is sex dependent. Comparison of static and evolutionary allometries of the studied traits revealed that response to the same environmental variable is genotype specific but has similarities between species of the same order. We conclude that the value of adult traits as estimators of the absolute body size may differ among species and the use of a single trait may result in wrong assumptions. Therefore, we suggest using a body size coefficient computed from several individual measurements. Our data is of special importance for monitoring activities of natural populations of the three dipteran flies, since they are harmful species causing economical damage (Drosophila, Ceratitis) or transferring diseases (Musca).
Similar content being viewed by others
References
Alves SM, Bélo M (2002) Morphometric variation in the housefly, Musca domestica (L.) with latitude. Genetica 115:243–251
Anderson WW (1966) Genetic divergence in M. Vetukhiv’s experimental populations of Drosophila pseudoobscura. 3. Divergence in body size. Genet Res 7:255–266
Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 3:1–58
Badyaev AV (2002) Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol 17:369–378
Beadle GW, Tatum EL, Clancy CW (1938) Food level in relation to rate of development and eye pigmentation in Drosophila melanogaster. Biol Bull 75:447–462
Bergmann C (1847) Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Göttinger Stud 3:595–708
Biddulph TA, Harrison JF (2014) Oxygen modulates density effects on body size in Drosophila melanogaster. Society for Integrative and Comparative Biology, Austin
Bookstein FL (1996) Biometrics, biomathematics and the morphometric synthesis. Bull Math Biol 58:313–365
Bryan EH (1977) Morphometric adaptation of the housefly, Musca domestica L., in the United States. Evolution 31:580–596
Burk T, Webb JC (1983) Effect of male size on calling propensity, song parameters and mating success in Caribbean fruit flies, Anastrepha suspensa (Loew) (Diptera: Tephritidae). Ann Entomol Soc Am 76:678–682
Cavicchi S, Guerra D, Natali V, Pezzoli C, Giorgi G (1989) Temperature‐related divergence in experimental populations of Drosophila melanogaster. II. Correlation between fitness and body dimensions. J Evol Biol 2:235–251
Cheverud JM (1982) Relationships among ontogenetic, static, and evolutionary allometry. Am J Phys Anthropol 59:139–149
Churchill-Stanland C, Stanland R, Wong TTY, Tanaka N, McInnis DO, Dowell R (1986) Size as a factor in the mating propensity of Mediterranean fruit flies, Ceratitis capitata (Diptera: Tephritidae), in the laboratory. J Econ Entomol 79:614–618
Cohen S (1993) The development of Drosophila melanogaster. CSHLP, New York, pp 747–841
Cowley DE, Atchley WR (1990) Development and quantitative genetics of correlation structure among body parts of Drosophila melanogaster. Am Nat 135:242–268
David JR, Clavel M-F (1967) Influence de la temperature subie au cours du development sur divers characters biometriques des adultes de Drosophila melanogaster Meigen. J Insect Physiol 13:717–729
de Moed GH, de Jong G, Schatloo W (1997) The phenotypic plasticity of wing size in Drosophila melanogaster: the cellular basis of its genetic variation. Heredity 79:260–267
Demerec M (1950) Biology of drosophila. Wiley, New York
Diamond SE, Kingsolver JG (2010) Environmental dependence of thermal reaction norms: host plant quality can reverse the temperature-size rule. Am Nat 175:1–10
DiAngelo JR, Bland ML, Bambina S, Cherry S, Birnbaum MM (2009) The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling. Proc Natl Acad Sci U S A 106:20853–20858
Edgar BA (2006) How flies get their size: genetics meets physiology. Nat Rev Genet 7:907–916
French V, Feast M, Partridge L (1998) Body size and cell size in Drosophila: the developmental response to temperature. J Insect Physiol 44:1081–1089
Gleiser RM, Urrutia J, Gorla DE (2000) Body size variation of the floodwater mosquito Aedes albifasciatus in Central Argentina. Med Vet Entomol 14:38–43
Gokhale RH, Shingleton AW (2015) Size control: the developmental physiology of body and organ size regulation. Wiley Interdiscip Rev Dev Biol 4:335–356
Head G (1995) Selection on fecundity and variation in the degree of sexual size dimorphism among spider species (class Aranea). Evolution 49:776–781
Hewitt CG (1914) The house-fly, Musca domestica Linn.: its structure, habits, development, relation to disease and control. University Press, Cambridge
Huxley JS (1924) Constant differential growth-ratios and their significance. Nature 114:895–896
Huxley JS, Tessier G (1936) Terminology of relative growth. Nature 137:780–781
Kacmarczyk T, Craddock EM (2000) Cell size is a factor in body size variation among Hawaiian and nonHawaiian species of Drosophila. Dros Inf Serv 83:144–148
Kammenga JE, Doroszuk A, Riksen JA, Hazendonk E, Spiridon L, Petrescu AJ, Tijsterman M, Plasterk RH, Bakker J (2007) A Caenorhabditis elegans wild-type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3. PLoS Genet 3, e34. doi:10.1371/journal.pgen.0030034
Khazaeli AA, Van Voorhies W, Curtsinger JW (2005) The relationship between life span and adult body size is highly strain-specific in Drosophila melanogaster. Exp Gerontol 40:77–85
Kingsolver JG, Huey RB (2008) Size, temperature and fitness: three rules. Evol Ecol Res 8:703–715
Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357
Koyama T, Rodrigues MA, Athanasiadis A, Shingleton AW, Mirth CK (2014) Nutritional control of body size through FoxO-ultraspiracle mediated ecdysone biosynthesis. Elife 3:1–20. doi:10.7554/eLife.03091
Lutz F (1948) Field book of insects. G. P. Putnam’s Sons, New York
Madhavan MM, Schneiderman HA (1977) Histological analysis of dynamics of growth of imaginal discs and histoblast nests during larval development of Drosophila melanogaster. Roux’s Arch Dev Biol 183:269–305
Miller RS, Thomas JL (1958) The effect of larval crowding and body size on the longevity of adult Drosophila melanogaster. Ecology 39:118–125
Mirth CK, Shingleton AW (2012) Integrating body and organ size in Drosophila: recent advances and outstanding problems. Front Endocrinol 3:49. doi:10.3389/fendo.2012.00049
Mirth CK, Tang HY, Makohon-Moore SC, Salhadar S, Gokhale RH, Warner RD, Koyama T, Riddiford LM, Shingleton AW (2014) Juvenile hormone regulates body size and perturbs insulin signaling in Drosophila. Proc Natl Acad Sci U S A 111:7018–23
Navarro-Campos C, Martínez-Ferrer MT, Campos JM, Fibla JM, Alcaide J, Bargues L, Marzal C, Garcia-Marí F (2011) The influence of host fruit and temperature on the body size of adult Ceratitis capitata (Diptera: Tephritidae) under laboratory and field conditions. Environ Entomol 40:931–938
Nunney L, Cheung W (1997) The effect of temperature on body size and fecundity in female drosophila melanogaster: evidence for adaptive plasticity. Evolution 51:1529–1535
Oliveira MM, Shingleton AW, Mirth CK (2014) Coordination of wing and whole-body development at developmental milestones ensures robustness against environmental and physiological perturbations. PLoS Genet 10, e1004408. doi:10.1371/journal.pgen.1004408
Pantalouris EM (1957) Size response of developing Drosophila to temperature change. J Genet 55:507–510
Partridge L, Ewing A, Chandler A (1987) Male size and mating success in Drosophila melanogaster: the role of male and female behaviour. Anim Behav 35:555–562
Peck LS, Maddrell SHP (2005) Limitation of size by hypoxia in the fruit fly Drosophila melanogaster. J Exp Zool A Comp Exp Biol 303A:968–975
Pitnick S, Markow TA (1995) Delayed male maturity is a cost of producing large sperm in Drosophila. Proc Natl Acad Sci USA 92:10614–10618
R Development Core Team (2008) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, http://www.R-project.org
Ray C (1960) The application of Bergmann’s and Allen’s rules to the poikilotherms. J Morphol 106:85–108
Robinson SJW, Partridge L (2001) Temperature and clinal variation in larval growth efficiency in Drosophila melanogaster. J Evol Biol 14:14–21
Rohlf FJ (2004) tpsUtil, File utility program, version 1.54. Department of Ecology and Evolution, State University of New York at Stony Brook
Rohlf FJ (2010) tpsDig, Digitize landmarks and outlines, version 2.17. Department of Ecology and Evolution, State University of New York at Stony Brook
Santos M, Fowler K, Partridge L (1994) Gene-environment interaction for body size and larval density in Drosophila melanogaster: an investigation of effects on development time, thorax length and adult sex ratio. Heredity 72:515–521
Scheiner SM, Lyman RF (1989) The genetics of phenotypic plasticity. Heritability. J Evol Biol 2:95–107
Scheiner SM, Lyman RF (1991) The genetics of phenotypic plasticity II. Response to selection. J Evol Biol 3:23–50
Schlichting CD, Pigliucci M (1999) Phentypic evolution—a reaction norm perspective. Heredity 82:344–344
Shine R (1979) Sexual selection and sexual dimorphism in the Amphibia. Copeia 2:297–306
Shine R (1994) Sexual size dimorphism in snakes revisited. Copeia 2:326–346
Shingleton AW, Mirth CK, Bates PW (2008) Developmental model of static allometry in holometabolous insects. Proc R Soc B 275:1875–1885
Shingleton AW, Estep CM, Driscoll MV, Dworkin I (2009) Many ways to be small: different environmental regulators of size generate distinct scaling relationships in Drosophila melanogaster. Proc R Soc B 276:2625–2633
StatSoft, Inc (1997) Electronic statistics textbook. Tulsa, OK: StatSoft. WEB: http://www.statsoft.com/textbook/stathome.html
Stillwell RC, Blanckenhorn WU, Teder T, Davidowitz G, Fox CW (2010) Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Annu Rev Entomol 55:227–245
Stillwell RC, Dworkin I, Shingleton AW, Frankino WA (2011) Experimental manipulation of body size to estimate morphological scaling relationships in drosophila. J Vis Exp 56:3162. doi:10.3791/3162
Teder T, Tammaru T (2005) Sexual size dimorphism within species increases with body size in insects. Oikos 108:321–334
Acknowledgments
We thank Y. Wu and L. Beukeboom for providing the Musca flies. This work has been funded by a German Academic Exchange Service (DAAD) fellowship #A/12/86783 to NS, the Göttingen Graduate School for Neurosciences, Biophysics, and Molecular Biosciences (GGNB) and the Volkswagen Foundation (project number: 85 983; to NP). Special thanks to the two anonymous reviewers for their helpful comments on the previous versions of the manuscript.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by Angelika Stollewerk
This article is part of the Special Issue “Size and Shape: Integration of morphometrics, mathematical modelling, developmental and evolutionary biology”, Guest Editors: Nico Posnien—Nikola-Michael Prpic.
Rights and permissions
About this article
Cite this article
Siomava, N., Wimmer, E.A. & Posnien, N. Size relationships of different body parts in the three dipteran species Drosophila melanogaster, Ceratitis capitata and Musca domestica . Dev Genes Evol 226, 245–256 (2016). https://doi.org/10.1007/s00427-016-0543-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-016-0543-6