Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-07T22:34:59.975Z Has data issue: false hasContentIssue false
  • English
  • Français

Phenotypic variation of the housefly, Musca domestica: amounts and patterns of wing shape asymmetry in wild populations and laboratory colonies

Published online by Cambridge University Press:  15 August 2013

J. Ludoški ,
M. Djurakic ,
B. Pastor ,
A. I. Martínez-Sánchez ,
S. Rojo  and
V. Milankov
J. Ludoški*
Affiliation:
Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, Trg Dositeja Obradovića 2, 21000 Novi Sad, Serbia
M. Djurakic
Affiliation:
Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, Trg Dositeja Obradovića 2, 21000 Novi Sad, Serbia
B. Pastor
Affiliation:
Instituto CIBIO (Centro Iberoamericano de la Biodiversidad), Universidad de Alicante, Alicante, Spain
A. I. Martínez-Sánchez
Affiliation:
Instituto CIBIO (Centro Iberoamericano de la Biodiversidad), Universidad de Alicante, Alicante, Spain
S. Rojo
Affiliation:
Instituto CIBIO (Centro Iberoamericano de la Biodiversidad), Universidad de Alicante, Alicante, Spain
V. Milankov
Affiliation:
Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, Trg Dositeja Obradovića 2, 21000 Novi Sad, Serbia
*
*Author for correspondence Phone: +381 21 485 2671 Fax: +381 21 450 620 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Musca domestica L. (Diptera: Muscidae) is a vector of a range variety of pathogens infecting humans and animals. During a year, housefly experiences serial population bottlenecks resulted in reduction of genetic diversity. Population structure has also been subjected to different selection regimes created by insect control programs and pest management. Both environmental and genetic disturbances can affect developmental stability, which is often reflected in morphological traits as asymmetry. Since developmental stability is of great adaptive importance, the aim of this study was to examine fluctuating asymmetry (FA), as a measure of developmental instability, in both wild populations and laboratory colonies of M. domestica. The amount and pattern of wing shape FA was compared among samples within each of two groups (laboratory and wild) and between groups. Firstly, the amount of FA does not differ significantly among samples within the group and neither does it differ between groups. Regarding the mean shape of FA, contrary to non-significant difference within the wild population group and among some colonies, the significant difference between groups was found. These results suggest that the laboratory colonies and wild samples differ in buffering mechanisms to perturbations during development. Hence, inbreeding and stochastic processes, mechanisms dominating in the laboratory-bred samples contributed to significant changes in FA of wing shape. Secondly, general patterns of left–right displacements of landmarks across both studied sample groups are consistent. Observed consistent direction of FA implies high degrees of wing integration. Thus, our findings shed light on developmental buffering processes important for population persistence in the environmental change and genetic stress influence on M. domestica.

Keywords

developmental instabilityfluctuating asymmetrygeometric morphometricsMusca domesticawing shape
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 1 , February 2014 , pp. 35 - 47
Copyright
Copyright © Cambridge University Press 2013 

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

Backus, V.L., Bryant, E.H., Hughes, C.R. & Meffert, L. (1995) Effect of migration or inbreeding followed by selection on low-founder-number populations: implications for captive breeding programs. Conservation Biology 9, 1216–1224.Google Scholar
Barin, A., Arabkhazaeli, F., Rahbari, S. & Madani, S. (2010) The housefly, Musca domestica, as a possible mechanical vector of Newcastle disease virus in the laboratory and field. Medical and Veterinary Entomology 24(1), 88–90.Google Scholar
Bitner-Mathé, B.C. & Klaczko, L.B. (1999) Heritability, phenotypic and genetic correlations of size and shape of Drosophila mediopunctata wings. Heredity 83, 688–696.Google Scholar
Black, W.C. & Krafsur, E.S. (1986 a) Population biology and genetics of winter house fly (Diptera: Muscidae) populations. Annals of the Entomological Society of America 79, 636–644.Google Scholar
Black, W.C. & Krafsur, E.S. (1986 b) Seasonal breeding structure in house fly, Musca domestica L., populations. Heredity 56, 289–298.Google Scholar
Black, W.C. & Krafsur, E.S. (1987) Fecundity and size in the housefly: investigations of some environmental sources and genetic correlates of variation. Medical and Veterinary Entomology 1, 369–382.Google Scholar
Bookstein, F.L. (1991) Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge, Cambridge University Press.Google Scholar
Breuker, C.J., Debat, V. & Klingenberg, C.P. (2006 a). Functional evo-devo. Trends in Ecology and Evolution 21, 488–492.Google Scholar
Breuker, C.J., Patterson, J.S. & Klingenberg, C.P. (2006 b) A single basis for developmental buffering of Drosophila wing shape. PloS ONE 1, e7.Google Scholar
Breuker, C.J., Gibbs, M., Van Dongen, S., Merckx, T. & Van Dyck, H. (2010) The use of geometric morphometrics in studying butterfly wings in an evolutionary ecological context. pp. 271–287 in Elewa, A.M.T. (Ed.) Morphometrics for Nonmorphometricians. Berlin, Heidelberg, Springer-Verlag.Google Scholar
Bryant, E.H. & Cowles, J.R. (2000) Differential responses of wild and laboratory strains of the housefly to PCBs. Journal of Chemical Ecology 26(4), 1001–1011.Google Scholar
Bryant, E.H. & Meffert, L.M. (1990) Fitness rebound in serially bottlenecked populations of the house fly. American Naturalist 136, 542–549.CrossRefGoogle Scholar
Bryant, E.H. & Meffert, L.M. (1996) Nonadditive genetic structuring of morphometric variation in relation to a population bottleneck. Heredity 77, 168–176.Google Scholar
Cafarchia, C., Lia, R.P., Romito, D. & Otranto, D. (2009) Competence of the housefly, Musca domestica, as a vector of Microsporum canis under experimental conditions. Medical and Veterinary Entomology 23(1), 21–25.CrossRefGoogle ScholarPubMed
Carreira, V.P., Soto, I.M., Mensch, J. & Fanara, J.J. (2011) Genetic basis of wing morphogenesis in Drosophila: sexual dimorphism and non-allometric effects of shape variation. BMC Developmental Biology 11, 32.Google Scholar
Carter, A.J., Osborne, E. & Houle, D. (2009) Heritability of directional asymmetry in Drosophila melanogaster . International Journal of Evolutionary Biology 2009, 759159.Google Scholar
Chapman, J.W. & Goulson, D. (2000) Environmental versus genetic influences on fluctuating asymmetry in the house fly, Musca domestica . Biological Journal of the Linnean Society 70, 403–413.Google Scholar
Chapman, P.A., Learmount, J., Morris, A.W. & McGreevy, P.B. (1993) The current status of insecticide resistance in Musca domestica in England and Wales and the implication for housefly control in intensive animal units. Pesticide Science 39, 225–235.Google Scholar
Čičková, H., Kozánek, M. & Takáč, P. (2013) Improvement of survival of the house fly (Musca domestica L.) larvae under mass-rearing conditions. Bulletin of Entomological Research 103(1), 119–125. DOI: http://dx.doi.org/10.1017/S000748531200065X Google Scholar
Clarke, G.M. (1993) Fluctuating asymmetry of invertebrate populations as a biological indicator of environmental quality. Environmental Pollution 82, 207–211.Google Scholar
Debat, V., Alibert, P., David, P., Paradis, E. & Auffray, J.-C. (2000) Independence between developmental stability and canalization in the skull of the house mouse. Proceedings of the Royal Society B 267, 423–430.Google Scholar
Debat, V., Bloyer, S., Faradji, F., Gidaszewski, N., Navarro, N., Orozco-terWengel, P., Ribeiro, V., Schlötterer, C., Deutsch, J.S. & Peronnet, F. (2011) Developmental stability: a major role for cyclin G in Drosophila melanogaster . PloS Genetics 7(10), e1002314.CrossRefGoogle Scholar
DiMichele, L., Paynter, K.T. & Powers, D.A. (1991) Evidence of lactate dehydrogenase-B allozyme effects in the teleost, Fundulus heteroclitus . Science 253, 898–900.Google Scholar
Dryden, I.L. & Mardia, K.V. (1998) Statistical Shape Analysis.Chichester, Wiley.Google Scholar
Emerson, P.M., Bailey, R.L., Walraven, G.E.L. & Lindsay, S.W. (2001) Human and other faeces as breeding media of the trachoma vector Musca sorbens . Medical and Veterinary Entomology 15, 314–320.Google Scholar
Fox, C.W. & Reed, D.H. (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65, 246–258.Google Scholar
Fox, C.W., Stillwell, R.C., Wallin, W.G., Curtis, C.L. & Reed, D.H. (2011) Inbreeding-environment interactions for fitness: complex relationships between inbreeding depression and temperature stress in a seed-feeding beetle. Evolutionary Ecology 25, 25–43.Google Scholar
Frankham, R. (2005) Stress and adaptation in conservation genetics. Journal of Evolutionary Biology 18, 279–293.CrossRefGoogle ScholarPubMed
Goulson, D., Bristow, L., Elderfield, E., Brinklow, K., Parry-Jones, B. & Chapman, J.W. (1999) Size, symmetry, and sexual selection in the housefly, Musca domestica . Evolution 53(2), 527–534.CrossRefGoogle ScholarPubMed
Greenberg, B. (1970) Flies and Disease. Ecology. Classification and Biotic Associations. New Jersey, Princeton University Press.Google Scholar
Greenberg, B. (1973) Flies and Diseases. Biology and Disease Transmission. New Jersey, Princeton University Press.Google Scholar
Grübel, P., Huang, L., Masubuchi, N., Stutzenberger, F.J. & Cave, D.R. (1998) Detection of Helicobacter pylori DNA in houseflies (Musca domestica) on three continents. Lancet 352, 788–789.Google Scholar
Hosken, D.J., Blanckenhorn, W.U. & Ward, P.I. (2000) Developmental stability in yellow dung flies (Scathophaga stercoraria): fluctuating asymmetry, heterozygosity and environmental stress. Journal of Evolutionary Biology 13, 919–926.Google Scholar
Kaufman, P.E., Nunez, S., Mann, R.S., Geden, C.J. & Scharf, M.E. (2010) Nicotinoid and pyrethroid insecticide resistance in house flies (Diptera: Muscidae) collected from Florida dairies. Pest Management Science 66, 290–294.Google Scholar
Klingenberg, C.P. (2003 a) A developmental perspective on developmental instability: theory, models and mechanisms. pp. 14–34 in Polak, M. (Ed.) Developmental Instability: Causes and Consequences. New York, Oxford University Press.Google Scholar
Klingenberg, C.P. (2003 b) Developmental instability as a research tool: using patterns of fluctuating asymmetry to infer the developmental origins of morphological integration. pp. 427–442 in Polak, M. (Ed.) Developmental Instability: Causes and Consequences. New York, Oxford University Press.CrossRefGoogle Scholar
Klingenberg, C.P. (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11, 353–357.Google Scholar
Klingenberg, C.P. & McIntyre, G.S. (1998) Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution 52(5), 1363–1375.Google Scholar
Klingenberg, C.P. & Monteiro, L.R. (2005) Distance and directions in multidimensional shape space: implications for morphometric applications. Systematic Biology 54(4), 678–688.Google Scholar
Klingenberg, C.P. & Nijhout, H.F. (1999) Genetics of fluctuating asymmetry: a developmental model of developmental instability. Evolution 53(2), 358–375.Google Scholar
Klingenberg, C.P. & Zaklan, S.D. (2000) Morphological integration between developmental compartments in the Drosophila wing. Evolution 54, 1273–1285.Google Scholar
Klingenberg, C.P., McIntyre, G.S. & Zaklan, S.D. (1998) Left-right asymmetry of wings and the evolution of body axes. Proceedings of the Royal Society B 265, 1255–1259.CrossRefGoogle ScholarPubMed
Klingenberg, C.P., Barluenga, M. & Meyer, A. (2002) Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56, 1909–1920.Google Scholar
Krafsur, E.S. (1985) Age composition and seasonal phenology of house fly (Diptera: Muscidae) populations. Journal of Medical Entomology 22, 515–523.Google Scholar
Krafsur, E.S., Bryant, N.L., Marquez, J.G. & Griffiths, N.T. (2000) Genetic distance among North American, British and West African house fly populations (Musca domestica L.). Biochemical Genetics 38(9/10), 275–284.Google Scholar
Krafsur, E.S., Cummings, M.A., Endsley, M.A., Marquez, J.G. & Nason, J.D. (2005) Geographic differentiation in the house fly estimated by microsatellite and mitochondrial variation. Journal of Heredity 96(5), 502–512.Google Scholar
Leamy, L.J. (1984) Morphometric studies in inbred and hybrid house mice. V. Directional and fluctuating asymmetry. American Naturalist 123, 579–593.Google Scholar
Leamy, L.J. & Klingenberg, C.P. (2005) The genetics and evolution of fluctuating asymmetry. Annual Review of Ecology Evolution and Systematics 36, 1–21.Google Scholar
Leamy, L.J., Meagher, S., Taylor, S., Carroll, L. & Potts, W.K. (2001) Size and fluctuating asymmetry of morphometric characters in mice: their associations with inbreeding and t-haplotype. Evolution 55(11), 2333–2341.Google Scholar
Lovatt, F.M. & Hoelzel, A.R. (2011) The impact of population bottlenecks on fluctuating asymmetry and morphological variance in two separate populations of reindeer on the island of South Georgia. Biological Journal of the Linnean Society 102, 798–811.Google Scholar
Mardia, K.V., Kent, J.T. & Bibby, J.M. (1979) Multivariate Analysis. London, Academic Press.Google Scholar
Marquez, J.G. & Krafsur, E.S. (2002) Gene flow among geographically diverse housefly populations (Musca domestica L.): a worldwide survey of mitochondrial diversity. Journal of Heredity 93(4), 254–259.Google Scholar
Meffert, L.M. & Regan, J.L. (2006) Reversed selection responses in small populations of the housefly (Musca domestica L.). Genetica 127, 1–9.Google Scholar
Meffert, L.M., Regan, J.L., Hicks, S.K., Mukana, N. & Day, S.B. (2006) Testing alternative methods for purging genetic load using the housefly (Musca domestica L.). Genetica 128, 419–427.Google Scholar
Messier, S. & Mitton, J.B. (1996) Heterozygosity at the malate dehydrogenase locus and developmental homeostasis in Apis mellifera . Heredity 76, 616–622.Google Scholar
Møller, A.P. (1996) Sexual selection, viability selection, and developmental instability in the domestic fly Musca domestica . Evolution 50, 746–752.Google Scholar
Møller, A.P. & Swaddle, J.P. (1997) Asymmetry, Developmental Stability and Evolution. Oxford, Oxford University Press.Google Scholar
Palmer, A.R. (1994) Fluctuating asymmetry analyses: a primer. pp. 335–364 in Markow, T.A. (Ed.) Developmental Instability: Its origins and evolutionary implications.Dordrecht, Kluwer.Google Scholar
Palmer, A.R. (1996) Waltzing with asymmetry. BioScience 46, 518–532.Google Scholar
Palmer, A.R. & Strobeck, C. (1986) Fluctuating asymmetry: measurements, analysis, patterns. Annual Review of Ecology and Systematics 17, 391–421.Google Scholar
Palmer, A.R. & Strobeck, C. (1992) Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power statistical tests. Acta Zoologica Fennica 191, 57–72.Google Scholar
Pastor, B. (2011) Biological parameters for the mass rearing of the housefly (Musca domestica L.) and its use as pig manure biodegradation agent. PhD Dissertation, CIBIO, University of Alicante, Spain.Google Scholar
Pastor, B., Čičková, H., Kozánek, M., Martinez-Sánchez, A., Takáč, P. & Rojo, S. (2011) Effect of the size of the pupae, adult diet, oviposition substrate and adult population density on egg production in Musca domestica (Diptera: Muscidae). European Journal of Entomology 108, 587–596.Google Scholar
Paynter, K.T., DiMichele, L., Hand, S.C. & Powers, D. (1992) Metabolic implications of Ldh-B genotype during early development in Fundulus heteroclitus . Journal of Experimental Zoology 257, 24–33.Google Scholar
Pélabon, C. & Hansen, T.F. (2008) On the adaptive accuracy of directional asymmetry in insect wing size. Evolution 62(11), 2855–2867.Google Scholar
Pélabon, C., Hansen, T.F., Carter, A.J.R. & Houle, D. (2010) Evolution of variation and variability under fluctuating, stabilizing, and disruptive selection. Evolution 64(7), 1912–1925.Google Scholar
Pertoldi, C., Kristensen, T.N., Andersen, D.H. & Loeschcke, V. (2006) Developmental instability as an estimator of genetic stress. Heredity 96, 122–127.Google Scholar
R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.R-project.org Google Scholar
Reed, D.H. & Bryant, E.H. (2001) Fitness, genetic load and purging in experimental populations of the housefly. Conservation Genetics 2, 57–62.Google Scholar
Rego, C., Matos, M. & Santos, M. (2006) Symmetry breaking in interspecific Drosophila hybrids is due to developmental noise. Evolution 60(4), 746–761.Google Scholar
Rohlf, F.J. (2010) TpsDig, version 2.16. Department of Ecology and Evolution, State University of New York at Stony Brook, New York. Available online at http://life.bio.sunysb.edu/morph/ Google Scholar
Rohlf, F.J. & Marcus, L.F. (1993) A revolution in morphometrics. Trends in Ecology and Evolution 8(4), 129–132.Google Scholar
Sanchez-Arroyo, H. (2008) House fly, Musca domestica Linnaeus. Institute of Food and Agricultural Sciences, University of Florida. Available online at http://edis.ifas.ufl.edu/in205 Google Scholar
Santos, M., Iriarte, P.F. & Cespedes, W. (2005) Genetics and geometry of canalization and developmental stability in Drosophila subobscura . BMC Evolutionary Biology 5, 7.Google Scholar
Sehgal, R., Bhatti, H.P., Bhasin, D.K., Sood, A.K., Nada, R., Malla, N. & Singh, K. (2002) Intestinal myiasis due to Musca domestica: a report of two cases. Japanese Journal of Infectious Diseases 55, 191–193.Google Scholar
Smith, K.G.V. (1986) A manual of Forensic Entomology. London, British Museum of Natural History.Google Scholar
Speight, M.R., Hunter, M.D. & Watt, A.D. (2008) Ecology of Insects: Concepts and Applications. 2nd edn. Oxford, Wiley-Blackwell.Google Scholar
Stat Soft, Inc. (2011) Statistica (data analysis software system), version 10. www.statsoft.com Google Scholar
Stige, L.C., David, B. & Alibert, P. (2006) On hidden heterogeneity in directional asymmetry – can systematic bias be avoided? Journal of Evolutionary Biology 19, 492–499.Google Scholar
Trotta, V., Cavicchi, S., Guerra, D., Andersen, D.H., Babbitt, G.A., Kristensen, T.N., Pedersen, K.S., Loeschcke, V. & Pertoldi, C. (2011) Allometric and non-allometric consequences of inbreeding on Drosophila melanogaster wings. Biological Journal of the Linnean Society 102, 626–634.Google Scholar
Tsubaki, Y. (1998) Fluctuating asymmetry of the oriental fruit fly (Dacus dorsalis) during the process of its extinction from the Okinawa Island. Conservation Biology 12, 926–929.Google Scholar
Van Dongen, S., Lens, L., Pape, E., Volckaert, F.A.M. & Raeymaekers, J.A.M. (2009) Evolutionary history shapes the association between developmental instability and population-level genetic variation in three-spined sticklebacks. Journal of Evolutionary Biology 22, 1695–1707.Google Scholar
Van Valen, L. (1962) A study of fluctuating asymmetry. Evolution 16, 125–142.Google Scholar
Wanaratana, S., Panyim, S. & Pakpinyo, S. (2011) The potential of house flies to act as a vector of avian influenza subtype H5N1 under experimental conditions. Medical and Veterinary Entomology 25(1), 58–63.CrossRefGoogle ScholarPubMed
Whitlock, M.C. & Fowler, K. (1996) The distribution among populations in phenotypic variance with inbreeding. Evolution 50(5), 1919–1926.Google Scholar
Wright, L.I., Tregenza, T. & Hosken, D.J. (2008) Inbreeding, inbreeding depression and extinction. Conservation Genetics 9, 833–843.CrossRefGoogle Scholar
Zelditch, M.L., Swiderski, D.L., Sheets, H.D. & Fink, W.L. (2004) Geometric Morphometrics for Biologists. London, Elsevier Academic Press.Google Scholar
Supplementary material: File

Ludoski Supplementary Material

Table

Download Ludoski Supplementary Material(File)
File 117.2 KB