Pupal shape and size dimorphism in Aedes albopictus (Skuse, 1894) (Diptera: Culicidae)
Article Sidebar
Main Article Content
Abstract
Aedes albopictus (Skuse, 1894) is a culicid mosquito associated with the transmission of pathogens causative for dengue, yellow fever, chikungunya, Mayaro and other diseases. Several recent studies have proposed that demographic surveys of dengue vector pupae are more useful than traditional larval indices for estimating populations. Geometric morphometrics is a tool for describing phenotypic variation that has been validated for characterizing sexual dimorphism. We undertook to apply this method to describe sexual and morphological dimorphism in A. albopictus pupae. Two-dimensional co-ordinates were digitalized from 60 specimens in two stages using 10 landmarks in pupae and 14 in wings. Configuration matrices were aligned by generalized procrustes analysis to extract matrix configurations and centroid size (CS). A discriminant analysis (DA) was used to test group (female or male) membership significance, and non-parametric ANOVA was used for CS differences. We found significant differences (Kruskal-Wallis P < 0.01) among pupal cephalothorax CS and adult wings; female pupae and adults were larger than males. The DA for cephalothorax and wing specimens showed significant differences (Hotelling P < 0.0001) between females and males. Through cross-validation, females and males were correctly classified with greater than 90% accuracy using the conformation characteristics described. Our study is the first description of phenotypic variation of pupal shape and size in A. albopictus laboratory colonies, and the results can be used as an additional tool in dengue entomological survey programs. More studies are necessary to confirm the variation between natural and laboratory populations.Â
Article Details
Authors own the copyright to the articles published in JoTT. This is indicated explicitly in each publication. The authors grant permission to the publisher Wildlife Information Liaison Development (WILD) Society to publish the article in the Journal of Threatened Taxa. The authors recognize WILD as the original publisher, and to sell hard copies of the Journal and article to any buyer. JoTT is registered under the Creative Commons Attribution 4.0 International License (CC BY), which allows authors to retain copyright ownership. Under this license the authors allow anyone to download, cite, use the data, modify, reprint, copy and distribute provided the authors and source of publication are credited through appropriate citations (e.g., Son et al. (2016). Bats (Mammalia: Chiroptera) of the southeastern Truong Son Mountains, Quang Ngai Province, Vietnam. Journal of Threatened Taxa 8(7): 8953–8969. https://doi.org/10.11609/jott.2785.8.7.8953-8969). Users of the data do not require specific permission from the authors or the publisher.
References
Adams, D.C., J. Rolhf & D.E. Slice (2004). Geometric morphometrics: Ten years of progress following the ‘revolution’. Italian Journal of Zoology 71: 5–16; http://doi.org/10.1080/11250000409356545
Armbruster, P. & R. Hutchinson (2002). Pupal Mass and Wing Length as Indicators of Fecundity in Aedes albopictus and Aedes geniculatus (Diptera: Culicidae). Journal of Medical Entomology 39(4): 699–704; http://doi.org/10.1603/0022-2585-39.4.699
Barrera, R. (2009). Simplified Pupal Surveys of Aedes aegypti (L.) for Entomologic Surveillance and Dengue Control. American Journal of Tropical Medicine and Hygiene 81(1): 100–107.
Barrera, R., M. Amador & G.C. Clark (2006). Use of the pupal survey technique for measuring Aedes aegypti (Diptera: Culicidae) productivity in Puerto Rico. American Journal of Tropical Medicine and Hygiene 74(2): 290–302.
Belen, A., B. Alten & A.M. Aytekin (2004). Altitudinal variation in morphometric and molecular characteristics of Phlebotomus papatasi populations. Medical and Veterinay Entomology 18: 343–350; http://doi.org/10.1111/j.0269-283X.2004.00514.x
Benedict, M.Q., R.S. Levine, W.A. Hawley & L.P. Lounibos (2007). Spread of the tiger: Global risk of invasion by the mosquito Aedes albopictus. Vector-borne and Zoonotic Diseases 7: 76–85; http://doi.org/10.1089/vbz.2006.0562
Bookstein, F.L. (1991). Morphometric Tools for Landmark Data: Geometry and Biology. EEUU, Cambridge.
Bueno, R. & R. Jiménez (2012). Implicaciones sanitarias del establecimiento y expansión en España del mosquito Aedes albopictus. Revista Española de Salud Pública 86: 319–330.
Calle, D.A., M. Quiñónez, H. Erazo & N. Jaramillo (2008). Discriminación por morfometrÃa geométrica de once especies de Anopheles (Nyssorhynchus) presentes en Colombia. Biomedica 28: 371–385.
Cantrell, W. (1939). Relation of size to sex in pupae of Aedes aegypti (L.), A. triseriatus (Say) and A. vexans (Meig.). Journal of Parasitology 24(4): 448–449.
Carreira, V., I. Soto, J. Mensch & J. Fanara (2011). Genetic basis of wing morphogenesis in Drosophila: sexual dimorphism and non-allometric effects of shape variation. BMC Developmental Biology 11: 32; http://doi.org/10.1186/1471-213X-11-32
Castro, A., S. Davidson, C. Azevedo, M. Bicudo de Paula & R. Marques (1994). Duration of larval and pupal development stages of Aedes albopictus in natural and artificial containers. Revista de Saúde Pública 29(1): 15–19.
Consoli, A.G. & R.L. de Oliveira (1994). Principais Mosquitos de Importância Sanitária no Brasil. Fiocruz, Rio de Janeiro, 228pp.
Couret, J., E. Doton & M.Q. Benedict (2014). Temperature, larval diet, and density effects on development rate and survival of Aedes aegypti (Diptera: Culicidae). PLoS One 9(2): e87468; http://doi.org/10.1371/journal.pone.0087468
Devicari, M., A.R. Lopes & L. Suesdek (2011). Wing sexual dimorphism in Aedes scapularis (Diptera: Culicidae). Biota Neotropica 11(2): 165–169; http://doi.org/10.1590/S1676-06032011000200016
Dujardin, J.P. (2008). Morphometrics applied to medical entomology. Infection, Genetics and Evolution 8: 875–890; http://doi.org/10.1016/j.meegid.2008.07.011
Focks, D.A. (2003). A Review of Entomological Sampling Methods and Indicators for Dengue Vectors. Gainsville, World Health Organization, 40pp.
Gratz, N.G. (2004). Critical review of the vector status of Aedes albopictus. Medical and Veterinary Entomology 18: 215–227.Â
Gunz, P. & P. Mitteroecker (2013). Semilandmarks: a method for quantifying curves and surfaces. Italian Journal of Zoology 24: 103–109.
Hammer, Ø. & D.A.T. Harper (2011). PAST: Palaeontological Statistics, versión 2.10. Available in: http:// folk.uio.no/ohammer/past.
Haramis, L.D. (1985). Larval nutrition, adult body size, and the biology of Aedes triseriatus, pp. 431–437. In: Lounibos, L.P., J.R. Rey, J.H. Frank (eds.). Ecology of Mosquitoes: Proceedings of a Workshop. Florida Medical Entomology Laboratory, Vero Beach, FL.
Harrison, B. (2005). Easily seen characters to identify the pupa of Aedes albopictus in the united states. Journal of the American Mosquito Control Association 21(4): 451–454.
Hayes, R.O. (1953). Studies on the artificial insemination of the mosquito Aedes aegypti (L.). Mosquito News 13(2): 145-152.
Hernandez, M., M. Piña, A. Soto-Vivas, M.A. Rangel & J. Liria (2015). Primer registro de Aedes albopictus (Skuse, 1894) (Diptera: Culicidae) en el Estado Carabobo, Venezuela. Salus 19: 39–41.
Jirakanjanakit, N., W.A.T. Leemingsa, S. Thongrungkiat, S. Apiwathnasorn, C. Singhaniyom, C. Bellec & J.P. Dujardin (2007). Influence of larval density or food variation on the geometry of the wing of Aedes (Stegomyia) aegypti. Tropical Medicine and International Health 12(11): 1354–1360.
Klingenberg, C.P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11: 353–357; http://doi.org/10.1111/j.1755-0998.2010.02924.x
Lounibos, L.P. (1994). Geographical and developmental components of adult size of neotropical Anopheles (Nyssorhynchus). Ecological Entomology 19: 138–146.
Massad, E., F.A.B. Coutinho, M.N. Burattini & L.F. Lopez (2001). The risk of yellow fever in a dengue-infested area. Transactions of the Royal Society of Tropical Medicine and Hygiene 9: 370–374.
Mikery-Pacheco, O., K. Serrano-DomÃnguez, P. MarcelÃn-Chong & D. Sánchez-Guillén (2015). Efficiency of the separation of Aedes (Stegomyia) albopictus (Diptera: Culicidae) male and female pupae using a sieving device. Acta Zoológica Mexicana 31(1): 113–115.
Moorefield, H.M. (1951). Sexual dimorphism in mosquito pupae. Mosquito News 11: 175-177.
Morales-Vargas, E.R., P. Ya-Umphan, N. Phumala-Morales, N. Komalamisra & J.P. Dujardin (2010). Climate associated size and shape changes in Aedes aegypti (Diptera: Culicidae) populations from Thailand. Infection, Genetics and Evolution 10: 580–585; http://doi.org/10.1016/j.meegid.2010.01.004
Muñoz, M. & J.C. Navarro (2012). Virus Mayaro: un arbovirus reemergente en Venezuela y Latinoamérica. Biomédica 32: 286–302; http://doi.org/10.7705/biomedica.v32i2.647
Nasci, R.S. & C.J. Mitchell (1994). Larval diet, adult size, and susceptibility of Aedes aegypti (Diptera: Culicidae) to infection with Ross River virus. Journal of Medical Entomology 31: 123–126.
Nuñez-RodrÃguez, J.A. & J. Liria (2017). Geometric morphometrics sexual dimorphism in three forensically-important species of Blow Fly (Diptera: Calliphoridae). Life: The Excitement of Biology 4(4): 272–284; http://doi.org/10.9784/LEB4(4)NunezRodriguez.01
Oliveira, P., E. Carvalho & L. Suesdek (2012). Temporal variation of wing geometry in Aedes albopictus. Memórias do Instituto Oswaldo Cruz 107(8): 1030–1034; http://doi.org/10.1590/S0074-02762012000800011
Penn, G.H. (1949). The pupae of mosquitoes of New Guinea. Pacific Science 3(1): 1–85.
Reiter, P. (1998). Aedes albopictus and the world trade in used tires, 1988-1995: the shape of things to come? Journal of the American Mosquito Control Association 14: 83–94.
Rohlf, J. (2008). tpsDig, Program for Digitalizing morphologic landmark and outlines for Geometric Morphometric Analyses, ver. 2.11. Department of Ecology and Evolution, State University of New York at Stony Brook. Available from: http://life.bio.sunysb.edu/morph/index.html
Rohlf, J. (2016). tpsRelw, Program provides a low dimensional approximation (via a principal components analysis) to the tangent space approximation of shape space, ver. 1.62. Department of Ecology and Evolution, State University of New York, Stony Brook. Available from: http://life.bio.sunysb.edu/morph/index.html
Rohlf, J. & L. Marcus (1993). A revolution in morphometrics. Trends in Ecology and Evolution 8: 129–132; http://doi.org/10.1016/0169-5347(93)90024-J
Rúa-Uribe, G., C. Suárez-Acosta & R. Rojo (2012). Implicaciones epidemiológicas de Aedes albopictus (Skuse) en Colombia. Revista Facultad Nacional de Salud Pública 30(3): 328–337.
Sheets, H.D. (2010). MakeFan, a tool for drawing alignment “fans†at equal angular spacing. Available from: http://www3.canisius.edu/~sheets/imp7.htm
Vargas, M. (1968). Sexual dimorphism of larvae and pupa of Aedes aegypti (Linn.). Mosquito News 28(3): 374–379.
Vásquez, M. & J. Liria (2012). MorfometrÃa geométrica alar para la
identificación de Chrysomya albicep sy C. megacephala (Diptera: Calliphoridae) de Venezuela. Revista de BiologÃa Tropical 60(3): 1-10; http://doi.org/10.15517/rbt.v60i3.1776
Virginio, F., P. Oliveira & L. Suesdek (2015). Wing sexual dimorphism of pathogen-vector culicids. Parasite and Vectors 8(1): 159–167; http://doi.org/10.1186/s13071-015-0769-6
Webster, M. & H.D. Sheets (2010). A practical introduction to landmark-based geometric morphometrics. pp. 163–188. In: Alroy, J. & G. Hunt (eds.). Quantitative Methods in Paleobiology. Paleontological Society Papers. Volume 16.
Xue, R.D., D.R. Barnard & G.C. Muller (2010). Effects of body size and nutritional regimen on survival in adult Aedes albopictus (Diptera: Culicidae). Journal of Medical Entomology 47(5): 778–782; http://doi.org/10.1603/ME09222