Hostname: page-component-f554764f5-44mx8 Total loading time: 0 Render date: 2025-04-22T12:13:27.643Z Has data issue: false hasContentIssue false
  • English
  • Français

Adaptation to different temperatures results in wing size divergence of the invading species Drosophila nasuta (Diptera: Drosophilidae) in Brazil

Published online by Cambridge University Press:  04 November 2024

Vinícius Alcântara Carvalho Lima Santos Open the ORCID record for Vinícius Alcântara Carvalho Lima Santos [Opens in a new window] ,
Ana Cristina Lauer Garcia Open the ORCID record for Ana Cristina Lauer Garcia [Opens in a new window]  and
Martín Alejandro Montes Open the ORCID record for Martín Alejandro Montes [Opens in a new window]
Vinícius Alcântara Carvalho Lima Santos
Affiliation:
Universidade Federal Rural de Pernambuco, Campus Dois Irmãos, Departamento de Biologia, Recife, Pernambuco, Brazil
Ana Cristina Lauer Garcia*
Affiliation:
Universidade Federal de Pernambuco, Centro Acadêmico de Vitória, Vitória de Santo Antão, Pernambuco, Brazil
Martín Alejandro Montes*
Affiliation:
Universidade Federal Rural de Pernambuco, Campus Dois Irmãos, Departamento de Biologia, Recife, Pernambuco, Brazil
*
Corresponding author: Ana Cristina Lauer Garcia; Email: [email protected]; Martín Alejandro Montes; Email: [email protected]
Corresponding author: Ana Cristina Lauer Garcia; Email: [email protected]; Martín Alejandro Montes; Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Invasive species threaten biodiversity on a global scale. The success of invasions depends on the species' adaptation to the different environmental conditions of new territories. Studies show that invasive insects present evolutionary changes in wing morphology in areas they are introduced to in response to abiotic conditions. In the last decade, the Asian Drosophila nasuta fly invaded and spread widely throughout Brazil. This insect has preferences for conserved environments and is related to the likely reduction in the abundance of native drosophilids in the Atlantic Forest. Ecological niche modelling analyses showed that rainfall and temperature are the main factors which delimit the geographic distribution of this species. Herein, we verified the existence of significant differences in the wing sizes of D. nasuta in Brazil and evaluated the influence of abiotic factors (rainfall and temperature) on the observed patterns. We conducted 11 measurements on the right-side wings of 240 D. nasuta males collected in the Amazon Forest, Caatinga, Cerrado and Atlantic Forest. Statistical analyses revealed the existence of two groups: one with larger wings, which brought together samples from locations with the lowest temperatures; and one with smaller wings, which corresponded to places with a hotter climate. One explanation for this result is the fact that large wings favour greater heat capture by flies in colder climates, increasing their survival chances in these environments. These rapid evolutionary changes in D. nasuta in this first decade of invasion in Brazil reveal the enormous adaptive potential of this species in this megadiverse country.

Keywords

abiotic factorsBrazilian biomesexotic speciesinsectsmicroevolutionmorphometry
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 114 , Issue 6 , December 2024 , pp. 756 - 762
Check for updates
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

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.)

Article purchase

Temporarily unavailable

References

Berwaerts, K, Aerts, P and van Dyck, H (2006) On the sex-specific mechanisms of butterfly flight: flight performance relative to flight morphology, wing kinematics, and sex in Pararge aegeria. Biological Journal of the Linnean Society 89, 675–687.CrossRefGoogle Scholar
Betts, CR and Wootton, RJ (1988) Wing shape and flight behaviour in butterflies (Lepidoptera: Papilionoidea and Hesperioidea): a preliminary analysis. Journal of Experimental Biology 138, 271–288.CrossRefGoogle Scholar
Bitner-Mathé, BC and Klaczko, LB (1999) Size and shape heritability in natural populations of Drosophila mediopunctata: temporal and microgeographical variation. Genetica 105, 35–42.CrossRefGoogle ScholarPubMed
David, JR, Araripe, LO, Bitner-Mathé, BC, Capy, P, Goñi, B, Klaczko, LB, Legout, H, Martins, MB, Voudibio, J, Yassin, A and Moreteau, B (2006) Quantitative trait analysis and geographic variability of natural populations of Zaprionus indianus, a recent invader in Brazil. Heredity 96, 53–62.CrossRefGoogle ScholarPubMed
Douglas, MM (1981) Thermoregulatory significance of thoracic lobes in the evolution of insect wings. Science 211, 84–86.CrossRefGoogle ScholarPubMed
Fox, NS, Veneracion, JJ and Blois, JL (2020) Are geometric morphometric analyses replicable? Evaluating landmark measurement error and its impact on extant and fossil Microtus classification. Ecology and Evolution 10, 3260–3275.CrossRefGoogle ScholarPubMed
Fraimout, A, Jacquemart, P, Villarroel, B, Aponte, DJ, Decamps, T, Herrel, A, Cornette, R and Debat, V (2018) Phenotypic plasticity of Drosophila suzukii wing to developmental temperature: implications for flight. Journal of Experimental Biology 221, jeb166868.CrossRefGoogle Scholar
Garcia, ACL, Silva, FP, Neves, CHCB and Montes, MA (2022) Current and future potential global distribution of the invading species Drosophila nasuta (Diptera: Drosophilidae). Biological Journal of the Linnean Society 135, 208–221.CrossRefGoogle Scholar
Gilchrist, GW and Huey, RB (2004) Plastic and genetic variation in wing loading as a function of temperature within and among parallel clines in Drosophila subobscura. Integrative and Comparative Biology 44, 461–470.CrossRefGoogle ScholarPubMed
Gilchrist, GW, Huey, RB, Balanyà, J, Pascual, M, Serra, L and Noor, M (2004) A time series of evolution in action: a latitudinal cline in wing size in South American Drosophila subobscura. Evolution 58, 768–780.Google Scholar
Glass, JR, Burnett, NP, Combes, SA, Weisman, E, Helbling, A and Harrison, JF (2024) Flying, nectar-loaded honey bees conserve water and improve heat tolerance by reducing wingbeat frequency and metabolic heat production. Proceedings of the National Academy of Sciences 121, e2311025121.CrossRefGoogle ScholarPubMed
Guayasamin, JM, Ribas, CC, Carnaval, AC, Carrillo, JD, Hoorn, C, Lohmann, LG, Riff, D, Ulloa, CU and Albert, JS (2024) Evolution of Amazonian biodiversity: a review. Acta Amazonica 54, e54bc21360.CrossRefGoogle Scholar
Hammer, Ø, Harper, DAT and Ryan, PD (2001) Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 1–9.Google Scholar
Heinrich, B (1974) Thermoregulation in endothermic insects. Science 185, 747–756.CrossRefGoogle ScholarPubMed
Huey, RB, Gilchrist, GW, Carlson, ML, Berrigan, D and Serra, L (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287, 308–309.CrossRefGoogle Scholar
IBGE (2019) Biomas e sistema costeiro-marinho do Brasil: compatível com a escala 1: 250000. Coordenação de Recursos Naturais e Estudos Ambientais, Rio de Janeiro. Available at https://biblioteca.ibge.gov.br/visualizacao/livros/liv101676.pdfGoogle Scholar
Karan, D, Moreteau, B and David, JR (1999) Growth temperature and reaction norms of morphometrical traits in a tropical drosophilid: Zaprionus indianus. Heredity 83, 398–407.CrossRefGoogle Scholar
Laparie, M, Vernon, P, Cozic, Y, Frenot, Y, Renault, D and Debat, V (2016) Wing morphology of the active flyer Calliphora vicina (Diptera: Calliphoridae) during its invasion of a sub-Antarctic archipelago where insect flightlessness is the rule. Biological Journal of the Linnean Society 119, 179–193.CrossRefGoogle Scholar
Leão, BFD, Roque, F, Deus, PHM and Tidon, R (2017) What happens when exotic species arrive in a new area? The case of drosophilids in the Brazilian Savanna. Drosophila Information Service 100, 65–69.Google Scholar
Loh, R and Bitner-Mathé, BC (2005) Variability of wing size and shape in three populations of a recent Brazilian invader, Zaprionus indianus (Diptera: Drosophilidae), from different habitats. Genetica 125, 271–281.CrossRefGoogle ScholarPubMed
Loh, R, David, JR, Debat, V and Bitner-Mathé, BC (2008) Adaptation to different climates results in divergent phenotypic plasticity of wing size and shape in an invasive drosophilid. Journal of Genetics 87, 209–217.CrossRefGoogle Scholar
Martins, TCSL, Santos, MFS, Santos, MMS, Araújo, JS, Neves, CHCB, Garcia, ACL and Montes, MA (2023) Drosophila nasuta (Diptera, Drosophilidae) in Brazil: a decade of invasion and occupation of more than half of the country. Anais da Academia Brasileira de Ciências 95, e20230507.CrossRefGoogle Scholar
Medeiros, HF, Monteiro, MP, Caçador, AWB, Pereira, CM, Praxedes, CLB, Martins, MB, Montes, MA and Garcia, ACL (2022) First records of the invading species Drosophila nasuta (Diptera: Drosophilidae) in the Amazon. Neotropical Entomology 51, 493–497.CrossRefGoogle ScholarPubMed
Mittermeier, RA, Turner, WR, Larsen, FW, Brooks, TM and Gascon, C (2011) Global biodiversity conservation: the critical role of hotspots. In Zachos, F and Habel, J (eds), Biodiversity Hotspots: Distribution and Protection of Conservation Priority Areas. Berlin, Heidelberg: Springer Berlin Heidelberg, pp. 3–22.CrossRefGoogle Scholar
Mollot, G, Pantel, JH and Romanuk, TN (2017) The effects of invasive species on the decline in species richness: a global meta-analysis. Advances in Ecological Research 56, 61–83.CrossRefGoogle Scholar
Montes, MA, Neves, CHCB, Ferreira, AF, Santos, MFS, Quintas, JIFP, Manetta, GDA, Oliveira, PV and Garcia, ACL (2021) Invasion and spreading of Drosophila nasuta (Diptera, Drosophilidae) in the Caatinga Biome, Brazil. Neotropical Entomology 50, 571–578.CrossRefGoogle ScholarPubMed
Oliveira, GH (2021) Avaliação da homogeneização biótica e preferência ambiental de drosofilídeos invasores no norte da Floresta Atlântica (Masters Thesis). Universidade Federal Rural de Pernambuco, Brazil.Google Scholar
Pass, G (2018) Beyond aerodynamics: the critical roles of the circulatory and tracheal systems in maintaining insect wing functionality. Arthropod Structure and Development 47, 391–407.CrossRefGoogle ScholarPubMed
Przybylska, MS, de Brito, FA and Tidon, R (2016) Ecological insights from assessments of phenotypic plasticity in a Neotropical species of Drosophila. Journal of Thermal Biology 62, 7–14.CrossRefGoogle Scholar
Pyšek, P, Hulme, PE, Simberloff, D, Bacher, S, Blackburn, TM, Carlton, JT, Dawson, W, Essl, F, Foxcroft, LC, Genovesi, P, Jeschke, JM, Kühn, I, Liebhold, AM, Mandrak, NE, Meyerson, LA, Pauchard, A, Pergl, J, Roy, HE, Seebens, H, van Kleunen, M, Vilà, M, Wingfield, MJ and Richardson, DM (2020) Scientists’ warning on invasive alien species. Biological Reviews 95, 1511–1534.CrossRefGoogle ScholarPubMed
Rejmánek, M and Richardson, DM (1996) What attributes make some plant species more invasive? Ecology 77, 1655–1661.CrossRefGoogle Scholar
Rohlf, FJ (2016) Thin-plate spline (TPS) computer program. Available at http://www.sbmorphometrics.org/index.htmlGoogle Scholar
Santos, MFS, Neves, CHCB, Oliveira, E, Ribeiro, MC, Faria-Júnior, JEQ, Montes, MA and Garcia, ACL (2021) Genetic diversity of the invasive species Drosophila nasuta (Diptera, Drosophilidae) in different biomes in Brazil. p. 275. In: 66° Brazilian Congress of Genetics, Ribeirão Preto, Brazil, 13 September – 16 September, Brazilian Society of Genetics.Google Scholar
Schäfer, MA, Berger, D, Rohner, PT, Kjaersgaard, A, Bauerfeind, SS, Guillaume, F, Fox, CW and Blanckenhorn, WU (2018) Geographic clines in wing morphology relate to colonization history in New World but not Old World populations of yellow dung flies. Evolution 72, 1629–1644.CrossRefGoogle Scholar
Seebens, H, Blackburn, TM, Dyer, EE, Genovesi, P, Hulme, PE, Jeschke, JM, Pagad, S, Pyšek, P, van Kleunen, M, Winter, M, Ansong, M, Arianoutsou, M, Bacher, S, Blasius, B, Brockerhoff, EG, Brundu, G, Capinha, C, Causton, CE, Celesti-Grapow, L, Dawson, W, Dullinger, S, Economo, EP, Fuentes, N, Guénard, B, Jäger, H, Kartesz, J, Kenis, M, Kühn, I, Lenzner, B, Liebhold, AM, Mosena, A, Moser, D, Nentwig, W, Nishino, M, Pearman, D, Pergl, J, Rabitsch, W, Rojas-Sandoval, J, Roques, A, Rorke, S, Rossinelli, S, Roy, HE, Scalera, R, Schindler, S, Štajerová, K, Tokarska-Guzik, B, Walker, K, Ward, DF, Yamanaka, T and Essl, F (2018) Global rise in emerging alien species results from increased accessibility of new source pools. Proceedings of the National Academy of Sciences 115, E2264–E2273.CrossRefGoogle ScholarPubMed
Silva, JMC, Leal, IR and Tabarelli, M (2017) Caatinga: The Largest Tropical Dry Forest Region in South America. New York: Springer.CrossRefGoogle Scholar
Silva, DG, Schmitz, HJ, Medeiros, HF, Rohde, C, Montes, MA and Garcia, ACL (2020) Geographic expansion and dominance of the invading species Drosophila nasuta (Diptera, Drosophilidae) in Brazil. Journal of Insect Conservation 24, 525–534.CrossRefGoogle Scholar
Spatz, DR, Jones, HP, Bonnaud, E, Kappes, P, Holmes, ND and Guzmán, YB (2023) Invasive species threats to seabirds. In Young, L and VanderWerf, E (eds), Conservation of Marine Birds. London: Academic Press, pp. 97–130.CrossRefGoogle Scholar
Su, T, Cui, G, Man, Z, Li, W, Huang, Z, Chen, J and Zhao, M (2023) Interspecific association of sika deer in terrestrial animal communities of Liancheng National Nature Reserve, China. Integrative Zoology 18, 688–703.CrossRefGoogle ScholarPubMed
Sun, J, Koski, TM, Wickham, JD, Baranchikov, YN and Bushley, KE (2024) Emerald ash borer management and research: decades of damage and still expanding. Annual Review of Entomology 69, 239–258.CrossRefGoogle ScholarPubMed
Tabarelli, M, Pinto, LP, Silva, JM, Hirota, M and Bede, L (2005) Challenges and opportunities for biodiversity conservation in the Brazilian Atlantic Forest. Conservation Biology 19, 695–700.CrossRefGoogle Scholar
Tidon, R and Sene, FM (1988) A trap that retains and keeps Drosophila alive. Drosophila Information Service 67, 89.Google Scholar
Vilela, CR and Goñi, B (2015) Is Drosophila nasuta Lamb (Diptera, Drosophilidae) currently reaching the status of a cosmopolitan species? Revista Brasileira de Entomologia 59, 346–350.CrossRefGoogle Scholar
Walter, BMT, Carvalho, AD and Ribeiro, JF (2008) O conceito de savana e de seu componente Cerrado. In Sano, SM, de Almeida, SP and Ribeiro, JF (eds), Cerrado: ecologia e flora. Distrito Federal: Embrapa Cerrados, pp. 21–45.Google Scholar
Wootton, RJ (1992) Functional morphology of insect wings. Annual Review of Entomology 37, 113–140.CrossRefGoogle Scholar
Yassin, A, David, JR and Bitner-Mathé, BC (2009) Phenotypic variability of natural populations of an invasive drosophilid, Zaprionus indianus, on different continents: comparison of wild-living and laboratory-grown flies. Comptes Rendus Biologies 332, 898–908.CrossRefGoogle ScholarPubMed
Supplementary material: File

Santos et al. supplementary material

Santos et al. supplementary material
Download Santos et al. supplementary material(File)
File 15.9 KB