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Differential inhibition of egg hatching in Aedes aegypti populations from localities with different winter conditions

Published online by Cambridge University Press:  27 November 2020

Raúl E. Campos
Affiliation:
Instituto de Limnología ‘Dr Raúl A. Ringuelet’, Universidad Nacional de La Plata-CONICET, CCT La Plata, Boulevard 120 y 62, No. 1437, La Plata (B 1900), Buenos Aires, Argentina
Gabriela Zanotti
Affiliation:
Departamento de Ecología, Genética y Evolución, and Instituto IEGEBA (UBA-CONICET), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, 4to piso, Laboratorio 54, C1428EHA, Buenos Aires, Argentina
Cristian M. Di Battista
Affiliation:
Instituto de Limnología ‘Dr Raúl A. Ringuelet’, Universidad Nacional de La Plata-CONICET, CCT La Plata, Boulevard 120 y 62, No. 1437, La Plata (B 1900), Buenos Aires, Argentina
Javier O. Gimenez
Affiliation:
Instituto de Medicina Regional, Área de Entomología, Universidad Nacional del Nordeste (UNNE), Avda. Las Heras, 727, 3500, Resistencia, Chaco, Argentina
Sylvia Fischer*
Affiliation:
Departamento de Ecología, Genética y Evolución, and Instituto IEGEBA (UBA-CONICET), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, 4to piso, Laboratorio 54, C1428EHA, Buenos Aires, Argentina
*
Author for correspondence: Sylvia Fischer, Email: [email protected]

Abstract

In Argentina, the mosquito Aedes aegypti (L.) (Diptera: Culicidae) is distributed from subtropical to temperate climates. Here, we hypothesized that the expansion of Ae. aegypti into colder regions is favoured by high-phenotypic plasticity and an adaptive inhibition of egg hatching at low temperatures. Thus, we investigated the hatching response of eggs of three populations: one from a subtropical region (Resistencia) and two from temperate regions (Buenos Aires City and San Bernardo) of Argentina. Eggs collected in the field were raised in three experimental colonies. F1 eggs were acclimated for 7 days prior to immersion at 7.6 or 22°C (control eggs). Five immersion temperatures were tested: 7.6, 10.3, 11.8, 14.1 and 16°C (range of mean winter temperatures of the three localities). A second immersion at 22°C was performed 2 weeks later to assess the inhibition to hatch under favourable conditions. After the first immersion, we compared the proportions of hatched eggs and dead larvae among treatment levels, whereas after the second immersion we compared the hatching response among the three populations. The factors that most influenced the egg hatching response were the geographical origin of the populations and the immersion temperature, but not the acclimation temperature. The proportions of hatching and larval mortality at low temperatures were higher for Resistencia than for Buenos Aires and San Bernardo, whereas the hatching response at ambient temperature was lower for San Bernardo than for Buenos Aires and Resistencia. The results support the hypothesis that populations from colder regions show an adaptive inhibition of egg hatching.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press.

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References

Bond, HA, Keirans, JE and Babbitt, MF (1970) Environmental influences on the viability of overwintering Aedes aegypti (L.) eggs. Mosquito News 30, 528533.Google Scholar
Bradshaw, WE (1976) Geography of photoperiodic response in diapausing mosquito. Nature 262, 384385.CrossRefGoogle ScholarPubMed
Brady, OJ, Golding, N, Pigott, DM, Kraemer, MUG, Messina, JP, Reiner, RC Jr, Scott, TW, Smith, DL, Gething, PW and Hay, SI (2014) Global temperature constraints on Aedes aegypti and Ae. albopictus persistence and competence for dengue virus transmission. Parasites & Vectors 7, 338.CrossRefGoogle ScholarPubMed
Brown, HE, Smith, C and Lashway, S (2017) Influence of the length of storage on Aedes aegypti (Diptera: Culicidae) egg viability. Journal of Medical Entomology 54, 489491.Google ScholarPubMed
Byttebier, B, De Majo, MS and Fischer, S (2014) Hatching response of Aedes aegypti (Diptera: Culicidae) eggs at low temperatures: effects of hatching media and storage conditions. Journal of Medical Entomology 51, 97103.CrossRefGoogle ScholarPubMed
Campos, RE (1993) Presencia de Aedes (Stegomyia) aegypti L. 1762 (Diptera: Culicidae) en la localidad de Quilmes, Provincia de Buenos Aires, República Argentina. Revista de la Sociedad Entomológica Argentina 52, 36.Google Scholar
Carbajo, AE, Cardo, MV and Vezzani, D (2019) Past, present and future of Aedes aegypti in its South American southern distribution fringe: what do temperature and population tell us? Acta Tropica 190, 149156.CrossRefGoogle ScholarPubMed
Carrizo Páez, RE, Carrizo Páez, MA and Murúa, AF (2016) First record of Aedes aegypti (Diptera: Culicidae) in San Juan, Argentina. Revista de la Sociedad Entomológica Argentina 75, 9395.Google Scholar
Chen, B and Kang, L (2005) Insect population differentiation in response to environmental stress. Progress in Natural Science 15(4), 289296.Google Scholar
Chown, SL and Terblanche, JS (2007) Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology 33, 50152.CrossRefGoogle Scholar
Conover, WJ (1999) Practical Nonparametric Statistics, 3rd Edn. New York, NY: John Wiley & Sons.Google Scholar
Curto, SI, Boffi, R, Carbajo, AE, Plastina, R and Schweigmann, N (2002) Reinfestación del territorio argentino por Aedes aegypti. Distribución geográfica (1994–1999). In Salomón, OD (ed.), Actualizaciones en Artropodología Sanitaria Argentina. Buenos Aires: Fundación Mundo Sano, pp. 127137.Google Scholar
Davis, NC (1932) The effects of heat and of cold upon Aedes (Stegomyia) aegypti. Part I: The survival of Stegomyia eggs under abnormal temperature conditions. American Journal of Epidemiology 16(1), 177191.CrossRefGoogle Scholar
De Majo, MS, Montini, P and Fischer, S (2017) Egg hatching and survival of immature stages of Aedes aegypti (Diptera: Culicidae) under natural temperature conditions during the cold season in Buenos Aires, Argentina. Journal of Medical Entomology 54, 106113.CrossRefGoogle ScholarPubMed
De Majo, MS, Zanotti, G, Campos, RE and Fischer, S (2019) Effects of constant and fluctuating low temperatures on the development of Aedes aegypti (Diptera: Culicidae) from a temperate region. Journal of Medical Entomology 56(6), 16611668.CrossRefGoogle Scholar
Denlinger, DL and Armbruster, PA (2014) Mosquito diapause. Annual Review of Entomology 59, 7393.CrossRefGoogle ScholarPubMed
Di Rienzo, JA, Casanoves, F, Balzarini, MG, Gonzalez, L, Tablada, M and Robledo, CW (2019) InfoStat versión 2019. Centro de Transferencia InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. Available at http://www.infostat.com.ar.Google Scholar
Diez, F, Breser, VJ, Quirán, EM and Rossi, GC (2014) Infestation levels and new records of Aedes aegypti (Diptera: Culicidae) in La Pampa Province, Argentina. Revista Chilena de Entomología 39, 6772.Google Scholar
Domínguez, C and Lagos, S (2001) Presencia de Aedes aegypti (Diptera: Culicidae) en la provincia de Mendoza, Argentina. Revista de la Sociedad Entomológica Argentina 60, 7980.Google Scholar
Eisen, L, Monaghan, AJ, Lozano Fuentes, S, Steinhoff, DF, Hayden, MH and Bieringer, PE (2014) The impact of temperature on the bionomics of Aedes (Stegomyia) aegypti, with special reference to the cool geographic range margins. Journal of Medical Entomology 51, 496516.CrossRefGoogle ScholarPubMed
Farnesi, LC, Martins, AJ, Valle, D and Rezende, GL (2009) Embryonic development of Aedes aegypti (Diptera: Culicidae): influence of different constant temperatures. Memorias do Instituto Oswaldo Cruz 104, 124126.CrossRefGoogle ScholarPubMed
Fischer, S, De Majo, MS, Quiroga, L, Paez, M and Schweigmann, N (2017) Long-term spatio-temporal dynamics of the mosquito Aedes aegypti in temperate Argentina. Bulletin of Entomological Research 107(2), 225233.CrossRefGoogle ScholarPubMed
Fischer, S, De Majo, MS, Di Battista, CM, Montini, P, Loetti, V and Campos, RE (2019) Adaptation to temperate climates: evidence of photoperiod-induced embryonic dormancy in Aedes aegypti in South America. Journal of Insect Physiology 117, 103887.CrossRefGoogle ScholarPubMed
Gillett, JD (1955a) Variation in the hatching response of Aedes eggs (Diptera; Culicidae). Bulletin of Entomological Research 46, 241254.CrossRefGoogle Scholar
Gillett, JD (1955b) The inherited basis of variation in the hatching response of Aedes eggs (Diptera: Culicidae). Bulletin of Entomological Research 46, 255265.CrossRefGoogle Scholar
Grech, M, Visintin, A, Laurito, M, Estallo, E, Lorenzo, P, Roccia, I, Korin, M, Goya, F, Ludueña Almeida, F and Almirón, W (2013) New records of mosquito species (Diptera: Culicidae) from Neuquén and La Rioja provinces, Argentina. Revista de Saude Publica 46, 387389.CrossRefGoogle Scholar
Huey, R, Gilchrist, G and Hendry, A (2005) Using invasive species to study evolution: case studies with Drosophila and salmon. In Sax, D, Stachowicz, J and Gaines, S (eds), Species Invasions: Insights into Ecology, Evolution, and Biogeography. New York: Sinauer, pp. 139164.Google Scholar
INDEC (2010) Censo 2010 Provincia de Buenos Aires. Resultados definitivos por partido. Available at http://www.estadistica.ec.gba.gov.ar/dpe/Estadistica/CENSO2010%20REVISION/librocenso2010.pdf.Google Scholar
Khatchikian, CE, Dennehy, JJ, Vitek, CJ and Livdahl, T (2009) Climate and geographic trends in hatch delay of the treehole mosquito, Aedes triseriatus Say (Diptera: Culicidae). Journal of Vector Ecology 34, 119128.CrossRefGoogle Scholar
Kraemer, MUG, Sinka, ME, Duda, KA, Mylne, AQN, Shearer, FM, Barker, CM, Moore, CG, Carvalho, RG, Coelho, GE, Van Bortel, W, Hendrickx, G, Schaffner, F, Elyazar, IRF, Teng, HJ, Brady, OJ, Messina, JP, Pigott, DM, Scott, TW, Smith, DL, Wint, GRW, Golding, N and Hay, SI (2015) The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. eLife 4, e08347.CrossRefGoogle ScholarPubMed
Kraemer, MUG, Reiner, RC, Brady, OJ, et al. (2019) Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nature Microbiology 4, 854863.CrossRefGoogle ScholarPubMed
Lee, CE, Remfert, JL and Chang, Y-M (2007) Response to selection and evolvability of invasive populations. Genetica 129, 179192.CrossRefGoogle ScholarPubMed
Lima, A, Lovin, DD, Hickner, PV and Severson, DW (2016) Evidence for an overwintering population of Aedes aegypti in Capitol Hill Neighborhood, Washington, DC. American Journal of Tropical Medicine and Hygiene 94, 231235.CrossRefGoogle ScholarPubMed
Lounibos, PL and Kramer, LD (2016) Invasiveness of Aedes aegypti and Aedes albopictus and vectorial capacity for Chikungunya virus. The Journal of Infectious Disease 214 (suppl. 5), 453458.CrossRefGoogle ScholarPubMed
Mayer, SV, Tesh, RB and Vasilakis, N (2017) The emergence of arthropod-borne viral diseases: a global prospective on dengue, Chikungunya and Zika fevers. Acta Tropica 166, 155163.CrossRefGoogle ScholarPubMed
Medlock, JM, Hnasford, KM, Versteirt, V, Cull, B, Kampen, H, Fontenille, D, Hendrickx, G, Zeller, H, Van Bortel, W and Schaffner, F (2015) An entomological review of invasive mosquitoes in Europe. Bulletin of Entomological Research 105, 637663.CrossRefGoogle ScholarPubMed
Ponnusamy, L, Böröczky, K, Wesson, DM, Schal, C and Apperson, CS (2011) Bacteria stimulate hatching of yellow fever mosquito eggs. PLoS One 6, e24409.CrossRefGoogle ScholarPubMed
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at https://www.R-project.org/.Google Scholar
Rossi, GC, Lestani, EA and D'Oria, JM (2006) Nuevos registros y distribución de mosquitos de la Argentina (Diptera: Culicidae). Revista de la Sociedad Entomológica Argentina 65, 5156.Google Scholar
Rubio, A, Cardo, MV, Vezzani, D and Carbajo, AE (2020) Aedes aegypti spreading in South America: new coldest and southernmost records. Memórias do Instituto Oswaldo Cruz 115, e190496.CrossRefGoogle ScholarPubMed
Rusticucci, MM, Venegas, SA and Vargas, WA (2003) Warm and cold events in Argentina and their relationship with South Atlantic and South Pacific Sea surface temperatures. Journal of Geophysical Research 108(11), 110.CrossRefGoogle Scholar
Sinclair, BJ, Williams, CM and Terblanche, JS (2012) Variation in thermal performance among insect populations. Physiological and Biochemical Zoology 85(6), 594606.CrossRefGoogle ScholarPubMed
Soper, FL (1967) Dynamics of Aedes aegypti distribution and density. Seasonal fluctuations in the Americas. Bulletin of the World Health Organization 36, 536538.Google ScholarPubMed
Stein, M and Oria, GI (2002) Identificación de criaderos de Aedes aegypti (Diptera: Culicidae) y cálculo de índices de infestación en la provincia del Chaco. In Salomón, OD (ed.), Actualizaciones en Artropodología Sanitaria Argentina. Buenos Aires: Fundación Mundo Sano, pp. 161166.Google Scholar
Tauber, MJ, Tauber, CA and Masaki, S (1986) Seasonal Adaptations of Insects. New York, USA: Oxford University Press.Google Scholar
Thomas, SM, Obermayr, U, Fischer, D, Kreyling, J and Beierkuhnlein, C (2012) Low-temperature threshold for egg survival of a post-diapause and non-diapause European aedine strain, Aedes albopictus (Diptera: Culicidae). Parasites & Vectors 5, 100.CrossRefGoogle Scholar
Urbanski, J, Mogi, M, O'Donnell, D, DeCotiis, M, Toma, T and Armbruster, P (2012) Rapid adaptive evolution of photoperiodic response during invasion and range expansion across a climatic gradient. American Naturalist 179, 490500.CrossRefGoogle ScholarPubMed
Vinogradova, EB (2007) Diapause in aquatic insects, with emphasis on mosquitoes. In Alekseev, VR, De Stasio, BT and Gilbert, JJ (eds), Diapause in Aquatic Invertebrates: Theory and Human Use. Dordrecht, The Netherlands: Springer, pp. 83113.CrossRefGoogle Scholar
Visintin, AM, Laurito, M, Diaz, LA, Benítez Musicant, G, Cano, C, Ramírez, R and Almirón, WR (2009) New records of mosquito species for central and Cuyo regions in Argentina. Journal of the American Mosquito Control Association 25, 208209.CrossRefGoogle ScholarPubMed
Vitek, CJ and Livdahl, TP (2006) Field and laboratory comparison of hatch rates in Aedes albopictus (Skuse). Journal of the American Mosquito Control Association 22, 609614.CrossRefGoogle Scholar
Warkentin, KM (2011) Environmentally cued hatching across taxa: embryos respond to risk and opportunity. Integrative and Comparative Biology 51, 1425.CrossRefGoogle ScholarPubMed
Weissman-Strum, A and Kindler, SH (1963) Effect of low temperatures on development, hatching and survival of the eggs of Aedes aegypti (L.). Nature 196, 12311232.CrossRefGoogle Scholar
Whitman, DW and Agrawal, AA (2009) What is phenotypic plasticity and why is it important? In Whitman, DW and Ananthakrishnan, TN (eds), Phenotypic Plasticity in Insects: Mechanisms and Consequences. Enfield, NH, USA: Science Publishers, pp. 163.Google Scholar
Zanotti, G, De Majo, MS, Alem, I, Schweigmann, N, Campos, R and Fischer, S (2015) New records of Aedes aegypti at the southern limit of its distribution in Buenos Aires province, Argentina. Journal of Vector Ecology 40, 408411.CrossRefGoogle Scholar
Zheng, ML, Zhang, DJ, Damiens, DD, Lees, RS and Gilles, JRL (2015) Standard operating procedures for standardized mass rearing of the dengue and Chikungunya vectors Aedes aegypti and Aedes albopictus (Diptera: Culicidae) – II – egg storage and hatching. Parasites & Vectors 8, 348.CrossRefGoogle ScholarPubMed
Zuur, AF, Ieno, EN, Walker, NJ, Saveliev, AA and Smith, GM (2009) Mixed Effects Models and Extensions in Ecology with R. New York, NY: Springer Science+Business Media.CrossRefGoogle Scholar