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Pheromone emission patterns and courtship sequences across distinct populations within Anastrepha fraterculus (Diptera-Tephritidae) cryptic species complex

Published online by Cambridge University Press:  29 November 2018

A.K.P. Roriz*
Affiliation:
Universidade Federal da Bahia, Instituto de Biologia, Barão do Jeremoabo s/n, Campus Universitário de Ondina, 40170-290, Salvador, BA, Brazil
H.F. Japyassú
Affiliation:
Universidade Federal da Bahia, Instituto de Biologia, Barão do Jeremoabo s/n, Campus Universitário de Ondina, 40170-290, Salvador, BA, Brazil National Institute of Science and Technology on Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution, R. Barão do Jeremoabo s/n, Campus Universitário de Ondina, 40170-290, Salvador, BA, Brazil
C. Cáceres
Affiliation:
Insect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, POBox 100, Seibersdorf, Austria
M. Teresa Vera
Affiliation:
Cátedra Terapéutica Vegetal, Departamento de Sanidad Vegetal, Facultad de Agronomía y Zootecnia, UNT, Avenida Kirchner 1900 – (4000) San Miguel de Tucumán, Tucumán, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
I.S. Joachim-Bravo
Affiliation:
Universidade Federal da Bahia, Instituto de Biologia, Barão do Jeremoabo s/n, Campus Universitário de Ondina, 40170-290, Salvador, BA, Brazil
*
*Author for correspondence Phone: +55 71 32836545 Fax: +55 71 32836511 E-mail: kellyroriz@gmail.com

Abstract

Sexual behavioural isolation can result from sexual selection and represents a relevant factor associated with the speciation process. We analysed the pheromone emission pattern and the courtship of males of five different populations of the Anastrepha fraterculus cryptic complex: Brazil (Vacaria, Tucumán and Piracicaba), Colombia and Peru. The time of pheromone emission was recorded in each population every 30 min during the day. The behavioural sequences of courting were video recorded and analysed using EthoSeq software. Males from different populations have showed different period of pheromone emission – Vacaria, Piracicaba and Tucumán executed calling only during the morning, Colombia only in the afternoon and Peru during both periods. The general frequencies of the courtship units of the males were distinct among the populations. Three groups were formed in the classification from the function of 14 behavioural routines: Vacaria, Piracicaba and Tucumán formed a single group (Brazil-1), while Colombia and Peru formed two distinct groups. In the probabilistic trees generated, the behavioural units that most contributed to the occurrence of copulation were distinct among the three groups formed: Brazil-1 (Contact, Alignment and Arrowhead-1); Colombia (Flying, Mobile, Contact and Alignment); Peru (Flying, Arrowhead-1 and Calling). Our results indicated differences in sexual behaviour that may explain the behavioural isolation found between the distinct groups in addition with the temporal isolation found between the Brazil-1 and Colombia populations. The evolutionary implications for the A. fraterculus cryptic species complex are discussed.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

The original version of this article was published with an error in the title and one incorrect author name. A notice detailing these has been published and the error rectified in both the PDF and HTML versions.

References

Alberti, A.C., Confalonieri, V.A., Zandomeni, R.O. & Vilardi, J.C. (2008) Phylogeographic studies on natural populations of the South American fruit fly, Anastrepha fraterculus (Diptera : Tephritidae). Genetica 132, 18.Google Scholar
Aluja, M. (1994). Bionomics and management of Anastrepha. Annual Review of Entomology 39, 155178.Google Scholar
Aluja, M., Piñero, J., Jácome, I., Díaz-Fleischer, F. & Sivinski, J. (1999) Behavior of flies in the genus Anastrepha (Trypetinae: Toxotrypanini). pp. 375406 in Aluja, M. & Norrbom, A. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, CRC Press.Google Scholar
Andersson, M. (1994) Sexual Selection. Princeton, NJ: Princeton University Press.Google Scholar
Antony, C. & Jallon, J.M. (1982) The chemical basis for sex recognition in Drosophila melanogaster. Journal of Insect Physiology 28, 873880.Google Scholar
Besag, J.E. (1972) Nearest-neighbour systems and the auto-logistic model for binary data. Journal of the Royal Statistical Society 34, 7583.Google Scholar
Boake, C.R.B. Deangelis, M.P., Ebra, K. & Andreadis, EK (1997) Is sexual selection and species recognition a continuum? Mating behavior of the stalk-eyed fly Drosophila heteroneura. Proceedings of the National Academy of Sciences USA 94, 1244212445.Google Scholar
Boller, E.F., Katsoyannos, B.I., Remund, U. & Chamber, D.L. (1981) Mensuring, monitoring and improving the quality of mass-reared Mediterranean fruit flies, Ceratitis capitata (Wied.) 1. The RAPID quality control system for early warning Z. Angew. Entomology 92, 6783.Google Scholar
Briceño, R.D. & Eberhad, W.G. (2002) Courtship in the medfly, Ceratitis capitata, includes tactile stimulation with the male's aristae. Entomologia Experimentalis et Applicata 102, 221228.Google Scholar
Briceño, R.D., Eberhad, W.G., Vilardi, J.C., Cayol, J.P. & Shelly, T. (2007) Courtship behavior of different wild strains of Ceratitis capitata (Diptera: Tephritidae). Florida Entomologist 90, 1518.Google Scholar
Břízová, R., Mendonça, A.L., Vanícková, L., Mendonça, A.L., Da Silva, C.E., Tomčala, A., Paranhos, B.A.J., Dias, V.S., Joachim-Bravo, I.A., Hoskovec, M., Kalinová, B. & Do Nascimento, R.R. (2013) Pheromone analyses of the Anastrepha fraterculus (Diptera: Tephritidae) cryptic species complex. Florida Entomologist 96, 11071115.Google Scholar
Butlin, R.K. & Ritchie, M.G. (1994) Mating behavior and speciation. pp. 4379 in Slater, P.J.B. & Halliday, T.R. (Eds) Behaviour and Evolution. Cambridge, Cambridge University Press.Google Scholar
Cáceres, C., Segura, D.F., Vera, M.T., Wornoayporn, V., Cladera, J.L., Teal, P., Sapountzis, P., Bourtzis, P., Zacharopoulou, A. & Robinson, A.S. (2009) Incipient speciation revealed in Anastrepha fraterculus (Diptera; Tephritidae) by studies on mating compatibility, sex pheromones, hybridization, and cytology. Biological Journal of the Linnean Society 97, 152165.Google Scholar
Canal, A.N., Hernández-Ortiz, V., Tigrero-Salas, J.O. & Selivon, D. (2015) Morphometric study of third-instar larvae from five morphotypes of the Anastrepha fraterculus cryptic species complex (Diptera, Tephritidae). ZooKeys 540, 4159.Google Scholar
Cayol, J.P. (1999) Changes in sexual behavior and life history traits of Tephritid species caused by mass-rearing processes. pp 843860 in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, Florida, USA, CRC Press.Google Scholar
Cobb, M. & Jallon, J.M. (1990) Pheromones, mate recognition and courtship stimulation in the Drosophila melanogaster species sub-group. Animal Behavior 39, 10581067.Google Scholar
Devescovi, F., Abraham, S., Roriz, A.K.P., Nolazco, N., Castaneda, R., Tadeo, E., Cáceres, C., Segura, D.F., Vera, M.T., Joachim-Bravo, I., Canal, N. & Rull, J. (2014) Ongoing speciation within the Anastrepha fraterculus cryptic species complex: the case of the Andean morphotype. Entomologia Experimentalis et Applicata 152, 238247.Google Scholar
Dias, V., Silva, J.G., Lima, K.M., Petitinga, C.S.C.D., Hernandez-Ortiz, V., Laumann, R.A., Paranhos, B.J., Uramoto, K., Zucchi, R.A. & Joachim-Bravo, I.S. (2015) An integrative multidisciplinary approach to understanding cryptic divergence in Brazilian species of the Anastrepha fraterculus complex (Diptera: Tephritidae). Biological Journal of the Linnean Society 117, 725746.Google Scholar
Dobzhansky, T. (1937) Genetics and the Origin of species. New York, Columbia University Press.Google Scholar
Dodson, G. (1982) Mating and territoriality in wild Anastrepha suspensa (Diptera: Tephritidae) in field cages. Journal of the Georgia Entomological Society 17, 189200.Google Scholar
Dutra, B.K., Fernandes, F.A., Nascimento, J.C., Quadros, F.C. & Oliveira, G.T. (2007) Intermediate metabolism during the ontogenetic development of Anastrepha fraterculus (Diptera : Tephritidae). Comparative Biochemistry and Physiology 147, 594599.Google Scholar
Giglio, E.M. & Dyer, K.A. (2013) Divergence of premating behaviors in the closely related species Drosophila subquinaria and D. recens. Ecology and Evolution 3, 365374.Google Scholar
Gomez Cendra, P., Calcagno, G., Belluscio, L. & Vilardi, S.J.C. (2011) Male courtship behavior of the South American fruit fly, Anastrepha fraterculus, from an Argentinean laboratory Strain. Journal of Insect Science 11, 118.Google Scholar
Hernández-Ortiz, V., Gómez-Anaya, J.A., Sánchez, A., McPheron, B.A. & Aluja, M. (2004) Morphometric analysis of Mexican and South American populations of the Anastrepha fraterculus complex (Diptera: Tephritidae) and recognition of a distinct Mexican morphotype. Bulletin of Entomological Research 94, 487499.Google Scholar
Hernández-Ortiz, A.V., Bartolucci, A.F., Morales-valles, P., Frías, D. & Selivon, D. (2012) Cryptic species of the Anastrepha fraterculus complex (Diptera : Tephritidae): a multivariate approach for the recognition of South American morphotypes. Annals of the Entomological Society of America 105, 305318.Google Scholar
Hernández-Ortiz, V., Canal, N.A., Tigrero Salas, J.O., Ruíz-Hurtado, F.M. & Dzul-Cauich, J.F. (2015) Taxonomy and phenotypic relationships of the Anastrepha fraterculus complex in the Mesoamerican and Pacific Neotropical dominions (Diptera, Tephritidae). ZooKeys 540, 95124.Google Scholar
Japyassú, H.F., Alberts, C.C., Izar, P. & Sato, T. (2006) Ethoseq: a tool for phylogenetic analysis and data mining on behavioral sequences. Behavior Research Methods 38, 549556.Google Scholar
Juárez, M.L., Devescovi, F., Břízová, R., Bachmann, G., Segura, D.F., Kalinová, B., Fernández, P., Ruiz, M.J., Yang, J., Teal, P.E.A., Cáceres, C., Vreysen, M.J.B., Hendrichs, J. & Vera, M.T. (2015) Evaluating mating compatibility within fruit fly cryptic species complexes and the potential role of sex pheromones in pre-mating isolation. ZooKeys 540, 125155.Google Scholar
Lande, R. (1981) Models of speciation by sexual selection on polygenic traits. Proceedings of the National Academy of Sciences of the USA 78, 37213725.Google Scholar
Lande, R. (1982) Rapid origin of sexual isolation and character divergence in a cline. Evolution 36, 213223.Google Scholar
Lima, I.S., House, P.E. & do Nascimento, R.R. (2001) Volatile substances from male Anastrepha fraterculus Wied. (Diptera: Tephitidae): identification and behavioral activity. Journal of Brazilian Chemical Society 12, 196201.Google Scholar
Malavasi, A. & Morgante, J.S. (1982) Genetic variation in natural populations of Anastrepha (Diptera: Tephritidae). Revista Brasileira de Genética 5, 253278.Google Scholar
Macedo, R.H. & Machado, G. (2013) Sexual Selection, Perspectives and Models from the Neotropics. 1st edn. Brazil: Academic Press Elsevier, 466p.Google Scholar
Manni, M., Lima, K.M., Guglielmino, C.R., Lanzavecchia, B.S., Juri, M., Vera, T., Cladera, J., Scolari, F., Gomulski, L., Bonizzoni, M., Gasperi, G., Silva, G.J. & Malacrida, A.R. (2015) Relevant genetic differentiation among Brazilian populations of Anastrepha fraterculus (Diptera, Tephritidae). ZooKeys 540, 157173.Google Scholar
Nanda, P. & Singh, B.N. (2012) Behavioural reproductive isolation and speciation in Drosophila. Journal of Bioscience 37, 359374.Google Scholar
Noor, M.A.F. (1999) Reinforcement and other consequences of sympatry. Heredity 83, 503508.Google Scholar
Passos Roriz, A.K., Japyassú, H.F. & Sordi Joachim-Bravo, I. (2018) Courtship in two morphotypes of the Anastrepha fraterculus (Diptera: Tephritidae) cryptic species complex and their implications for understanding mate recognition. Journal of Insect Behavior. https://doi.org/10.1007/s10905-018-9697-6.Google Scholar
Ritchie, M.G. (1996) The shape of female mating preferences. Proceedings of the National Academy of Sciences of the United States of America 93, 1462814631.Google Scholar
Ritchie, M.G. (2007) Sexual selection and speciation. Annual Review of Ecology, Evolution, and Systematics 38, 79102.Google Scholar
Roriz, A.K.P., Japyassú, H.F. & Joachim-Bravo, I.S. (2017) Incipient speciation in the Anastrepha fraterculus (Diptera: Tephritidae) cryptic complex: reproductive compatibility between A.sp.1 aff. fraterculus and A.sp.3 aff. fraterculus. Entomologia Experimentalis et Applicata 162, 346357.Google Scholar
Rull, J., Abraham, S., Kovaleski, A., Segura, D.F., Islam, A., Wornoayporn, V., Dammalage, T., Tomas, U.S. & Vera, M.T. (2012) Random mating and reproductive compatibility among Argentinean and southern Brazilian populations of Anastrepha fraterculus (Diptera: Tephritidae). Bulletin of Entomological Research 102, 435443.Google Scholar
Rull, J., Abraham, S., Kovaleski, A., Segura, D.F., Mendoza, M., Liendo, M.C. & Vera, M.T. (2013) Evolution of pre-zygotic and post-zygotic barriers to gene flow among three cryptic species within the Anastrepha fraterculus complex. Entomologia Experimentalis et Applicata 148, 213222.Google Scholar
Ryan, M.J. & Rand, A.S. (1993) Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47, 647657.Google Scholar
Segura, D.F., Vera, M.T., Rull, J., Wornoayporn, V.T., Islam, A. & Robinson, A.S. (2011) Assortative mating among Anastrepha fraterculus (Diptera: Tephritidae) hybrids as a possible route to radiation of the fraterculus cryptic species complex. Biological Journal of the Linnean Society 102, 346354.Google Scholar
Selivon, D. & Perondini, A.L.P. (1998) Eggshell morphology in two cryptic species of the Anastrepha fraterculus complex (Diptera: Tephritidae). Annals of Entomological Society of America 91, 473478.Google Scholar
Selivon, D., Perondini, A.L.P. & Morgante, J.S. (1999) Haldane's rule and other aspects of reproductive isolation observed in the Anastrepha fraterculus complex (Diptera: Tephritidae). Genetics and Molecular Biology 22(4), 507510.Google Scholar
Selivon, D., Vretos, C., Fontes, L. & Perondini, A.L.P. (2004) New variant forms in the Anastrepha fraterculus complex (Diptera: Tephritidae) p. 253–258 in Brian Barnes. (Org.) Proceedings of 6th International Fruit Fly Symposium. Irene: Isteg Scientific Publications.Google Scholar
Selivon, D., Perondini, P. & Morgante, J.S. (2005) A genetic-morphological characterization of two cryptic species of the Anastrepha fraterculus complex (Diptera: Tephritidae). Annals of Entomological Society of America 98, 367381.Google Scholar
Steck, G.J. (1991) Biochemical systematics and population genetic-structure of Anastrepha fraterculus and related species (Diptera, tephritidae). Annals of Entomological Society of America 84, 1028.Google Scholar
Stone, A. (1942) The fruit flies of the genus Anastrepha. U.S. Dep. Agric. Misc.Google Scholar
Vaníčková, L., Svatoš, A., Kroiss, J., Kaltenpoth, M., do Rufino, R.N., Hoskovec, M., Břízová, R. & Kalinová, B. (2012) Cuticular hydrocarbons of the South American fruit fly Anastrepha fraterculus: variability with sex and age. Journal of Chemical Ecology 38, 11331142.Google Scholar
Vaníčková, L., Virgilio, M., Tomčala, A., Břízová, R., Ekesi, S., Hoskovec, M., Kalinová, B., Do Nascimento, R.R. & De Meyer, M. (2014) Resolution of three cryptic agricultural pests (Ceratitis fasciventris, C. anonae, C. rosa, Diptera: Tephritidae) using cuticular hydrocarbon profiling. Bulletin of Entomological Research 104, 631638.Google Scholar
Vaníčková, L., Hernández-Ortiz, V., Joachim-Bravo, I.S., Dias, V., Roriz, A.K.P., Laumann, R.A., Mendonça, A.L., Paranhos, B.A.J. & do Nascimento, R.R. (2015 a). Current knowledge of the species complex Anastrepha fraterculus (Diptera, Tephritidae) in Brazil. ZooKeys 540, 211237.Google Scholar
Vaníčková, L., Břízová, R., Pompeiano, A., Ferreira, L.L., de Aquino, N.C., Tavares, R.F., Rodriguez, L.D., Mendonça, A.L., Canal, N.A. & do Nascimento, R.R. (2015 b) Characterisation of the chemical profiles of Brazilian and Andean morphotypes belonging to the Anastrepha fraterculus complex (Diptera, Tephritidae). ZooKeys 540, 193209.Google Scholar
Vaníčková, L., Břízová, R., Mendonça, A.L., Pompeiano, A. & do Nascimento, R.R. (2015 c) Intraspecific variation of cuticular hydrocarbon profiles in the Anastrepha fraterculus (Diptera: Tephritidae) species complex. Journal of Applied Entomology 139, 679689.Google Scholar
Vera, M.T., Cáceres, C., Wornoayporn, V., Islam, A., Robinson, A.S., De La Veja, M.H., Hendrichs, J. & Cayol, J.P. (2006) Mating incompatibility among populations of the South American fruit fly Anastrepha fraterculus (Diptera: Tephritidae). Annals of the Entomological Society of America 99, 387397.Google Scholar
Wu, C.-I., Hollocher, H., Begun, D.J., Aquadro, C.F., Xu, Y. & Wu, M.-L. (1995). Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation. Proceedings of the National Academy of Sciences USA 92, 25192523.Google Scholar
Yamada, H., Tomaru, M., Matsuda, M. & Oguma, Y. (2008) Behavioral sequence leading to sexual isolation between Drosophila ananassae and D. pallidosa. Journal of Insect Behavior 21, 222239.Google Scholar
Zucchi, RA (2016) Fruit flies in Brazil – Anastrepha species their host plants and parasitoids. Available online at http://www.lea.esalq.usp.br/anastrepha (accessed 13 August 13 2018).Google Scholar
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