Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-24T11:14:09.364Z Has data issue: false hasContentIssue false

The effect of winter length on survival and duration of dormancy of four sympatric species of Rhagoletis exploiting plants with different fruiting phenology

Published online by Cambridge University Press:  21 September 2016

J. Rull*
Affiliation:
PROIMI Biotecnología-CONICET, LIEMEN-División Control Biológico de Plagas, Av. Belgrano y Pje. Caseros, T4001MVB San Miguel de Tucumán, Tucumán, Argentina
E. Tadeo
Affiliation:
Red de Manejo Biorracional de Plagas y Vectores, Instituto de Ecología, A.C., Xalapa, Veracruz 91070, México
R. Lasa
Affiliation:
Red de Manejo Biorracional de Plagas y Vectores, Instituto de Ecología, A.C., Xalapa, Veracruz 91070, México
M. Aluja
Affiliation:
Red de Manejo Biorracional de Plagas y Vectores, Instituto de Ecología, A.C., Xalapa, Veracruz 91070, México
*
*Author for correspondence Phone: +54 381 - 434 4888 Fax: +54 381 - 434 4887 E-mail: pomonella@gmail.com

Abstract

Dormancy has been thoroughly studied for several species of economic importance in the genus Rhagoletis in temperate areas of North America and Europe. Much less is known on life history regulation for species inhabiting high-elevation areas in the subtropics at the southern extreme of their geographical range. Host plant phenology has been found to play a key role in generating allochronic isolation among sibling species and host races of Rhagoletis in the course of sympatric speciation, and has important implications for pest management. We compare the effect of winter length on survival to adult eclosion and dormancy duration among four species of Rhagoletis (three of them sympatric) exploiting hosts with different fruiting phenology in subtropical isolated highlands. Survival and duration of dormancy was found to be different among the four species. At 24°C, a very small proportion (<1%) of R. pomonella, R. turpiniae and R. zoqui completed development without becoming dormant, while in the case of R. solanophaga the majority of the population emerged after development within 40 days of pupation. Also, a large proportion of braconid parasitoids infesting Rhagoletis eggs and larvae emerged as adults without becoming dormant. Greatest survival after artificial winter was obtained for R. pomonella (50–60%) and R. zoqui (30%) after only four weeks at 5°C (a third of the time reported for studies on northern R. pomonella), while R. turpiniae, under identical environmental conditions experienced low adult emergence, and highest survival (11%) was recorded for flies exposed to 5°C during 10 and 12 weeks. For R. pomonella, there was a strong positive relationship between winter length and time to post-winter adult eclosion that was not observed for R. zoqui. In sum, for R. pomonella, mild winters in highland subtropical areas appear to select for flies better able to withstand longer periods of warm temperature before winter than flies exploiting late fruiting hosts and inhabiting northern latitudes. In the case of R. turpiniae and R. zoqui environmental cues such as fluctuations in humidity and/or different temperature thresholds (5°C) may play a more important role than winter length in life history regulation. Continuous host availability for R. solanophaga appears to have selected for non-diapausing flies. From an applied perspective our results are useful for handling flies in the laboratory to conduct research and suggest that non-diapausing strains of flies and parasitoids may be selected for SIT and innundative biological control programs.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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

Baker, C.R.B. & Miller, G.W. (1978) The effect of temperature on the post-diapause development of four geographical populations of the European fruit fly (Rhagoletis cerasi). Entomologia Experimentalis et Applicata 23, 113.Google Scholar
Berlocher, S.H. (2000) Radiation and divergence in the Rhagoletis pomonella species group: inferences from allozymes. Evolution 54, 543557.Google Scholar
Boller, E.F. & Prokopy, R.J. (1976) Bionomics and management of Rhagoletis . Annual Review of Entomology 21, 223246.Google Scholar
Boller, E.F., Haisch, A. & Prokopy, R.J. (1971) Sterile principles for insect control or eradication. p. 77 in Self, L.A. (Ed.) Sterile Insect Release Method Against Rhagoletis Cerasi L.: Preparatory Ecological and Behavioural Studies. Vienna, IAEA.Google Scholar
Danks, H.V. (1987) Insect Dormancy: An Ecological Perspective. Ottawa, Canada, Biological Survey of Canada (Terrestrial Arthropods).Google Scholar
Danks, H.V. (2002) The range of insect dormancy responses. European Journal of Entomology 99, 127142.Google Scholar
Danks, H.V. (2006) Insect adaptations to cold and changing environments. The Canadian Entomologist 138, 123.Google Scholar
Chen, Y.H., Opp, S.B., Berlocher, S.H. & Roderick, G.K. (2006) Are bottlenecks associated with colonization? Genetic diversity and diapause variation of native and introduced Rhagoletis completa populations. Oecologia 149, 656667.Google ScholarPubMed
Comisión Nacional del Agua (2015) Available online at http://smn.cna.gob.mx/index.php?option=com_content&view=article&id=164:veracruz&catid=14&Itemid=2 (acceded 15 October 2015).Google Scholar
Dambroski, H.R. & Feder, J.L. (2007) Host plant and latitude-related diapause variation in Rhagoletis pomonella: a test for multifaceted life history adaptation on different stages of diapause development. Journal of Evolutionary Biology 20, 21012112.Google Scholar
Egan, S.P., Ragland, G.J., Assour, L., Powell, T.H.Q., Hood, G.R., Emrich, S., Nosil, P. & Feder, J.L. (2015) Experimental evidence of genome-wide impact of ecological selection during early stages of speciation-with-gene-flow. Ecology Letters 18, 817825.Google Scholar
Feder, J.L. & Filchak, K.E. (1999) It's about time: the evidence for host plant-mediated selection in the apple maggot fly, Rhagoletis pomonella, and its implications for fitness trade-offs in phytophagous insects. pp. 211225 in Proceedings of the 10th International Symposium on Insect-Plant Relationships, Netherlands, Springer.Google Scholar
Feder, J.L., Hunt, T.A. & Bush, G.L. (1993) The effects of climate, host plant phenology and host fidelity on the genetics of apple and hawthorn infesting races of Rhagoletis pomonella . Entomologia Experimentalis et Applicata 69, 117135.Google Scholar
Feder, J.L., Stolz, U., Lewis, K.M., Perry, W., Roethele, J.B. & Rogers, A. (1997) The effects of winter length on the genetics of apple and hawthorn races of Rhagoletis pomonella (Diptera: Tephritidae). Evolution 51, 18621876.Google Scholar
Feder, J.L., Berlocher, S.H., Roethele, J.B., Dambroski, H., Smith, J.J., Perry, W.L., Garvrilovic, V., Filchak, K.E., Rull, J. & Aluja, M. (2003 a) Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis . Proceedings of the National Academy of Sciences 100, 1031410319.Google Scholar
Feder, J.L., Roethele, J.B., Filchak, K., Niedbalski, J. & Romero-Severson, J. (2003 b) Evidence for inversion polymorphism related to sympatric host race formation in the apple maggot fly, Rhagoletis pomonella . Genetics 163, 939953.Google ScholarPubMed
Feder, J.L., Xie, X., Rull, J., Velez, S., Forbes, A., Leung, B., Dambroski, H., Filchak, K.E. & Aluja, M. (2005) Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis . Proceedings of the National Academy of Sciences of the United States of America 102, 65736580.Google Scholar
Feder, J.L., Powell, T.H., Filchak, K. & Leung, B. (2010) The diapause response of Rhagoletis pomonella to varying environmental conditions and its significance for geographic and host plant-related adaptation. Entomologia Experimentalis et Applicata 136, 3144.Google Scholar
Filchak, K.E., Roethele, J.B. & Feder, J.L. (2000) Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella . Nature 407, 739742.Google Scholar
Frías, D. (1986) Biología poblacional de Rhagoletis nova (Schiner). Biología 13, 7584.Google Scholar
Frías, D., Capetillo, J. & Leppe, I.N. (1991) Aspectos de la biología de” Rhagoletis tomatis” Foote (Diptera. Tephritidae) en poblaciones de la II Región de Chile. Acta Entomológica chilena 16, 193199.Google Scholar
Haisch, A. & Boller, E.F. (1971) Genetic control of the European cherry fruit fly, Rhagoletis cerasi L. Progress report on rearing and sterilization. p. 67 in Self, L.A. (Ed.), Sterility Principle for Insect Control or Eradication: Proceedings of a Symposium Jointly Organized by the IAEA and FAO, Athens, 14–18 Sept. 1970. International Atomic Energy Agency.Google Scholar
Hernández-Ortiz, V. & Frias, D. (1999) A revision of the striatella species group of the genus Rhagoletis (Diptera: Tephritidae). Insecta Mundi 13, 1120.Google Scholar
Kasana, A. & AliNiazee, M.T. (1994) Effect of constant temperatures on development of the walnut husk fly, Rhagoletis completa . Entomologia Experimentalis et Applicata, 73, 247254.Google Scholar
Köppler, K., Kaffer, T. & Vogt, H. (2009) Substantial progress made in the rearing of the European cherry fruit fly, Rhagoletis cerasi . Entomologia Experimentalis et Applicata 132, 283288.Google Scholar
Koštál, V. (2006) Eco-physiological phases of insect diapause. Journal of Insect Physiology 52, 113127.Google Scholar
Lyons-Sobaski, S. & Berlocher, S.H. (2009) Life history phenology differences between southern and northern populations of the apple maggot fly, Rhagoletis pomonella . Entomologia Experimentalis et Applicata 130, 149159.Google Scholar
Menu, F. & Desouhant, E. (2002) Bet-hedging for variability in life cycle duration: bigger and later-emerging chestnut weevils have increased probability of a prolonged diapause. Oecologia 132, 167174.Google Scholar
Moral, Y.M.A.D., Peña, A.H.D.L., Dzul-Cauich, J.F. & Hernández-Ortiz, V. (2015) Fluctuación poblacional de adultos de Rhagoletis zoqui en nogal de Castilla (Juglans regia L.) en Puebla, México. Southwestern Entomologist 40, 409418.Google Scholar
Moraiti, C.A., Nakas, C.T. & Papadopoulos, N.T. (2012) Prolonged pupal dormancy is associated with significant fitness cost for adults of Rhagoletis cerasi (Diptera: Tephritidae). Journal of Insect Physiology 58, 11281135.Google Scholar
Michel, A.P., Rull, J., Aluja, M. & Feder, J.L. (2007) The genetic structure of hawthorn-infesting Rhagoletis pomonella populations in Mexico: implications for sympatric host race formation. Molecular Ecology 16, 28672878.Google Scholar
Ovruski, S.M., Wharton, R.A., Rull, J. & Guillén, L. (2007) Aganaspis alujai (Hymenoptera: Figitidae: Eucoilinae), a new species attacking Rhagoletis (Diptera: Tephritidae) in the neotropical region. Florida Entomologist 90, 626634.Google Scholar
Phipps, J.B. (1997) Monograph of northern Mexican Crataegus (Rosaceae, subfam. Maloideae). SIDA, Botanical Miscellany No 15.Google Scholar
Powell, T.H., Forbes, A.A., Hood, G.R. & Feder, J.L. (2014) Ecological adaptation and reproductive isolation in sympatry: genetic and phenotypic evidence for native host races of Rhagoletis pomonella . Molecular Ecology 23, 688704.Google Scholar
Prokopy, R.J. (1968) The influence of photoperiod, temperature and food on the initiation of diapause in the apple maggot. Canadian Entomologist 100, 318329.Google Scholar
Prokopy, R.J. & Papaj, D.R. (2000) Behavior of flies of the genera Rhagoletis, Zonosemata, and Carpomya (Trypetinae: Carpomyina). pp. 219252 in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, CRC Press.Google Scholar
Rull, J., Aluja, M. & Feder, J.L. (2010) Evolution of intrinsic reproductive isolation among four North American populations of Rhagoletis pomonella (Diptera: Tephritidae). Biological Journal of the Linnean Society 100, 213233.Google Scholar
Rull, J., Aluja, M. & Feder, J.L. (2011) Distribution and basic biology of black cherry-infesting Rhagoletis (Diptera: Tephritidae) in México. Annals of the Entomological Society of America 104(2), 202211.Google Scholar
Rull, J., Aluja, M., Feder, J.L. & Berlocher, S.H. (2006) The distribution and host range of hawthorn-infesting Rhagoletis (Diptera: Tephritidae) in Mexico. Annals of the Entomological Society of America 99, 662672.Google Scholar
Rull, J., Aluje, M., Tadeo, E., Guillen, L., Scott, E., Glover, M. & Feder, J.L. (2013) Distribution, host plant affiliation, phenology, and phylogeny of walnut-infesring Rhagoletis flies (Diptera: Tephritidae) in Mexico. Biological Journal of the Linnean Society 110, 765779.Google Scholar
Rull, J., Wharton, R.A., Feder, J.L., Guillen, L., Sivinski, J., Forbes, A. & Aluja, M. (2009) Latitudinal variation in guild composition and parasitism rates of North American, hawthorn infesting Rhagoletis. Environmental Entomology 38, 588599.Google Scholar
Sinclair, B.J., Vernon, P., Klok, C.J. & Chown, S.L. (2003) Insects at low temperatures: an ecological perspective. Trends in Ecology & Evolution 18, 257262.Google Scholar
Smith, D.C. (1988) Heritable divergence of Rhagoletis pomonella host races by seasonal asynchrony. Nature 336, 6667.Google Scholar
Smith, J.J. & Bush, G.L. (1999) Phylogeny of the subtribe Carpomyina (Trypetinae), emphasizing relationships of the genus Rhagoletis. pp. 187217 in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, CRC Press.Google Scholar
Stone, D.E., Oh, S.H., Tripp, E.A., Ríos, L.E.G. & Manos, P.S. (2009) Natural history, distribution, phylogenetic relationships, and conservation of Central American black walnuts (Juglans sect. Rhysocaryon). Journal of the Torrey Botanical Society 136, 125.Google Scholar
Tadeo, E., Feder, J.L., Egan, S., Schuler, H., Aluja, M. & Rull, J. (2015) Divergence and evolution of reproductive barriers among three allopatric populations of Rhagoletis cingulatea across eastern North America and México. Entomología Experimentalis et Applicata 156, 301311.Google Scholar
Tauber, M.J., Tauber, C.A. & Masaki, S. (1986) Seasonal Adaptations of Insects. New York, USA, Oxford University Press.Google Scholar
Teixeira, L.A. & Polavarapu, S. (2005 a) Diapause development in the blueberry maggot Rhagoletis mendax (Diptera: Tephritidae). Environmental Entomology 34, 4753.Google Scholar
Teixeira, L.A. & Polavarapu, S. (2005 b) Evidence of a heat-induced quiescence during pupal development in Rhagoletis mendax (Diptera: Tephritidae). Environmental Entomology 34, 292297.Google Scholar
Vankirk, J.R. & AliNiazee, M.T. (1982) Diapause development in the western cherry fruit fly, Rhagoletis indifferens Curran (Diptera, Tephritidae). Zeitschrift für Angewandte Entomologie 93, 440445.Google Scholar
Xie, Q., Hou, B. & Zhang, R. (2008) Thermal responses of oriental fruit fly (Diptera: Tephritidae) late third instars: mortality, puparial morphology, and adult emergence. Journal of Economic Entomology 101(3), 736–41.Google Scholar
Yee, W.L., Nash, M.J., Goughnour, R.B., Cha, D.H., Linn, C.E. & Feder, J.L. (2014) Ammonium carbonate is more attractive than apple and hawthorn fruit volatile lures to Rhagoletis pomonella (Diptera: Tephritidae) in Washington state. Environmental Entomology 43(4), 957968.Google Scholar