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Phenotypic plasticity in clutch size regulation among populations of a potential invasive fruit fly from environments that vary in host heterogeneity and isolation

Published online by Cambridge University Press:  21 May 2018

M. Aluja ,
A. Birke ,
F. Díaz-Fleischer  and
J. Rull
M. Aluja*
Affiliation:
Instituto de Ecología, A.C., Apartado Postal 63, 91000 Xalapa, Veracruz, Mexico
A. Birke
Affiliation:
Instituto de Ecología, A.C., Apartado Postal 63, 91000 Xalapa, Veracruz, Mexico
F. Díaz-Fleischer
Affiliation:
INBIOTECA, Universidad Veracruzana, 91000 Xalapa, Veracruz, Mexico
J. Rull
Affiliation:
PROIMI Biotecnología-CONICET, LIEMEN-División Control Biológico de Plagas, Av. Belgrano y Pje. Caseros, T4001MVB San Miguel de Tucumán, Tucumán, Argentina
*
*Author for correspondence Phone: +52-228-8421841 E-mail: [email protected]
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Abstract

Phenotypic plasticity is thought to evolve in response to environmental unpredictability and can shield genotypes from selection. However, selection can also act on plastic traits. Egg-laying behaviour, including clutch size regulation, is a plastic behavioural trait among tephritid fruit flies. We compared plasticity in clutch size regulation among females of Anastrepha ludens populations stemming from environments that differed in the degree of predictability in egg-laying opportunities. Clutch size regulation in response to hosts of different sizes was compared among flies from (a) a wild, highly isolated population, (b) a wild population that switches seasonally from a small wild host fruit that varies greatly in abundance to an abundant large-sized commercial host, and (c) a laboratory population. Flies from all three populations adjusted clutch number and size according to host size. However, flies from the heterogeneous wild environment were more plastic in adjusting clutch size than flies from agricultural settings that also laid fewer eggs; yet both populations were more plastic in adjusting clutch size in line with host size when compared with laboratory females. When wild and orchard females encountered the largest host, clutch size was extremely variable and egg regulation did not follow the same trend. Heterogeneity in host availability in space and time appears to be as important as seasonal variation in host size in maintaining plastic clutch size regulation behaviour. In stable environments, there was a clear reduction in the plasticity of these traits.

Keywords

invasive speciesbehavioural plasticityenvironmental variabilityclutch size regulation
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 2 , April 2019 , pp. 169 - 177
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Copyright
Copyright © Cambridge University Press 2018 

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References

Aluja, M. (1994). Bionomics and management of Anastrepha. Annual Review of Entomology 39, 155–178.10.1146/annurev.en.39.010194.001103Google Scholar
Aluja, M., Piñero, J., Jácome, I., Díaz-Fleischer, F. & Sivinski, J. (2000). Behavior of flies in the genus Anastrepha (Trypetinae: Toxotrypanini). pp. 375–408 in Aluja, M. & Norrbom, A.L. (Eds) Fruit flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, CRC Press.Google Scholar
Aluja, M., Díaz-Fleischer, F., Papaj, D.R., Lagunes, G. & Sivinski, J. (2001). Effects of age, diet, female density and host resource on egg-load in Anastrepha ludens and A. obliqua (Diptera: Tephiritidae). Journal of Insect Physiology 47, 975–988.Google Scholar
Aluja, M., Rull, J., Pérez-Staples, D., Díaz-Fleischer, F. & Sivinski, J. (2009). Random mating among Anastrepha ludens (Diptera: Tephritidae) adults of geographically distant and ecologically distinct populations in Mexico. Bulletin of Entomological Research 99, 207–214.10.1017/S0007485308006299Google Scholar
Aluja, M., Birke, A., Guillén, L., Díaz-Fleischer, F. & Nestel, D. (2011 a). Coping with an unpredictable and stressful environment: the life history and metabolic response to variable food and host availability in a polyphagous tephritid fly. Journal of Insect Physiology 57, 1592–1601.Google Scholar
Aluja, M., Guillén, L., Rull, J., Höhn, H., Frey, J., Graf, B. & Samietz, J. (2011 b). Is the Alpine divide becoming more permeable to biological invasions as a result of global warming? Insights on the invasion and establishment of the walnut husk fly, Rhagoletis completa (Diptera: Tephritidae) in Switzerland. Bulletin of Entomological Research 101, 451–465.10.1017/S0007485311000010Google Scholar
Aluja, M., Birke, A., Ceymann, M., Guillén, L., Arrigoni, E., Baumgartner, D., Pascacio-Villafán, C. & Samietz, J. (2014). Agroecosystems resilience to an invasive insect species that could expand its geographical range in response to global climate change. Agriculture, Ecosystem & Environment 186, 54–63.Google Scholar
Auld, J.R., Agrawal, A.A. & Relyea, R.A. (2010). Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proceedings of the Royal Society B: Biological Sciences 277, 503–511.Google Scholar
Baayen, R.H., Davidson, D.J. & Bates, D.M. (2008). Mixed-effects modeling with crossed random effects for subjects and items. Journal of Memory and Language 59, 390–412.10.1016/j.jml.2007.12.005Google Scholar
Badyaev, A. (2005). Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proceedings of the Royal Society B: Biological Sciences 272, 877–886.Google Scholar
Bates, D., Maechler, M. & Bolker, B. (2011). Lme4: Linear Mixed-Effects Models Using S4 Classes. R Package Version 0.999375-42. Available online at http://CRAN.R-project.org/package=lme4 (accessed 20 November 2016).Google Scholar
Birke, A., Guillén, L., Midgarden, D. & Aluja, M. (2013). Fruit flies, Anastrepha ludens (Loew), A. obliqua (Macquart) and A. grandis (Macquart) (Diptera: Tephritidae): three pestiferous tropical fruit flies that could potentially expand their range to temperate areas. pp. 192–213 in Peña, J. (Ed.) Potential Invasive Pests of Agricultural Crops. FL, CABI International.Google Scholar
Carroll, S.P., Dingle, H. & Klassen, S.P. (1997). Genetic differentiation of fitness-associated traits among rapidly evolving populations of the soapberry bug. Evolution 51, 1182–1188.Google Scholar
Carroll, S.P., Klassen, S.T.P. & Dingle, H. (1998). Rapidly evolving adaptations to host ecology and nutrition in the soapberry bug. Evolutionary Ecology 12, 955–968.10.1023/A:1006568206413Google Scholar
Charmantier, A., McCleery, R.H., Cole, L.R., Perrins, C., Loeske, E.B., Kruuk, B.C. & Sheldon, B.C. (2008). Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800–803.10.1126/science.1157174Google Scholar
Chown, S.L., Slabber, S., McGeoch, M.A., Janion, C. & Leinaas, H.P. (2007). Phenotypic plasticity mediates climate change responses among invasive and indigenous arthropods. Proceedings of the Royal Society B: Biological Sciences 274, 2531–2537.Google Scholar
Davidson, A.M., Jennions, M. & Nicotra, A.B. (2011). Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecology Letters 14, 419–431.Google Scholar
Davies, G.M. & Gray, A. (2015). Don't let spurious accusations of pseudoreplication limit our ability to learn from natural experiments (and other messy kinds of ecological monitoring). Ecology & Evolution 5, 5295–5304.10.1002/ece3.1782Google Scholar
Díaz-Fleischer, F. & Aluja, M. (2003 a). Behavioural plasticity in relation to egg and time limitation: the case of two fly species in the genus Anastrepha (Diptera: Tephritidae). Oikos 100, 125–133.Google Scholar
Díaz-Fleischer, F. & Aluja, M. (2003 b). Influence of conspecific presence, experience, and host quality on oviposition behavior and clutch size determination in Anastrepha ludens (Diptera: Tephritidae). Journal of Insect Behavior 16, 537–554.Google Scholar
Díaz-Fleischer, F., Papaj, D.R., Prokopy, R.J., Norrbom, A.L. & Aluja, M. (2000). Evolution of fruit fly oviposition behavior. pp. 811–842 in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behaviour. Boca Raton, FL, CRC Press.Google Scholar
Duyck, P.F., David, P. & Quilici, S. (2004). A review of relationships between interspecific competition and invasions in fruit flies (Diptera: Tephritidae). Ecological Entomology 29, 511–520.10.1111/j.0307-6946.2004.00638.xGoogle Scholar
Eggers, S., Griesser, M., Nystrand, M. & Ekman, J. (2006). Predation risk induces changes in nest-site selection and clutch size in the Siberian jay. Proceedings of the Royal Society B: Biological Sciences 273, 701–706.Google Scholar
Ernande, B. & Dieckmann, U. (2004). The evolution of phenotypic plasticity in spatially structured environments: implications of intraspecific competition, plasticity costs and environmental characteristics. Journal of Evolutionary Biology 17, 613–628.Google Scholar
Flatt, T. (2005). The evolutionary genetics of canalization. The Quarterly Review of Biology 80, 287–316.10.1086/432265Google Scholar
Fordyce, J.A. (2005). Clutch size plasticity in the Lepidoptera. pp. 125–144 in Ananthakrishnan, T.N. & Whitman, D.W. (Eds) Insects and Phenotypic Plasticity. Enfield, NH, Science Publishers Inc.Google Scholar
Fox, C.W. & Czesak, M.E. (2000). Evolutionary ecology of progeny size in arthropods. Annual Review of Entomology 45, 341–369.10.1146/annurev.ento.45.1.341Google Scholar
Frey, J., Guillén, L., Frey, B., Samietz, J., Rull, J. & Aluja, M. (2013). Developing diagnostic SNP panels for the identification of true fruit flies (Diptera: Tephritidae) within the limits of COI-based species delimitation. BMC Evolutionary Biology 13, 106.Google Scholar
Ghalambor, C.K., McKay, J.K., Carroll, S.P. & Reznick, D.N. (2007). Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21, 394–407.10.1111/j.1365-2435.2007.01283.xGoogle Scholar
Gilchrist, A.S., Cameron, E.C., Sved, J.A. & Meats, A.W. (2012). Genetic consequences of domestication and mass rearing of pest fruit fly Bactrocera tryoni (Diptera: Tephritidae). Journal of Economic Entomology 105, 1051–1056.10.1603/EC11421Google Scholar
Jácome, I., Aluja, M. & Liedo, P. (1999). Impact of adult diet on demographic and population parameters of the tropical fruit fly Anastrepha serpentina (Diptera: Tephritidae). Bulletin of Entomological Research 89, 165–175.Google Scholar
Jordan, M.A. & Snell, H.L. (2002). Life history trade-offs and phenotypic plasticity in the reproduction of Galapagos lava lizards (Microlophus delanonis). Oecologia 130, 44–52.10.1007/s004420100776Google Scholar
Karsten, M., van Vuuren, B.J., Barnaud, A. & Terblanche, J.S. (2013). Population genetics of Ceratitis capitata in South Africa: implications for dispersal and pest management. PLoS ONE 8, e54281.Google Scholar
Lee, C.E. (2002). Evolutionary genetics of invasive plants. Trends in Ecology & Evolution 17, 386–391.10.1016/S0169-5347(02)02554-5Google Scholar
Malacrida, A.R., Guglielmino, C.R., D’ Adamo, P., Torti, C., Marinoni, F. & Gasperi, G. (1996). Allozyme divergence and phylogenetic relationships among species of tephritid flies. Heredity 76, 592–602.Google Scholar
Norrbom, A.L. (2003). Host Plant Data Base for Anastrepha and Toxotrypana (Diptera: Tephritidae: Toxotrypanini). Diptera data dissemination disk. Washington, DC, CD-ROM, North Amer. Dipterist's Soc.Google Scholar
Oroño, L., Paulin, A.C., Alberti, A.C., Hilal, M., Ovruski, S., Vilardi, J.C., Rull, J. & Aluja, M. (2013). Effect of host plant chemistry on genetic differentiation and reduction of gene flow among Anastrepha fraterculus (Diptera: Tephritidae) populations exploiting sympatric, synchronic hosts. Environmental Entomology 42, 790–798.Google Scholar
Papadopoulos, N.T., Plant, R.E. & Carey, J.R. (2013). From trickle to flood: the large-scale, cryptic invasion of California by tropical fruit flies. Proceedings of the Royal Society B: Biological Sciences 280, 1466–1476.Google Scholar
Parsons, K.J. & Robinson, B.W. (2006). Replicated evolution of integrated plastic responses during early adaptive divergence. Evolution 60, 801–813.Google Scholar
Pecina-Quintero, J., López-Arroyo, I., Loera Gallardo, J., Pons, J.L., Hernández, N., Mayek Pérez, S., Hernández Delgado, S., Rull, J. & Aluja, M. (2009). Genetic differences between Anastrepha ludens (Diptera: Tephritidae) populations stemming from a native and an exotic host in NE Mexico. Agricultura Técnica 35, 320–328.Google Scholar
Pimentel, D., Zuniga, R. & Morrison, D. (2005). Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52, 273–288.Google Scholar
R Core Team (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.R-project.org/Google Scholar
Plummer, C.C., McPhail, M. & Monk, J.W. (1941) The yellow chapote: a native host of the Mexican fruit fly. United States Department of Agriculture Technical Bulletin 755, 1–12.Google Scholar
Relyea, R.A. (2001). Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82, 523–540.Google Scholar
Richards, C.L., Bossdorf, O., Muth, N.Z., Gurevitch, J. & Pigliucci, M. (2006). Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters 9, 981–993.Google Scholar
Schliserman, P., Aluja, M., Rull, J. & Ovruski, S. (2014). Habitat degradation and introduction of exotic plants favor persistence of invasive species and population growth of native polyphagous fruit fly pests in a Northwestern Argentinean mosaic. Biological Invasions 16, 2599–2613.Google Scholar
Schutze, M., Krosch, M., Armstrong, K., Chapman, T., Englezou, A., Chomič, A. & Clarke, A. (2012). Population structure of Bactrocera dorsalis s.s., B. papayae and B. philippinensis (Diptera: Tephritidae) in Southeast Asia: evidence for a single species hypothesis using mitochondrial DNA and wing-shape data. BMC Evolutionary Biology 12, 130.Google Scholar
Thomas, D.B. (2003). Reproductive phenology of the Mexican fruit fly Anastrepha ludens (Loew) (Diptera: Tephritidae) in the Sierra Madre Oriental, Northern Mexico. Neotropical Entomology 32, 385–397.Google Scholar
Thomas, D.B. & Loera-Gallardo, J. (1998). Dispersal and longevity of mass-released, sterilized Mexican fruit flies (Diptera: Tephritidae). Environmental Entomology 27, 1045–1052.Google Scholar
Van Buskirk, J. & Relyea, R.A. (1998). Natural selection for phenotypic plasticity: predator-induced morphological responses in tadpoles. Biological Journal of Linnean Society 65, 301–328.Google Scholar
Xu, L., Zhou, C., Xiao, Y., Zhang, P., Tang, Y. & Xu, Y.I.J.U.A.N. (2012). Insect oviposition plasticity in response to host availability: the case of the tephritid fruit fly Bactrocera dorsalis. Ecological Entomology 37, 446–452.Google Scholar