Introduced Drosophila subobscura populations perform better than native populations during an oviposition choice task due to increased fecundity but similar learning ability

Abstract

The success of invasive species is tightly linked to their fitness in a putatively novel environment. While quantitative components of fitness have been studied extensively in the context of invasive species, fewer studies have looked at qualitative components of fitness, such as behavioral plasticity, and their interaction with quantitative components, despite intuitive benefits over the course of an invasion. In particular, learning is a form of behavioral plasticity that makes it possible to finely tune behavior according to environmental conditions. Learning can be crucial for survival and reproduction of introduced organisms in novel areas, for example, for detecting new predators, or finding mates or oviposition sites. Here we explored how oviposition performance evolved in relation to both fecundity and learning during an invasion, using native and introduced Drosophila subobscura populations performing an ecologically relevant task. Our results indicated that, under comparable conditions, invasive populations performed better during our oviposition task than did native populations. This was because invasive populations had higher fecundity, together with similar cognitive performance when compared to native populations, and that there was no interaction between learning and fecundity. Unexpectedly, our study did not reveal an allocation trade-off (i.e., a negative relationship) between learning and fecundity. On the contrary, the pattern we observed was more consistent with an acquisition trade-off, meaning that fecundity could be limited by availability of resources, unlike cognitive ability. This pattern might be the consequence of escaping natural enemies and/or competitors during the introduction. The apparent lack of evolution of learning may indicate that the introduced population did not face novel cognitive challenges in the new environment (i.e., cognitive “pre-adaptation”). Alternatively, the evolution of learning may have been transient and therefore not detected.

References Alexander, J. M., P. J. Edwards, M. Poll, C. G. Parks, and H. Dietz. 2009. Establishment of parallel altitudinal clines in traits of native and introduced forbs. Ecology 90:612–622. Amiel, J. J., R. Tingley, and R. Shine. 2011. Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles. PLoS One 6:e18277. Balanya, J., C. Segarra, A. Prevosti, and L. Serra. 1994. Colonization of America by Drosophila subobscura: the founder event and a rapid expansion. J. Hered. 85:427–432. Barker, J. S. F., J. Frydenberg, J. Gonzalez, H. I. Davies, A. Ruiz, J. G. Sorensen, et al. 2009. Bottlenecks, population differentiation and apparent selection at microsatellite loci in Australian Drosophila buzzatii. Heredity 102:389–401. Bates, D., M. Maechler, B. Bolker, and S. Walker. 2014. lme4: linear mixed-effects models using Eigen and S4 [Internet]. Available at: http://CRAN.R-project.org/package=lme4 Battesti, M., C. Moreno, D. Joly, and F. Mery. 2012. Spread of social information and dynamics of social transmission within Drosophila groups. Curr. Biol. 22:309–313. Bezzina, C. N., J. J. Amiel, and R. Shine. 2014. Does invasion success reflect superior cognitive ability? A case study of two congeneric lizard species (Lampropholis, Scincidae). PLoS One 9:e86271. Blackburn, T. M., P. Pysek, S. Bacher, J. T. Carlton, R. P. Duncan, V. Jarosik, et al. 2011. A proposed unified framework for biological invasions. Trends Ecol. Evol. 26:333–339. Blossey, B., and R. Notzold. 1995. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J. Ecol. 83:887–889. Blumenthal, D. M., and R. A. Hufbauer. 2007. Increased plant size in exotic populations: a common-garden test with 14 invasive species. Ecology 88:2758–2765. Bolker, B. M., M. E. Brooks, C. J. Clark, S. W. Geange, J. R. Poulsen, M. H. H. Stevens, et al. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24:127–135. Brncic, D., A. Prevosti, M. Budnik, M. Monclus, and J. Ocana. 1981. Colonization of Drosophila subobscura in Chile. 1. 1st population and cytogenetic studies. Genetica 56:3–9. Budnik, M., M. Benado, and L. Cifuentes. 1997. Colonization of Drosophila subobscura in Chile: experimental preadult competition with local species under bi- and tri-specific conditions. Neth. J. Zool. 47:133–141. Calabria, G., J. Máca, G. Bächli, L. Serra, and M. Pascual. 2012. First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J. Appl. Entomol. 136:139–147. Canty, A., and B. Ripley. 2015. boot: Bootstrap R (S-Plus) functions. R package version 1.3-16. https://cran.r-project.org/web/packages/boot/citation.html Castañeda, L. E., J. Balanyà, L. Rezende Enrico, M. Santos. 2013. Vanishing chromosomal inversion clines in Drosophila subobscura from Chile: is behavioral thermoregulation to blame? Am. Nat. 182:249–259. Chapple, D. G., S. M. Simmonds, and B. B. M. Wong. 2012. Can behavioral and personality traits influence the success of unintentional species introductions? Trends Ecol. Evol. 27:57–64. Chippindale, A. K., A. M. Leroi, S. B. Kim, and M. R. Rose. 1993. Phenotypic plasticity and selection in Drosophila life-history evolution. I. Nutrition and the cost of reproduction. J. Evol. Biol. 6:171–193. Colautti, R. I., and J. A. Lau. 2015. Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol. Ecol. 24:1999–2017. Colautti, R. I., A. Ricciardi, I. A. Grigorovich, and H. J. MacIsaac. 2004. Is invasion success explained by the enemy release hypothesis? Ecol. Lett. 7:721–733. Crispo, E. 2007. The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61:2469–2479. Davidson, A. M., M. Jennions, and A. B. Nicotra. 2011. Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis Ecol. Lett. 14:419–431. Dlugosch, K. M., and I. M. Parker. 2008. Invading populations of an ornamental shrub show rapid life history evolution despite genetic bottlenecks. Ecol. Lett. 11:701–709. Doak, P., P. Kareiva, and J. Kingsolver. 2006. Fitness consequences of choosy oviposition for a time-limited butterfly. Ecology 87:395–408. Dukas, R. 2005. Learning affects mate choice in female fruit flies. Behav. Ecol. 16:800–804. Durka, W., O. Bossdorf, D. Prati, and H. Auge. 2005. Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol. Ecol. 14:1697–1706. Dybdahl, M. F., and S. L. Kane. 2005. Adaptation vs. phenotypic plasticity in the success of a clonal invader. Ecology 86:1592–1601. Ebeling, S. K., J. Stoecklin, I. Hensen, and H. Auge. 2011. Multiple common garden experiments suggest lack of local adaptation in an invasive ornamental plant. J. Plant Ecol. 4:209–220. Egas, M., and M. W. Sabelis. 2001. Adaptive learning of host preference in a herbivorous arthropod. Ecol. Lett. 4:190–195. Fernandez Iriarte, P. J., J. Balanya, M. Pascual, F. Mestres, E. R. Hasson, A. Fontdevila, et al. 2009. Tracking the origin of an invasive species: Drosophila subobscura in Argentina. J. Evol. Biol. 22:650–658. Fincke, O. M., and H. Hadrys. 2001. Unpredictable offspring survivorship in the damselfly, Megaloprepus coerulatus, shapes parental behavior, constrains sexual selection, and challenges traditional fitness estimates. Evolution 55:762–772. Foucaud, J., A.-S. Philippe, C. Moreno, and F. Mery. 2013. A genetic polymorphism affecting reliance on personal versus public information in a spatial learning task in Drosophila melanogaster. Proc. Biol. Sci. 280:20130588. Geiger, J. H., P. D. Pratt, G. S. Wheeler, and D. A. Williams. 2011. Hybrid vigor for the invasive exotic Brazilian peppertree (Schinus terebinthifolius Raddi., Anacardiaceae) in Florida. Int. J. Plant Sci. 172:655–663. Gilchrist, G. W., R. B. Huey, J. Balanya, M. Pascual, and L. Serra. 2004. A time series of evolution in action: a latitudinal cline in wing size in South American Drosophila subobscura. Evolution 58:768–780. Horkova, K., and V. Kovac. 2014. Different life-histories of native and invasive Neogobius melanostomus and the possible role of phenotypic plasticity in the species' invasion success. Knowl. Manag. Aquat. Ecosyst. 412:01–11. Huey, R. B., G. W. Gilchrist, M. L. Carlson, D. Berrigan, and L. Serra. 2000. Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309. Kajita, Y., E. M. O'Neill, Y. Zheng, J. J. Obrycki, and D. W. Weisrock. 2012. A population genetic signature of human releases in an invasive ladybeetle. Mol. Ecol. 21:5473–5483. Kawecki, T. J. 2010. Evolutionary ecology of learning: insights from fruit flies. Popul. Ecol. 52:15–25. Keane, R. M., and M. J. Crawley. 2002. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17:164–170. Kotrschal, A., E. J. P. Lievens, J. Dahlbom, A. Bundsen, S. Semenova, M. Sundvik, et al. 2014. Artificial selection on relative brain size reveals a positive genetic correlation between brain size and proactive personality in the guppy. Evolution 68:1139–1149. Lande, R. 2015. Evolution of phenotypic plasticity in colonizing species. Mol. Ecol. 24:2038–2045. Lavergne, S., and J. Molofsky. 2007. Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc. Natl Acad. Sci. USA 104:3883–3888. Lee, C. E. 2002. Evolutionary genetics of invasive species. Trends Ecol. Evol. 17:386–391. Leger, E. A., and K. J. Rice. 2003. Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecol. Lett. 6:257–264. Long, T. A. F., P. M. Miller, A. D. Stewart, and W. R. Rice. 2009. Estimating the heritability of female lifetime fecundity in a locally adapted Drosophila melanogaster population. J. Evol. Biol. 22:637–643. Lowry, H., A. Lill, and B. B. M. Wong. 2013. Behavioural responses of wildlife to urban environments. Biol. Rev. 88:537–549. Maron, J. L., and M. Vila. 2001. When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373. Maron, J. L., M. Vila, R. Bommarco, S. Elmendorf, and P. Beardsley. 2004. Rapid evolution of an invasive plant. Ecol. Monogr. 74:261–280. Maynard Smith, J. 1958. The effects of temperature and of egg-laying on the longevity of Drosophila subobscura. J. Exp. Biol. 35:832–842. McKinney, M. L. 2006. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 127:247–260. McKinney, M. L., and J. L. Lockwood. 1999. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol. Evol. 14:450–453. Merilä, J., and B. C. Sheldon. 2000. Lifetime reproductive success and heritability in nature. Am. Nat. 155:301–310. Mery, F., and T. J. Kawecki. 2002. Experimental evolution of learning ability in fruit flies. Proc. Natl Acad. Sci. USA 99:14274–14279. Mery, F., and T. J. Kawecki. 2003. A fitness cost of learning ability in Drosophila melanogaster. Proc. Biol. Sci. 270:2465–2469. Mery, F., and T. J. Kawecki. 2004. An operating cost of learning in Drosophila melanogaster. Anim. Behav. 68:589–598. Meyer, G. A., and H. M. Hull-Sanders. 2008. Altered patterns of growth, physiology and reproduction in invasive genotypes of Solidago gigantea (Asteraceae). Biol. Invasions 10:303–317. Meyer, G., R. Clare, and E. Weber. 2005. An experimental test of the evolution of increased competitive ability hypothesis in goldenrod, Solidago gigantea. Oecologia 144:299–307. Mooney, H. A., and R. J. Hobbs. 2000. Invasive species in a changing world. Island Press, Washington, DC. Moran, E. V., and J. M. Alexander. 2014. Evolutionary responses to global change: lessons from invasive species. Ecol. Lett. 17:637–649. Papaj, D., and R. Prokopy. 1989. Ecological and evolutionary aspects of learning in phytophagous insects. Annu. Rev. Entomol. 34:315–350. Pascual, M., M. Constanti, G. Ribo, and A. Prevosti. 1990. Genetic changes in mating activity in laboratory strains of Drosophila subobscura. Genetica 80:39–43. Pascual, M., L. Serra, and F. J. Ayala. 1998. Interspecific laboratory competition of the recently sympatric species Drosophila subobscura and Drosophila pseudoobscura. Evolution 52:269–274. Pascual, M., M. P. Chapuis, F. Mestres, J. Balanya, R. B. Huey, G. W. Gilchrist, et al. 2007. Introduction history of Drosophila subobscura in the New World: a microsatellite-based survey using ABC methods. Mol. Ecol. 16:3069–3083. Pekkala, N., J. S. Kotiaho, and M. Puurtinen. 2011. Laboratory relationships between adult lifetime reproductive success and fitness surrogates in a Drosophila littoralis population. PLoS One 6:e24560. Pigliucci, M., C. J. Murren, and J. Mitton. 2003. Perspective: genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution 57:1455–1464. Prevosti, A., G. Ribo, L. Serra, M. Aguade, J. Balana, M. Monclus, et al. 1988. Colonization of America by Drosophila subobscura: experiment in natural populations that supports the adaptive role of chromosomal-inversion polymorphism. Proc. Natl Acad. Sci. USA 85:5597–5600. R Core Team. 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Reed, D. H., and E. H. Bryant. 2004. Phenotypic correlations among fitness and its components in a population of the housefly. J. Evol. Biol. 17:919–923. Rey, O., A. Estoup, M. Vonshak, A. Loiseau, S. Blanchet, L. Calcaterra, et al. 2012. Where do adaptive shifts occur during invasion? A multidisciplinary approach to unravelling cold adaptation in a tropical ant species invading the Mediterranean area. Ecol. Lett. 15:1266–1275. Rezende, E. L., J. Balanya, F. Rodriguez-Trelles, C. Rego, I. Fragata, M. Matos, et al. 2010. Climate change and chromosomal inversions in Drosophila subobscura. Clim. Res. 43:103–114. Reznick, D. 1985. Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267. Reznick, D., L. Nunney, and A. Tessier. 2000. Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol. Evol. 15:421–425. Roth, T. C., and V. V. Pravosudov. 2009. Hippocampal volumes and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison. Proc. Biol. Sci. 276:401–405. Roth, T. C., A. Brodin, T. V. Smulders, L. D. LaDage, and V. V. Pravosudov. 2010a. Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365:915. 2010;365: 2423–2423. Roth, T. C., L. D. LaDage, and V. V. Pravosudov. 2010b. Learning capabilities enhanced in harsh environments: a common garden approach. Proc. Biol. Sci. 277:3187–3193. Sakai, A. K., F. W. Allendorf, J. S. Holt, D. M. Lodge, J. Molofsky, K. A. With, et al. 2001. The population biology of invasive species. Annu. Rev. Ecol. Syst. 32:305–332. Santos, M., I. Fragata, J. Santos, P. Simoes, A. Marques, M. Lima, et al. 2010. Playing Darwin. Part B. 20 years of domestication in Drosophila subobscura. Theory Biosci. 129: 97–102. Santos, J., M. Pascual, P. Simões, I. Fragata, M. Lima, B. Kellen, et al. 2012. From nature to the laboratory: the impact of founder effects on adaptation. J. Evol. Biol. 25:2607–2622. Sgró, C. M., and A. A. Hoffmann. 1998. Heritable variation for fecundity in field-collected Drosophila melanogaster and their offspring reared under different environmental temperatures. Evolution 52:134–143. Simões, P., J. Santos, I. Fragata, L. D. Mueller, M. R. Rose, M. Matos, et al. 2008. How repeatable is adaptive evolution? The role of geographical origin and founder effects in laboratory adaptation. Evolution 62:1817–1829. Simões, P., G. Calabria, J. Picão-Osório, J. Balanyà, and M. Pascual. 2012. The genetic content of chromosomal inversions across a wide latitudinal gradient. PLoS One 7:e51625. Snell-Rood, E. C., G. Davidowitz, and D. R. Papaj. 2011. Reproductive tradeoffs of learning in a butterfly. Behav. Ecol. 22:291–302. Sol, D., S. Timmermans, and L. Lefebvre. 2002. Behavioural flexibility and invasion success in birds. Anim. Behav. 63:495–502. Sol, D., R. P. Duncan, T. M. Blackburn, P. Cassey, and L. Lefebvre. 2005. Big brains, enhanced cognition, and response of birds to novel environments. Proc. Natl Acad. Sci. USA 102:5460–5465. Sol, D., S. Bacher, S. M. Reader, and L. Lefebvre. 2008. Brain size predicts the success of mammal species introduced into novel environments. Am. Nat. 172:S63–S71. Tatem, A. J., and S. I. Hay. 2007. Climatic similarity and biological exchange in the worldwide airline transportation network. Proc. Biol. Sci. 274:1489–1496. Thompson, J., and O. Pellmyr. 1991. Evolution of oviposition behavior and host preference in Lepidoptera. Annu. Rev. Entomol. 36:65–89.