Skip to main content
Log in

Experimental Evolution of Alkaloid Tolerance in Sibling Drosophila Species with Different Degrees of Specialization

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Drosophila buzzatii and Drosophila koepferae are sibling species with marked ecological differences related to their patterns of host exploitation. D. buzzatii is a polyphagous species with a sub-cosmopolitan distribution, while D. koepferae is endemic to the mountain plateaus of the Andes, where it exploits alkaloidiferous columnar cacti as primary hosts. We use experimental evolution to study the phenotypic response of these cactophilic Drosophila when confronting directional selection to cactus chemical defenses for 20 generations. Flies adapted to cactus diets also experienced higher viability on alkaloid-enriched media, suggesting the selection of adaptive genetic variation for chemical-stress tolerance. The more generalist species D. buzzatii showed a rapid adaptive response to moderate levels of secondary metabolites, whereas the columnar cacti specialist D. koepferae tended to maximize fitness under harder conditions. The evolutionary dynamic of fitness-related traits suggested the implication of metabolic efficiency as a key mediator in the adaptive response to chemical stress. Although we found no evidence of adaptation costs accompanying specialization, our results suggest the involvement of compensatory evolution. Overall, our study proposes that differential adaptation to secondary metabolites may contribute to varying degrees of host specialization, favoring niche partitioning among these closely related species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agrawal, A. A. (2001). Phenotypic plasticity in the interactions and evolution of species. Science, 294(5541), 321–326.

    Article  CAS  PubMed  Google Scholar 

  • Agrawal, A. A., & Weber, M. G. (2015). On the study of plant defence and herbivory using comparative approaches: How important are secondary plant compounds. Ecology Letters, 18(10), 985–991.

    Article  PubMed  Google Scholar 

  • Ali, J. G., & Agrawal, A. A. (2012). Specialist versus generalist insect herbivores and plant defense. Trends in Plant Science, 17(5), 293–302.

    Article  CAS  PubMed  Google Scholar 

  • Annicchiarico, P. (2002). Genotype × environment interaction: Challenges and opportunities for plant breeding and cultivar recommendations. Rome: Food and Agriculture Organization of the United Nations.

    Google Scholar 

  • Barker, J. S. F. (2013). Genetic history of a colonizing population: Drosophila buzzatii (Diptera: Drosophilidae) in Australia. Biological Journal of the Linnean Society, 109(3), 682–698.

    Article  Google Scholar 

  • Barker, J. S. F., & Starmer, W. T. (1982). Ecological genetics and evolution: The cactus-yeast-Drosophila model system. London: Academic Press.

    Google Scholar 

  • Bono, J. M., Matzkin, L. M., Castrezana, S., & Markow, T. A. (2008). Molecular evolution and population genetics of two Drosophila mettleri cytochrome P450 genes involved in host plant utilization. Molecular Ecology, 17(13), 3211–3221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brattsten, L. B., Wilkinson, C. F., & Eisner, T. (1977). Herbivore-plant interactions: Mixed-function oxidases and secondary plant substances. Science, 196(4296), 1349–1352.

    Article  CAS  PubMed  Google Scholar 

  • Cabrera, A. L. (1976). Enciclopedia Argentina de Agricultura y Jardinería. Buenos Aires: ACME.

    Google Scholar 

  • Calabrese, E. J., & Baldwin, L. A. (2003). Toxicology rethinks its central belief. Nature, 421(6924), 691–692.

    Article  CAS  PubMed  Google Scholar 

  • Camargo, F. P., Araujo, A. C. V., de Moraes, E. M., & Dos Santos, A. C. A. (2016). A comparison between cactophilic yeast communities isolated from Cereus hildmannianus and Praecereus euchlorus necrotic cladodes. Fungal Biology, 120(10), 1175–1183.

    Article  PubMed  Google Scholar 

  • Clark, A. G., & Fucito, C. D. (1998). Stress tolerance and metabolic response to stress in Drosophila melanogaster. Heredity, 81(5), 514–527.

    Article  CAS  PubMed  Google Scholar 

  • Conner, J. K. (2003). Artificial selection: A powerful tool for ecologists. Ecology, 84(7), 1650–1660.

    Article  Google Scholar 

  • Cooper, M., DeLacy, I. H., & Basford, K. E. (1996). Relationships among analytical methods used to analyse genotypic adaptation in multi-environment trials. In M. Cooper, G.L. Hammer (Eds.), Plant adaptation and crop improvement (pp. 193–224). Wallingford: CAB International in association with IRRI and ICRISAT.

    Google Scholar 

  • Corio, C., Soto, I. M., Carreira, V., Padró, J., Betti, M. I., & Hasson, E. (2013). An alkaloid fraction extracted from the cactus Trichocereus terscheckii affects fitness in the cactophilic fly Drosophila buzzatii (Diptera: Drosophilidae). Biological Journal of the Linnean Society, 109(2), 342–353.

    Article  Google Scholar 

  • Cortese, M. D., Norry, F. M., Piccinali, R., & Hasson, E. (2002). Direct and correlated responses to artificial selection on developmental time and wing length in Drosophila buzzatii. Evolution, 56(12), 2541–2547.

    Article  PubMed  Google Scholar 

  • Costantini, D., Metcalfe, N. B., & Monaghan, P. (2010). Ecological processes in a hormetic framework. Ecology Letters, 13(11), 1435–1447.

    Article  PubMed  Google Scholar 

  • De Panis, D. N., Padró, J., Furió-Tarí, P., Tarazona, S., Carmona, M., Soto, P. S., I. M., … & Hasson, E. (2016). Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila. Molecular Ecology, 25(18), 4534–4550.

    Article  PubMed  Google Scholar 

  • Ehrlich, P. R., & Raven, P. H. (1964). Butterflies and plants: A study in coevolution. Evolution, 18, 586–608.

    Article  Google Scholar 

  • Fanara, J. J., Fontdevila, A., & Hasson, E. (1999). Oviposition preference and life history traits in cactophilic Drosophila koepferae and D. buzzatii in association with their natural hosts. Evolutionary Ecology, 13(2), 173–190.

    Article  Google Scholar 

  • Fanara, J. J., & Hasson, E. (2001). Oviposition acceptance and fecundity schedule in the cactophilic sibling species Drosophila buzzatii and D. koepferae on their natural hosts. Evolution, 55(12), 2615–2619.

    Article  CAS  PubMed  Google Scholar 

  • Fanara, J. J., Soto, I. M., Lipko, P., & Hasson, E.. (Patterson (2016). First record of Drosophila buzzatii & Wheeler) (Diptera: Drosophilidae) emerging from a non-cactus host. Neotropical Entomology, 45(3), 333–335.

    Article  CAS  PubMed  Google Scholar 

  • Fernández Iriarte, P., & Hasson, E. (2000). The role of the use of different host plants in the maintenance of the inversion polymorphism in the cactophilic Drosophila buzzatii. Evolution, 54(4), 1295–1302.

    Article  PubMed  Google Scholar 

  • Fogleman, J. C., & Danielson, P. B. (2001). Chemical interactions in the cactus-microorganism-Drosophila model system of the Sonoran Desert 1. American Zoologist, 41(4), 877–889.

    CAS  Google Scholar 

  • Fontdevila, A., Pla, C., Hasson, E., Wasserman, M., Sanchez, A., Naveira, H., & Ruiz, A. (1988). Drosophila koepferae: A new member of the Drosophila serido (Diptera: Drosophilidae) superspecies taxon. Annals of the Entomological Society of America, 81(3), 380–385.

    Article  Google Scholar 

  • Forbes, V. E. (2000). Is hormesis an evolutionary expectation? Functional Ecology, 14(1), 12–24.

    Article  Google Scholar 

  • Franco, F. F., & Manfrin, M. H. (2013). Recent demographic history of cactophilic Drosophila species can be related to Quaternary palaeoclimatic changes in South America. Journal of Biogeography, 40(1), 142–154.

    Article  Google Scholar 

  • Futuyma, D. J., & Moreno, G. (1988). The evolution of ecological specialization. Annual Review of Ecology and Systematics, 19(1), 207–233.

    Article  Google Scholar 

  • Gloss, A. D., Vassão, D. G., Hailey, A. L., Dittrich, A. C. N., Schramm, K., Reichelt, M., … & Montfort, W. R. (2014). Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the Drosophilidae. Molecular Biology and Evolution, 31(9), 2441–2456.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goenaga, J., Fanara, J. J., & Hasson, E. (2013). Latitudinal variation in starvation resistance is explained by lipid content in natural populations of Drosophila melanogaster. Evolutionary Biology, 40(4), 601–612.

    Article  Google Scholar 

  • Hasson, E., Naveira, H., & Fontdevila, A. (1992). The breeding sites of Argentinian cactophilic species of the Drosophila mulleri complex (subgenus Drosophila-repleta group). Revista chilena de historia natural, 65(3), 319–326.

    Google Scholar 

  • Hasson, E., Soto, I. M., Carreira, V. P., Corio, C., Soto, E. M., & Betti, M. (2009). .Host plants, fitness and developmental instability in a guild of cactophilic species of the genus Drosophila. In Ecotoxicology research developments. New York: Nova Science Publisher Inc.

    Google Scholar 

  • Hoffmann, A. A., & Parsons, P. A. (1989). An integrated approach to environmental stress tolerance and life-history variation: Desiccation tolerance in Drosophila. Biological Journal of the Linnean Society, 37(1-2), 117–136.

    Article  Google Scholar 

  • Jablonski, D. (2017). Approaches to macroevolution: 2. Sorting of variation, some overarching issues, and general conclusions. Evolutionary Biology, 44, 451–475.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kassen, R. (2002). The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology, 15(2), 173–190.

    Article  Google Scholar 

  • Kolss, M., Vijendravarma, R. K., Schwaller, G., & Kawecki, T. J. (2009). Life-history consequences of adaptation to larval nutritional stress in drosophila. Evolution, 63(9), 2389–2401.

    Article  PubMed  Google Scholar 

  • Lande, R. (2009). Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. Journal of Evolutionary biology, 22(7), 1435–1446.

    Article  PubMed  Google Scholar 

  • Lande, R., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution, 37, 1210–1226.

    Article  PubMed  Google Scholar 

  • Loxdale, H. D., Lushai, G., & Harvey, J. A. (2011). The evolutionary improbability of ‘generalism’in nature, with special reference to insects. Biological Journal of the Linnean Society, 103(1), 1–18.

    Article  Google Scholar 

  • Manfrin, M. H., & Sene, F. M. (2006). Cactophilic Drosophila in South America: A model for evolutionary studies. Genetica, 126(1–2), 57–75.

    Article  PubMed  Google Scholar 

  • Marden, J. H. (2013). Nature’s inordinate fondness for metabolic enzymes: Why metabolic enzyme loci are so frequently targets of selection. Molecular Ecology, 22(23), 5743–5764.

    Article  CAS  PubMed  Google Scholar 

  • Markow, T. A., & O’Grady, P. M. (2005). Drosophila:. In a guide to species identification and use. New York: Academic Press.

    Google Scholar 

  • Matzkin, L. M. (2012). Population transcriptomics of cactus host shifts in Drosophila mojavensis. Molecular Ecology, 21(10), 2428–2439.

    Article  PubMed  Google Scholar 

  • McGirr, J. A., Johnson, L. M., Kelly, W., Markow, T. A., & Bono, J. M. (2017). Reproductive Isolation Among Drosophila arizonae from Geographically Isolated Regions of North America. Evolutionary Biology, 44(1), 82–90.

    Article  Google Scholar 

  • McKenzie, J. A., & Clarke, G. M. (1988). Diazinon resistance, fluctuating asymmetry and fitness in the Australian sheep blowfly, lucilia cuprina. Genetics, 120(1), 213–220.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mithöfer, A., & Boland, W. (2012). Plant defense against herbivores: Chemical aspects. Annual Review of Plant Biology, 63, 431–450.

    Article  PubMed  Google Scholar 

  • Murren, C. J., Maclean, H. J., Diamond, S. E., Steiner, U. K., Heskel, M. A., Handelsman, C. A., … & Relyea, R. A. (2014). Evolutionary change in continuous reaction norms. The American Naturalist, 183(4), 453–467.

    Article  PubMed  Google Scholar 

  • Nylin, S., & Janz, N. (2009). Butterfly host plant range: An example of plasticity as a promoter of speciation? Evolutionary Ecology, 23(1), 137–146.

    Article  Google Scholar 

  • Oliveira, D. C., Almeida, F. C., O’Grady, P. M., Armella, M. A., DeSalle, R., & Etges, W. J. (2012). Monophyly, divergence times, and evolution of host plant use inferred from a revised phylogeny of the Drosophila repleta species group. Molecular Phylogenetics and Evolution, 64(3), 533–544.

    Article  PubMed  Google Scholar 

  • Padró, J., Carreira, V., Corio, C., Hasson, E., & Soto, I. M. (2014). Host alkaloids differentially affect developmental stability and wing vein canalization in cactophilic Drosophila buzzatii. Journal of Evolutionary Biology, 27(12), 2781–2797.

    Article  PubMed  Google Scholar 

  • Parsons, P. A. (2001). The hormetic zone: An ecological and evolutionary perspective based upon habitat characteristics and fitness selection. The Quarterly Review of Biology, 76(4), 459–467.

    Article  CAS  PubMed  Google Scholar 

  • Piccinali, R., Aguadé, M., & Hasson, E. (2004). Comparative molecular population genetics of the Xdh locus in the cactophilic sibling species Drosophila buzzatii and D. koepferae. Molecular Biology and Evolution, 21(1), 141–152.

    Article  CAS  PubMed  Google Scholar 

  • Piccinali, R. V., Mascord, L. J., Barker, J. S. F., Oakeshott, J. G., & Hasson, E. (2007). Molecular population genetics of the α-Esterase5 gene locus in original and colonized populations of Drosophila buzzatii and its sibling Drosophila koepferae. Journal of Molecular Evolution, 64(2), 158–170.

    Article  CAS  PubMed  Google Scholar 

  • Pischedda, A., & Chippindale, A. (2005). Sex, mutation and fitness: Asymmetric costs and routes to recovery through compensatory evolution. Journal of Evolutionary Biology, 18(4), 1115–1122.

    Article  CAS  PubMed  Google Scholar 

  • Rohlf, F. J. (2015). The tps series of software. Hystrix, The Italian Journal of Mammalogy, 26(1), 9–12.

    Google Scholar 

  • Rosenthal, G. A., & Berenbaum, M. R.(2012). Herbivores: Their interactions with secondary plant metabolites: Ecological and Evolutionary Processes (Vol. 2). London: Academic Press.

    Google Scholar 

  • Santos, M., Ruiz, A., Barbadilla, A., Quezada-Díaz, J. E., Hasson, E., & Fontdevila, A. (1988). The evolutionary history of Drosophila buzzatii. XlV. Larger flies mate more often in nature. Heredity, 61, 255–262.

    Article  Google Scholar 

  • Sgro, C. M., & Hoffmann, A. A. (2004). Genetic correlations, tradeoffs and environmental variation. Heredity, 93(3), 241–248.

    Article  CAS  PubMed  Google Scholar 

  • Soto, I. M., Carreira, V. P., Corio, C., Padró, J., Soto, E. M., & Hasson, E. (2014). Differences in tolerance to host cactus alkaloids in Drosophila koepferae and D. buzzatii. PLoS ONE, 9(2), e88370.

    Article  PubMed  PubMed Central  Google Scholar 

  • Soto, I. M., Carreira, V. P., Fanara, J. J., & Hasson, E. (2007). Evolution of male genitalia: Environmental and genetic factors affect genital morphology in two Drosophila sibling species and their hybrids. BMC Evolutionary Biology, 7(1), 77.

    Article  PubMed  PubMed Central  Google Scholar 

  • Soto, I. M., Carreira, V. P., Soto, E. M., & Hasson, E. (2008). Wing morphology and fluctuating asymmetry depend on the host plant in cactophilic Drosophila. Journal of Evolutionary Biology, 21(2), 598–609.

    Article  CAS  PubMed  Google Scholar 

  • Timbrel, J. A. (2009). Principles of biochemical toxicology (4th edn.). London: Informa Healthcare.

    Google Scholar 

  • Vijendravarma, R. K., Narasimha, S., & Kawecki, T. J. (2012). Adaptation to abundant low quality food improves the ability to compete for limited rich food in Drosophila melanogaster. PLoS ONE, 7(1), e30650.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wan, J. S., Pang, C. K., & Bonser, S. P. (2017). Does the cost of adaptation to extremely stressful environments diminish over time? A literature synthesis on how plants adapt to heavy metals and pesticides. Evolutionary Biology, 44, 411–426.

    Article  Google Scholar 

  • Whittaker, R. H., & Feeny, P. P. (1971). Allelochemicals: Chemical interactions between species. Science, 171(3973), 757–770.

    Article  CAS  PubMed  Google Scholar 

  • Wink, M., Schmeller, T., & Latz-Brüning, B. (1998). Modes of action of allelochemical alkaloids: Interaction with neuroreceptors, DNA, and other molecular targets. Journal of Chemical Ecology, 24(11), 1881–1937.

    Article  CAS  Google Scholar 

  • Zar, J. H. (1996). Biostatistical analysis. New Jersey: Prentice Hall Inc.

    Google Scholar 

Download references

Acknowledgements

We want to thanks to Pedro Fontanarrosa for assistance in running the experiments, and to Sergio Szajnman for invaluable technical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julián Padró.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Padró, J., De Panis, D.N., Vrdoljak, J. et al. Experimental Evolution of Alkaloid Tolerance in Sibling Drosophila Species with Different Degrees of Specialization. Evol Biol 45, 170–181 (2018). https://doi.org/10.1007/s11692-017-9441-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-017-9441-8

Keywords

Navigation