Abstract
Competition between microorganisms and arthropods has been shown to be an important ecological interaction determining animal development and spatial distribution patterns in saprophagous communities. In fruit-inhabiting Drosophila, variation in insect developmental success is not only determined by species-specific effects of various noxious filamentous fungi but, as suggested by an earlier study, also by additive genetic variation in the ability to successfully withstand the negative impact of the fungi. If this variation represents a direct adaptive response to the degree to which insect breeding substrates are infested with harmful fungi, genetic variation for successful development in the presence of fungi could be maintained by variation in infestation of resource patches with fungi. We selected for the ability to resist the negative influence of mould by maintaining replicated Drosophila melanogaster populations on substrates infested with Aspergillus nidulans. After five cycles of exposure to the fungus during the larval stage, the selected populations were compared with unselected control populations regarding adult survival and reproduction to reveal an evolved resistance against the fungal competitor. On fungus-infested larval feeding substrates, emerged adults from mould-selected populations had higher survival rates and higher early fecundity than the control populations. In the unselected populations, females had higher mortality rates than males, and a high proportion of both females and males appeared to be unable to lay eggs or fertilise eggs, respectively. When larvae developed on non-infested food we found indications of a loss of resistance to abiotic and starvation stress in the adult stage in flies from the selected populations. This suggests that there are costs associated with an increase in resistance against the microbial competitor. We discuss the underlying mechanisms that might have selected for increased resistance against harmful fungi.
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Abdou RF, Megalla SE, Azab SG (1984) Mutagenic effects of aflatoxin B-1 and G-1 on the Egyptian cotton leaf-worm, Spodoptera littoralis (Boisd.). Mycopathologia 88:23–26
Berenbaum MR (2002) Postgenomic chemical ecology: from genetic code to ecological interactions. J Chem Ecol 28:873–896
Bijlsma R, Loeschcke V (2005) Environmental stress, adaptation and evolution: an overview. J Evol Biol 18:744–749
Bok JW, Keller NP (2004) LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 3:527–535
Bubliy OA, Loeschcke V (2005) Correlated responses to selection for stress resistance and longevity in a laboratory population of Drosophila melanogaster. J Evol Biol 18:789–803
Burkepile DE, et al. (2006) Chemically mediated competition between microbes and animals: microbes as consumers in food webs. Ecology 87:2821–2831
Capaul M, Ebert D (2003) Parasite-mediated selection in experimental Daphnia magna populations. Evol Int J Org Evol 57:249–260
Chippindale AK, Chu TJF, Rose MR (1996) Complex trade-offs and the evolution of stravation resistance in Drosophila melanogaster. Evol Int J Org Evol 50:753–766
Cipollini ML, Stiles EW (1993) Fruit rot, antifungal defense, and palatability of fleshy fruits for fungivorous birds. Ecology 74:751–762
Conner JK (2003) Artificial selection: a powerful tool for ecologists. Ecology 84:1650–1660
Coustau C, Chevillon C, Ffrench-Constant R (2000) Resistance to xenobiotics and parasites: can we count the cost? Trends Ecol Evol 15:378–383
Crist TO, Friese CF (1993) The impact of fungi on soil seeds: implications for plants and granivores in a semiarid shrub-steppe. Ecology 74:2231–2239
Diamond JM (1987) Competition among different taxa. Nature 326:241
Djawdan M, Sugiyama TT, Schlaeger LK, Bradley TJ, Rose MR (1996) Metabolic aspects of the trade-off between fecundity and longevity in Drosophila melanogaster. Physiol Zool 69:1176–1195
Ellers J (1996) Fat and eggs: an alternative method to measure the trade-off between survival and reproduction in insects parasitoids. Neth J Zool 46:227–235
Fellowes M, Kraaijeveld AR, Godfray HCJ (1998) Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proc R Soc B 265:1553–1558
Foerster RE, Würgler FE (1984) In vitro studies on the metabolism of aflatoxin B1 and aldrin in testes of genetically different strains of Drosophila melanogaster. Arch Toxicol 56:12–17
Fry JD (2003) Detecting ecological trade-offs using selection experiments. Ecology 84:1672–1678
Fuller RC, Baer CF, Travis J (2005) How and when selection experiments might actually be useful. Integr Comp Biol 45:391–404
Gillespie JH, Turelli M (1989) Genotype–environment interactions and the maintenance of polygenic variation. Genetics 107:321–330
Hochberg ME, Lawton JH (1990) Competition between kingdoms. Trends Ecol Evol 5:367–371
Hodge S (1996) The relationship between Drosophila occurrence and mould abundance on rotting fruit. Br J Entomol Nat Hist 9:87–91
Hodge S, Arthur W (1997) Direct and indirect effects of Drosophila larvae on the growth of moulds. Entomologist 116:198–204
Hodge S, Mitchell P, Arthur W (1999) Factors affecting the occurrence of facilitative effects in interspecific interactions: an experiment using two species of Drosophila and Aspergillus niger. Oikos 87:166–174
Janzen DH (1977) Why fruits rot, seeds mold and meat spoils. Am Nat 111:691–713
Kolss M, Kraaijeveld AR, Mery F, Kawecki TJ (2006) No trade-off between learning ability and parasitoid resistance in Drosophila melanogaster. J Evol Biol 19:1359–1363
Kraaijeveld AR, Godfray HCJ (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389:278–280
Kraaijeveld AR, Godfray HCJ (2008) Selection for resistance to a fungal pathogen in Drosophila melanogaster. Heredity 100:400–406
Kraaijeveld AR, Barker CL, Godfray HCJ (2008) Stage-specific sex differences in Drosophila immunity to parasites and pathogens. Evol Ecol 22:217–228
Lee S-E, Campbell BC (2000) In vitro metabolism of aflatoxin B1 by larvae of navel orangeworm, Amyelois transitella (Walker) (Insecta, Leptidoptera, Pyralidae) and codling moth, Cydia pomonella (L.) (Insecta, Leptidoptera, Tortricidae). Arch Insect Biochem Physiol 45:166–174
Luong LT, Polak M (2007) Costs of resistance in the Drosophila–Macrocheles system: a negative genetic correlation between ectoparasite resistance and reproduction. Evol Int J Org Evol 61:1391–1402
Matzkin LM, Watts TD, Bitler BG, Machado CA, Markow TA (2006) Functional genomics of cactus host shifts in Drosophila mojavensis. Mol Ecol 15:4635–4643
McKean K, Yourth C, Lazzaro B, Clark A (2008) The evolutionary costs of immunological maintenance and deployment. BMC Evol Biol 8:76
Melone PD, Chinnici JP (1986) Selection for increased resistance to aflatoxin B1 toxicity in Drosophila melanogaster. J Invert Pathol 48:60–65
Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation in bumblebee workers. Science 290:1166–1168
Niu G, Wen Z, Rupasinghe SG, Zeng RS, Berenbaum MR, Schuler MA (2008) Aflatoxin B1 detoxification by CYP321A1 in Helicoverpa zea. Arch Insect Biochem Physiol 69:32–45
Polak M (2003) Heritability of resistance against ectoparasitism in the Drosophila–Macrocheles system. J Evol Biol 16:74–82
Reiss J (1975) Insecticidal and larvicidal activities of the mycotoxins aflatoxin B1, rubratoxin B, patulin and diacetoxyscirpenol towards Drosophila melanogaster. Chem Biol Interact 10:339–342
Rion S, Kawecki TJ (2007) Evolutionary biology of starvation resistance: what we have learned from Drosophila. J Evol Biol 20:1655–1664
Rohlfs M (2005a) Clash of kingdoms or why Drosophila larvae positively respond to fungal competitors. Front Zool 2:2
Rohlfs M (2005b) Density-dependent insect-mold interactions: effects on fungal growth and spore production. Mycologia 97:996–1001
Rohlfs M (2006) Genetic variation and the role of insect life history traits in the ability of Drosophila larvae to develop in the presence of a filamentous fungus. Evol Ecol 20:271–289
Rohlfs M, Hoffmeister TS (2003) An evolutionary explanation of the aggregation model of species coexistence. Proc R Soc B (Suppl) 270:S33–S35
Rohlfs M, Obmann B (2009) Species-specific responses of dew fly larvae to mycotoxins. Mycotox Res 25:103–112
Rohlfs M, Obmann B, Petersen R (2005) Competition with filamentous fungi and its implications for a gregarious life-style in insects living on ephemeral resources. Ecol Entomol 30:556–563
Rohlfs M, Albert M, Keller NP, Kempken F (2007) Secondary chemicals protect mould from fungivory. Biol Lett 3:523–525
Rozen DE, Engelmoer DJP, Smiseth PT (2008) Antimicrobial strategies in burying beetles breeding on carrion. Proc Natl Acad Sci USA 105:17890–17895
Sandland GJ, Minchella DJ (2003) Costs of immune defense: an enigma wrapped in an environmental cloak? Trends Parasitol 19:571–574
SAS Institute (2005) SAS/STAT 9.1 user’s guide—the GLIMMIX procedure. SAS Institute, Cary
Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc B 270:357–366
Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50:529–551
Shivik JA (2006) Are vultures birds, and do snakes have venom, because of macro- and microscavenger conflict? Bioscience 56:819–823
Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037
Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285
Susuki S (2001) Suppression of fungal development on carcasses by the burying beetle Nicrophorus quadripunctatus (Coleoptera: Silphidae). Entomol Sci 4:403–405
Tinsley MC, Blanford S, Jiggins FM (2006) Genetic variation in Drosophila melanogaster pathogen susceptibility. Parasitology 132:767–773
Tollrian R, Harvell CD (eds) (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton
Acknowledgments
We thank Coralie Herbst, Gesa Wölm, Jens Berner and Mourad Bouchedda for their help with collecting data for the fitness assay. Christiana Anagnostou is acknowledged for her support with establishing and maintaining the Drosophila base population. The A. nidulans strain used in this study was provided by Nancy P. Keller (University of Wisconsin, Madison, Wis.). We thank Munjong Kolss for critical comments on an earlier version of this paper. This study was supported by a Deutsche Forschungsgemeinschaft research grant to M. R. (Ro3523/2-1). The experiments described in this paper comply with the current laws of Germany.
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Communicated by Thomas Hoffmeister.
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Wölfle, S., Trienens, M. & Rohlfs, M. Experimental evolution of resistance against a competing fungus in Drosophila melanogaster . Oecologia 161, 781–790 (2009). https://doi.org/10.1007/s00442-009-1414-x
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DOI: https://doi.org/10.1007/s00442-009-1414-x