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Geographic and within-population variation in the globeflower–globeflower fly interaction: the costs and benefits of rearing pollinators’ larvae

  • Plant Animal Interactions
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Abstract

Interspecific interactions can vary within and among populations and geographic locations, and this variation can influence the nature of the interaction (e.g. mutualistic vs. antagonistic) and its evolutionary stability. Globeflowers are exclusively pollinated by flies, whose larvae feed only on their seeds. Here we document geographic variability in costs and benefits in globeflowers in sustaining their pollinating flies throughout the range of this arctic-alpine European plant over several years. A total of 1,710 flower heads from 38 populations were analysed for their carpel, egg and seed contents. Individual and population analyses control for the confounding influences of variation in both: (1) population traits, such as fly density and egg distribution among flower heads; and (2) individuals traits, such as carpel and egg numbers per flower head. Despite considerable variation in ecological conditions and pollinator densities across populations, large proportions (range 33–58%) of seeds were released after predation, with a benefit-to-cost ratio of 3, indicating that the mutualism is stable over the whole globeflower geographical range. The stability of the mutualistic interaction relies on density-dependent competition among larvae co-developing in a flower head. This competition is revealed by a sharp decrease in the number of seeds eaten per larva with increasing larval number, and is intensified by non-uniform egg distribution among globeflowers within a population. Carpel number is highly variable across globeflowers (range 10–69), and flies lay more eggs in large flowers. Most plants within a population contribute to the rearing of pollinators, but the costs are greater for some than for others. Large globeflowers lose more seed to pollinator larvae, but also release more seed than smaller plants. The apparent alignment of interests between fly and plants (positive relationship between numbers of seed released and destroyed) is shown to hide a conflict of interest found when flower size is controlled for.

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References

  • Addicott JF (1986) Variation in the costs and benefits of mutualism—the interaction between yuccas and yucca moths. Oecologia 70:486–494

    Article  Google Scholar 

  • Anstett MC, Hossaert-McKey M, Kjellberg F (1997) Figs and fig pollinators: evolutionary conflicts in a coevolved mutualism. Trends Ecol Evol 12:94–99

    Article  Google Scholar 

  • Axelrod R, Hamilton W D (1981) The evolution of cooperation. Science 211:1390–1396

    Article  PubMed  CAS  Google Scholar 

  • Bao T, Addicott JF (1998) Cheating in mutualism: defection of Yucca baccata against its yucca moths. Ecol Lett 1:155–159

    Article  Google Scholar 

  • Bronstein J (2001) The costs of mutualism. Am Zool 41:825–839

    Article  Google Scholar 

  • Bull JJ, Rice WR (1991) Distinguishing mechanisms for the evolution of cooperation. J Theor Biol 149:63–74

    PubMed  CAS  Google Scholar 

  • Charnov EL, Maynard-Smith J, Bull JJ (1976) Why be a hermaphrodite? Nature 263:126–125

    Article  Google Scholar 

  • De Jong R, Stadler E. (2001) Sensilla on cabbage root fly tarsae sensitive to egg-associated compounds. Chemoecology 11:145–147

    Article  Google Scholar 

  • DeAngelis DL, Holland JN (2006) Emergence of ratio-dependent and predator-dependent functional responses for pollination mutualism and seed parasitism. Ecol Modell 191:551–556

    Article  Google Scholar 

  • Després L (2003) Sex and pollen: the role of males in stabilising a plant–seed eater pollinating mutualism. Oecologia 135:60–66

    PubMed  Google Scholar 

  • Després L, Jaeger N (1999) Evolution of oviposition strategies and speciation in the globeflower flies Chiastocheta spp. (Anthomyiidae). J Evol Biol 12:822–831

    Article  Google Scholar 

  • Després L, Cherif M (2004). The role of competition in adaptive radiation: a field study on sequentially ovipositing host-specific seed predators. J Anim Ecol 73:109–116

    Article  Google Scholar 

  • Hemborg ÅM, Després L (1999) Oviposition by mutualistic seed parasitic pollinators and its effects on annual fitness of single- and multi-flowered host plants. Oecologia 120:427–436

    Article  Google Scholar 

  • Herre EA, West SA (1997) Conflict of interest in a mutualism: documenting the elusive fig wasp–seed trade-off. Proc R Soc Lond B Biol Sci 264:1501–1507

    Article  Google Scholar 

  • Herre EA, Knowlton N, Mueller UG, Rehner S.A. (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53

    Article  PubMed  Google Scholar 

  • Holland JN, DeAngelis DL (2001) Population dynamics and the ecological stability of obligate pollination mutualisms. Oecologia 126:575–586

    Article  Google Scholar 

  • Holland JN, Fleming TH (1999) Geographic and population variation in pollinating seed-consuming interactions between senita cacti (Lophocereus schottii) and senita moths (Upiga virescens). Oecologia 121:405–410

    Article  Google Scholar 

  • Huth CJ, Pellmyr O (1999) Yucca moth oviposition and pollination is affected by past flower visitors: evidence for a host-marking pheromone. Oecologia 119:593–599

    Article  Google Scholar 

  • Jaeger N, Després L (1998) Obligate mutualism between Trollius europaeus and its seed-parasite pollinators Chiastocheta flies in the Alps. C R Acad Sci Paris 321:789–796

    Google Scholar 

  • Jaeger N, Till-Bottraud I, Després L (2000) Evolutionary conflict between Trollius europaeus and its seed parasite pollinators Chiastocheta flies. Evol Ecol Res 2:885–896

    Google Scholar 

  • Jaeger N, Pompanon F, Després L (2001) Variation in predation costs with Chiastocheta egg number on Trollius europaeus: how many seeds to pay for pollination? Ecol Entomol 26:1–7

    Article  Google Scholar 

  • Janzen DH (1979) How many babies do figs pay for babies? Biotropica 11:48–50

    Article  Google Scholar 

  • Johannesen J, Loeschcke V (1996) Distribution, abundance and oviposition patterns of four coexisting Chiastocheta species (Diptera: Anthomyiidae). J Anim Ecol 65:567–576

    Article  Google Scholar 

  • Morris WF, Bronstein JL, Wilson WG (2003) Three-way coexistence in obligate mutualist–exploiter interactions: the potential role of competition. Am Nat 161:860–875

    Article  PubMed  Google Scholar 

  • Pellmyr O (1989) The cost of mutualism: interactions between Trollius europaeus and its pollinating parasites. Oecologia 78:53–59

    Article  Google Scholar 

  • Pellmyr O, Huth CJ (1994) Evolutionary stability of mutualism between yuccas and yucca moths. Nature 372:257–260

    Article  CAS  Google Scholar 

  • Pompanon F, Pettex E, Després L (2006) Patterns of resource exploitation in four coexisting globeflower fly species (Chiastocheta sp.). Acta Oecol 29: 233–240

    Article  Google Scholar 

  • Wiseman BR, Snook ME, Isenhour DJ (1993) Maysin content and growth of corn earworm larvae (Lepidoptera: Noctuidae) on silks from first and second ears of corn. J Econ Entomol 86:939–944

    Google Scholar 

  • Yu DW (2001) Parasites of mutualisms. Biol J Linn Soc 72:529–546

    Article  Google Scholar 

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Acknowledgements

We thank N. Jaeger and J.-F. Desmet for field assistance and A. Herre for helpful comments on the manuscript. L. D. was supported by the French Centre National de la Recherche Scientifique (CNRS) and Å. M. H. by the Royal Swedish Academy of Sciences, the National Research Foundation in South Africa, and the Swedish Foundation for International Cooperation in Research and Higher Education (STINT).

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Authors and Affiliations

  1. Laboratoire d’Ecologie Alpine, CNRS UMR 5553, Université J. Fourier, BP 53, 38041, Grenoble, France

    Laurence Després & Sébastien Ibanez

  2. Department of Botany, University of Cape Town, Private Bag, Rondebosch, 7700, South Africa

    Åsa M. Hemborg

  3. Laboratoire Génome, Populations, Interactions, Adaptation, CNRS UMR 5171, Université Montpellier 2, 34095, Montpellier, France

    Bernard Godelle

Authors
  1. Laurence Després
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  2. Sébastien Ibanez
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  3. Åsa M. Hemborg
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  4. Bernard Godelle
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Correspondence to Laurence Després.

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Communicated by Jacqui Shykoff.

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Després, L., Ibanez, S., Hemborg, Å.M. et al. Geographic and within-population variation in the globeflower–globeflower fly interaction: the costs and benefits of rearing pollinators’ larvae. Oecologia 151, 240–250 (2007). https://doi.org/10.1007/s00442-006-0578-x

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  • DOI: https://doi.org/10.1007/s00442-006-0578-x

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