All Title Author
Keywords Abstract

PLOS Biology  2008 

A Role for Parasites in Stabilising the Fig-Pollinator Mutualism

DOI: 10.1371/journal.pbio.0060059

Full-Text   Cite this paper   Add to My Lib

Abstract:

Mutualisms are interspecific interactions in which both players benefit. Explaining their maintenance is problematic, because cheaters should outcompete cooperative conspecifics, leading to mutualism instability. Monoecious figs (Ficus) are pollinated by host-specific wasps (Agaonidae), whose larvae gall ovules in their “fruits” (syconia). Female pollinating wasps oviposit directly into Ficus ovules from inside the receptive syconium. Across Ficus species, there is a widely documented segregation of pollinator galls in inner ovules and seeds in outer ovules. This pattern suggests that wasps avoid, or are prevented from ovipositing into, outer ovules, and this results in mutualism stability. However, the mechanisms preventing wasps from exploiting outer ovules remain unknown. We report that in Ficus rubiginosa, offspring in outer ovules are vulnerable to attack by parasitic wasps that oviposit from outside the syconium. Parasitism risk decreases towards the centre of the syconium, where inner ovules provide enemy-free space for pollinator offspring. We suggest that the resulting gradient in offspring viability is likely to contribute to selection on pollinators to avoid outer ovules, and by forcing wasps to focus on a subset of ovules, reduces their galling rates. This previously unidentified mechanism may therefore contribute to mutualism persistence independent of additional factors that invoke plant defences against pollinator oviposition, or physiological constraints on pollinators that prevent oviposition in all available ovules.

References

[1]  Keller L, editor. (1999) Levels of selection in evolution. Princeton (New Jersey): Princeton University Press. 318 p.
[2]  West SA, Griffin A, Gardner A (2007) Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol 20: 415–432.
[3]  Yu DW (2001) Parasites of mutualisms. Biol J Linn Soc 72: 529–546.
[4]  Ferdy JB, Despres L, Godelle B (2002) Evolution of mutualism between globeflowers and their pollinating flies. J Theoret Biol 217: 219–234.
[5]  Kiers ET, Rousseau RA, West SA, Denison RF (2003) Host sanctions and the legume-rhizobia mutualism. Nature 425: 78–81.
[6]  Bronstein JL, Ziv Y (1997) Costs of two non-mutualistic species in a yucca/yucca moth mutualism. Oecologia 112: 379–385.
[7]  Edwards DP, Hassall M, Sutherland WJ, Yu DW (2006) Selection for protection in an ant-plant mutualism: host sanctions, host modularity, and the principal-agent game. Proc Biol Sci 273: 595–602.
[8]  Foster KR, Wenseleers T (2006) A general model for the evolution of mutualisms. J Evol Biol 19: 1283–1293.
[9]  West SA, Griffin AS, Gardner A (2007) Evolutionary explanations of cooperation. Curr Biol 17: R661–R672.
[10]  Cook JM, Rasplus JY (2003) Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol Evol 18: 241–248.
[11]  Weiblen GD (2002) How to be a fig wasp. Ann Rev Entomol 47: 299–330.
[12]  R?nsted N, Weiblen GD, Cook JM, Salamin N, Machado CA, et al. (2005) 60 million years of co-divergence in the fig-wasp symbiosis. Proc Biol Sci 272: 2593–2599.
[13]  Ganeshaiah KN, Kathuria P, Shaankar RU (1999) Does optimal packing of flowers in syconia shape style length variation in monoecious figs. Biotropica 31: 312–320.
[14]  Ganeshaiah KN, Kathuria P, Shaankar RU, Vasudeva R (1995) Evolution of style length variability in figs and optimization of ovipositor length in their pollinator wasps: a coevolutionary model. J Genet 74: 25–39.
[15]  Anstett MC (2001) Unbeatable strategy, constraint and coevolution, or how to resolve evolutionary conflicts: the case of the fig/wasp mutualism. Oikos 95: 476–484.
[16]  Jousselin E, Hossart-McKey M, Vernet D, Kjellberg F (2001) Egg deposition patterns of fig pollinating wasps: implications for studies on the stability of the mutualism. Ecol Entomol 26: 602–608.
[17]  Jousselin E, Kjellberg F, Herre EA (2004) Flower specialization in a passively pollinated monoecious fig: a question of style and stigma. Int J Plant Sci 165: 587–593.
[18]  Bronstein JL (1988) Mutualism, antagonism and the fig pollinator interaction. Ecology 69: 1298–1302.
[19]  Nedft RJ, Compton SG (1996) Regulation of seed and pollinator production in the fig-fig wasp mutualism. J Anim Ecol 65: 170–182.
[20]  Herre EA (1989) Coevolution of reproductive characteristics in 12 species of New World figs and their pollinating wasps. Experientia 45: 637–647.
[21]  West SA, Herre SA (1994) The ecology of the New World fig-parasitizing wasps Idarnes and the implication for the evolution of the fig-pollinator mutualism. Proc Biol Sci 258: 67–72.
[22]  Herre EA (1999) Laws governing species interactions? Encouragement and caution from figs and their associates. In: Keller L, editor. Levels of selection in evolution. Princeton (New Jersey): Princeton University Press. pp. 209–237.
[23]  Anstett MC, Bronstein JL, Hossart-McKey M (1996) Resource allocation: a conflict in the fig/fig wasp mutualism. J Evol Biol 9: 417–428.
[24]  Yu DW, Ridley J, Jousselin E, Herre EA, Compton SG, et al. (2004) Oviposition strategies, host coercion and the stable exploitation of figs by their hosts. Proc Biol Sci 271: 1185–1195.
[25]  Kerdelhue C, Rasplus JY (1996) Non-pollinating afrotropical fig wasps affect the fig-pollinator mutualism in Ficus within the subgenus Sycomorus. Oikos 75: 3–14.
[26]  Zhen WQ, Huang JH, Yang DR, Zhu CD, Xiao H (2005) Ovipositor length of three Apocrypta species: effect on oviposition behavior and correlation with syconial thickness. Phytoparasitica 33: 113–120.
[27]  Bronstein JL (1991) The nonpollinating wasp fauna of Ficus pertusa: exploitation of a mutualism. Oikos 61: 175–186.
[28]  Kuttamathiathu JJ (1955) The biology of Philotrypesis caricae (L.), parasite of Blastophaga psenes (L.) (Chalcidoidea: parasitic Hymenoptera). Proc XVth Int Cong Zool 15: 662–664.
[29]  Dixon DJ, Jackes BR, Bielig LM (2001) Figuring out the figs: the Ficus obliqua-Ficus rubiginosa complex (Moraceae: Urostigma sect. Malvanthera). Aust Syst Bot 14: 133–154.
[30]  Weiblen GD (2000) Phylogenetic relationships of functionally dioecious Ficus (Moraceae) based on ribosomal DNA sequences and morphology. Am J Bot 87: 1342–1357.
[31]  Schatz B, Proffit M, Rhaki BV, Borges RM, Hossaert-McKey M (2006) Complex interactions on fig trees: ants capturing parasitic wasps as possible indirect mutualists of the fig/fig wasp interaction. Oikos 113: 344–352.
[32]  Crabb BA, Pellmyr O (2006) Impact of the third trophic level on an obligate mutualism: do yucca plants benefit from parasitoids of their pollinators. Int J Plant Sci 167: 119–124.
[33]  Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398: 701–704.
[34]  Galil J, Eisikowitch D (1968) On the pollination ecology of Ficus sycomorous in East Africa. Ecology 49: 259–269.
[35]  Haine ER, Martin J, Cook JM (2006) Deep mtDNA divergences indicate cryptic species in a fig-pollinating wasp. BMC Evol Biol 6: 83.

Full-Text

comments powered by Disqus