Fig trees (Ficus spp.) are pollinated by tiny wasps that enter their enclosed inflorescences (syconia). The wasp larvae also consume some fig ovules, which negatively affects seed production. Within syconia, pollinator larvae mature mostly in the inner ovules whereas seeds develop mostly in outer ovules—a stratification pattern that enables mutualism persistence. Pollinators may prefer inner ovules because they provide enemy-free space from externally ovipositing parasitic wasps. In some Australasian Ficus, this results in spatial segregation of pollinator and parasite offspring within syconia, with parasites occurring in shorter ovules than pollinators. Australian figs lack non-pollinating fig wasps (NPFW) that enter syconia to oviposit, but these occur in Africa and Asia, and may affect mutualist reproduction via parasitism or seed predation. We studied the African fig, F. burkei, and found a similar general spatial pattern of pollinators and NPFWs within syconia as in Australasian figs. However, larvae of the NPFW Philocaenus barbarus, which enters syconia, occurred in inner ovules. Philocaenus barbarus reduced pollinator abundance but not seed production, because its larvae replaced pollinators in their favoured inner ovules. Our data support a widespread role for NPFWs in contributing to factors preventing host overexploitation in fig-pollinator mutualisms. 1. Introduction Mutualisms are reciprocally beneficial interspecific interactions [1, 2], and a well-known system is that between fig trees (Ficus spp.) and their agaonid wasp pollinators [3–6]. In return for pollination, the wasps gall some fig ovules, which are then eaten by the larvae. About half (300+) of Ficus species are monoecious, where both male flowers and ovules are present in the same syconium (enclosed inflorescence or “fig”). Within monoecious syconia, ovules are highly variable in length [7–10]. Long (inner) ovules have short styles and mature near the centre of the syconium, whereas short (outer), long-styled ovules mature nearer the outer wall (see Figure 1). Female pollinating wasps (foundresses) lay their eggs by inserting their ovipositors down the flower styles. At maturation, wasp galls are clustered at the syconium’s centre [4, 6, 9–13] with seeds at the outer wall. This spatial stratification of pollinating wasps and seeds enables mutualism stability, although the mechanisms preventing the wasps from galling all ovules are unclear. Figure 1: Variation in style and pedicel length in female flowers of monoecious Ficus (adapted from Dunn et al. [ 13]). Mechanisms proposed to
S. A. West, A. S. Griffin, and A. Gardner, “Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection,” Journal of Evolutionary Biology, vol. 20, no. 2, pp. 415–432, 2007.
E. A. Herre, K. C. Jandér, and C. A. Machado, “Evolutionary ecology of figs and their associates: recent progress and outstanding puzzles,” Annual Review of Ecology, Evolution, and Systematics, vol. 39, pp. 439–458, 2008.
K. N. Ganeshaiah, P. Kathuria, R. Uma Shaanker, and R. Vasudeva, “Evolution of style-length variability in figs and optimization of ovipositor length in their pollinator wasps: a coevolutionary model,” Journal of Genetics, vol. 74, no. 1-2, pp. 25–39, 1995.
E. Jousselin, F. Kjellberg, and E. A. Herre, “Flower specialization in a passively pollinated monoecious fig: a question of style and stigma?” International Journal of Plant Sciences, vol. 165, no. 4, pp. 587–593, 2004.
D. W. Yu, J. Ridley, E. Jousselin et al., “Oviposition strategies, host coercion and the stable exploitation of figs by wasps,” Proceedings of the Royal Society B, vol. 271, no. 1544, pp. 1185–1195, 2004.
S. A. West and E. A. Herre, “The ecology of the New World fig-parasitizing wasps Idarnes and implications for the evolution of the fog-pollinator mutualism,” Proceedings of the Royal Society B, vol. 258, no. 1351, pp. 67–72, 1994.
D. W. Dunn, D. W. Yu, J. Ridley, and J. M. Cook, “Longevity, early emergence and body size in a pollinating fig wasp—implications for stability in a fig-pollinator mutualism,” Journal of Animal Ecology, vol. 77, no. 5, pp. 927–935, 2008.
R. W. Wang, J. Ridley, B. F. Sun et al., “Interference competition and high temperatures reduce the virulence of fig wasps and stabilize a fig-wasp mutualism,” PLoS ONE, vol. 4, no. 11, article e7802, 2009.
S. G. Compton and S. van Noort, “Southern African fig wasps (Hymenoptera: Chalcidoidea): resource utilisation and host relationships,” Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, vol. 95, pp. 423–435, 1992.
F. Zhang, Y. Peng, S. G. Compton, Y. Zhao, and D. Yang, “Host pollination mode and mutualist pollinator presence: net effect of internally ovipositing parasite in the fig-wasp mutualism,” Naturwissenschaften, vol. 96, no. 4, pp. 543–549, 2009.
E. Jousselin, M. Hossaert-Mckey, D. Vernet, and F. Kjellberg, “Egg deposition patterns of fig pollinating wasps: implications for studies on the stability of the mutualism,” Ecological Entomology, vol. 26, no. 6, pp. 602–608, 2001.
S. G. Compton, K. C. Holton, V. K. Rashbrook, S. Van Noort, S. L. Vincent, and A. B. Ware, “Studies of Ceratosolen galili, a non-pollinating agaonid fig wasp,” Biotropica, vol. 23, no. 2, pp. 188–194, 1991.
N. R？nsted, G. Salvo, and V. Savolainen, “Biogeographical and phylogenetic origins of African fig species (Ficus section Galoglychia),” Molecular Phylogenetics and Evolution, vol. 43, no. 1, pp. 190–201, 2007.
S. A. West, E. A. Herre, D. M. Windsor, and P. R. S. Green, “The ecology and evolution of the New World non-pollinating fig wasp communities,” Journal of Biogeography, vol. 23, no. 4, pp. 447–458, 1996.
J. M. Cook and S. A. Power, “Effects of within-tree flowering asynchrony on the dynamics of seed and wasp production in an Australian fig species,” Journal of Biogeography, vol. 23, no. 4, pp. 487–493, 1996.
N. R？nsted, G. D. Weiblen, J. M. Cook, N. Salamin, C. A. Machado, and V. Savolainen, “60 million years of co-divergence in the fig-wasp symbiosis,” Proceedings of the Royal Society B, vol. 272, no. 1581, pp. 2593–2599, 2005.