3. There is impressive morphological co-evolution between figs and fig wasps and this, combined with a high degree of partner specificity, led to the expectation that figs and pollinators have cospeciated extensively. Comparison of deep phylogenies supports long-term codivergence of figs and pollinators, but also suggests that some host shifts have occurred.4. Phylogenies of more closely related species do not match perfectly and may even be incongruent, suggesting significant roles for processes other than strict cospeciation. Combined with recent evidence on host specificity patterns, this suggests that pollinator wasps may often speciate by host shifts between closely related figs, or by duplication (the wasp speciates but the fig doesn't). The frequencies and biological details of these different modes of speciation invite further study.5. Far less is known about speciation in non-pollinating fig wasps. Some lineages have probably co-evolved with figs and pollinators for most of the evolutionary history of the symbiosis, while others appear to be more recent colonisers. Many species appear to be highly host-plant specific, but those that lay eggs through the fig wall without entering the syconium (the majority of species) may be subject to fewer constraints on host shifting than pollinators. There is evidence for substantial host shifting in at least one genus, but also evidence for ecological speciation on the same host plant by niche shifts in other cases.6. Finally, recent work has begun to address the issue of 'community phylogeny' and provided evidence for long-term co-divergence of multiple pollinating and nonpollinating wasp lineages with their host figs.
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.
Escalation (macroevolutionary increase) or divergence (disparity between relatives) in trait values are two frequent outcomes of the plant-herbivore arms race. We studied the defences and caterpillars associated with 21 sympatric New Guinean figs. Herbivore generalists were concentrated on hosts with low protease and oxidative activity. The distribution of specialists correlated with phylogeny, protease and trichomes. Additionally, highly specialised Asota moths used alkaloid rich plants. The evolution of proteases was conserved, alkaloid diversity has escalated across the studied species, oxidative activity has escalated within one clade, and trichomes have diverged across the phylogeny. Herbivore specificity correlated with their response to host defences: escalating traits largely affected generalists and divergent traits specialists; but the effect of escalating traits on extreme specialists was positive. In turn, the evolution of defences in Ficus can be driven towards both escalation and divergence in individual traits, in combination providing protection against a broad spectrum of herbivores.
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