Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism

Abstract

Figs (Ficus spp., Moraceae) and their pollinating wasps (Agaonidae, Chalcidoidea) constitute perhaps the most tightly integrated pollination mutualism that is known. Figs are characterized by extraordinarily high global and local species diversity. It has been proposed that the diversification of this mutualism has occurred through strict-sense coadaptation and cospeciation between pairs of fig and wasp species that are associated in highly specific one-to-one relationships. However, existing studies cast doubt on the generality of this proposition. Here, we review our current knowledge of the evolutionary history of the fig͞fig-wasp mutualism. We critically examine the idea that codivergence between figs and their pollinators has been dominated by strict-sense cospeciation. We present phylogenetic and population genetic data from neotropical fig and fig wasp species that suggest that a more accurate model for diversification in this mutualism is that of groups of genetically well defined wasp species coevolving with genetically less well defined (frequently hybridizing) groups of figs. Last, we use our results to assess previously proposed hypotheses on models of speciation in this mutualism.

Comparative Dating of Attine Ant and Lepiotaceous Cultivar Phylogenies Reveals Coevolutionary Synchrony and Discord

“…However, most mutualistic symbioses involve complex patterns of interactions among multiple species pools rather than pairwise specialization (Borowicz and Juliano 1991;Bruns et al 2002;Clay and Schardl 2002;Thompson 2005;Ollerton 2006;Herre et al 2008). Less intimate symbioses characterized by host sharing or symbiont switching frequently produce intricate patterns of complete or partial discord between symbiont phylogenies (e.g., termites and their fungal cultivars [Aanen et al 2002], figs and fig wasps [Machado et al 2005;Herre et al 2008;Jackson et al 2008], yucca moths and yucca [Smith et al 2008], squid and their bioluminescent symbionts [Dunlap et al 2007], lichen symbioses [Piercey-Normore and DePriest 2001;Rikkinen et al 2002], and mycorrhizal symbioses [Bidartondo 2005;Shefferson et al 2007]). A major goal of current efforts is to understand the coevolutionary dynamics of complex mutualistic interactions (Ollerton 2006;Guimarães et al 2007;Jousselin et al 2008).…”

Mutualism favours higher host specificity than does antagonism in plant–herbivore interaction

“…In addition, fig herbivores in general are dominated by insects that feed on several locally available fig hosts (Novotny et al 2002(Novotny et al , 2006. Given that shared pollinators can result in hybridization among closely related, co-occurring figs (Machado et al 2005), selection may favour figs relying on specialist pollinators to achieve effective conspecific pollination. Thus, these observations indicate that pollinating seed parasites may in fact attain a higher degree of host specificity than that of their parasitic ancestors owing to coevolutionary selection arising after the evolution of pollination mutualism.…”

Symbiont fidelity and the origin of species in fungus-growing ants

“…Mutualists can be tightly integrated, resulting in coadaptation and cospeciation (that is, speciation in one partner results in simultaneous speciation in the other), or 'diffusely' associated because of frequent host switching. Diffuse coevolution has been proposed to occur in a variety of mutualisms, such as those between figs and fig-wasp pollinators 4,8,9 , squids and their bioluminescent bacterial symbionts 10 , and fungus-growing insects and their cultivated fungi [11][12][13][14][15][16][17] .…”