The chalcidoid wasp family Agaonidae includes nearly four hundred described species, all of which have intimate mutualistic relationships with Ficus figs (of which there are around 800 described species). As now commonly defined (i.e., excluding the non-pollinating fig wasps; Rasplus et al. 1998; Munro et al. 2011), the family Agaonidae is monophyletic (i.e., the group is descended from a single common ancestor and includes all lineages descended from that ancestor). Both figs and fig-pollinating wasps occur mainly in tropical and subtropical areas of the southern hemisphere. Fig wasp diversity varies geographically, with the Asian and Australasian regions harboring the highest species richness. Figs and their wasp pollinators provide extraordinary opportunities to investigate fundamental questions in evolution and ecology relating to coevolution, speciation, and the evolution and maintenance of mutualisms. Both the figs and their pollinating wasps are completely dependent on each other for survival and reproduction: figs can only be pollinated by fig wasps and fig wasps can only reproduce within figs. (Most commercial figs are parthenocarpic, requiring no fertilization, and hence no pollination at all, to produce fruit, and this phenomenon is sometimes seen in some wild fig species as well. See Kislev et al. 2006 a,b;Lev-Yadun et al. 2006.)
These tiny wasps are closely associated with the unusual fig inflorescence, an enclosed receptacle known as a syconium, which isa hollow sphere lined with hundreds of tiny flowers.One or more female pollinator wasps enter the fig through a small pore (the ostiole) and pollinate the flowers, laying eggs in some of them, and then (typically) die inside the fig. Pollinator wasp larvae develop in galls within the flowers, each consuming the contents of one would-be seed. After becoming adults, pollinator offspring then mate within the syconium and the females fly to another fig to oviposit and pollinate. Emerging males chew holes in galls containing the females and their telescopic abdominal segments are curled beneath the body so that the genitalia may be inserted into the galls. Unlike the females (which must travel to find a new host on which to lay eggs), male pollinator wasps are wingless (typically with vestigial eyes, antennae, and tarsi) and have highly specialized mouth parts for chewing females out of their galls, fighting with other males, and, most importantly, for chewing an exit tunnel for the inseminated female wasps to leave the syconium.
Although it was once believed that there was a strict one-to-one relationship between each Ficus fig species and a corresponding agaonid pollinator, it is now apparent that fig wasps have frequently colonized new species of figs to the point that many (possibly most) fig species are pollinated by more than one wasp species. In other cases, pollinator lineages have apparently diverged into two species on a single host species.The most common (although by no means the only) deviation from one-to-one specificity is the situation in which two pollinator taxa are geographically isolated across the host range. Given that interspecific hybridization and introgression appear to be widespread among figs, Machado et al. (2005) suggested that the best model for understanding the evolutionary dynamics of the fig-fig wasp mutualism is one in which groups of genetically well defined species of wasps coevolve with groups of genetically less well defined (frequently hybridizing) groups of figs.
Two major modes of fig pollination may be distinguished by differences in wasp behavior and morphology. Actively pollinating species remove pollen they have collected in special thoracic pollen pockets with their forelegs, depositing it on the stigmatic surface of the flower when laying eggs in a fraction of fig flowers. In contrast, passively pollinating species do not have functional pollen pockets or active pollination behavior and pollen is transported on the abdomen instead.
In monoecious fig species (i.e., those in which each individual tree functions as both a female and a male), all syconia are essentially the same and produce both seeds and pollen-dispersing wasps. In the case of functionally dioecious fig species (i.e., those in which different individual trees function as either males or females), female pollinator wasps are attracted to both gall and seed figs and pollinate both types, but their offspring only develop in gall figs (the seed figs produce only seeds, no wasps). Gall figs are functionally “male” because they yield the wasp larvae that disperse fig pollen as adults.Ovules that would otherwise produce seed instead serve to nourish wasp offspring. On the other hand, seed figs (which contain no male flowers) are functionally “female” because the styles are too long for the wasp ovipositors to reach the ovules, so viable seeds result from pollination. Conservative estimates suggest that fig wasps routinely disperse pollen over distances of over 10 km and that breeding populations of figs constitute hundreds of individuals spread over areas more than 100 square km.
Nonpollinators are also important components of fig wasp communities, having negative impacts on the mutualism. Three distinct guilds of nonpollinators have been identified: gall makers that attack figs from the exterior, gall makers that enter figs as do the pollinators, and parasitoids that attack other fig wasp larvae. Parasitoids have extraordinarily long ovipositors that are capable of piercing the fig receptacle.
(Weiblen 2002; Cook and Rasplus 2003; Machado et al. 2005; Marussich and Machado 2007 and references therein; Zavodna et al. 2007 and references therein; Lopez-Vaamonde et al. 2009; Moe et al. 2011)
The family Agaonidae is a group of pollinating and nonpollinating fig wasps. They spend their larval stage inside the fruits of figs. The pollinating wasps (Agaoninae, Kradibiinae, and Tetrapusiinae) are the mutualistic partners of the fig trees. The nonpollinating fig wasps are parasitic.
The family has changed several times since its taxonomic appearance after the work of Francis Walker in 1846 described from the wasp genus Agaon. For long the subfamilies Epichrysomallinae, Otitesellinae, Sycoecinae, Sycoryctinae, Sycophaginae, and Agaoninae were the subdivisions of the family. Recent works building strong molecular phylogenies with an extended sampling size have changed the composition of Agaonidae. First, the paraphyletic groups have been excluded (Epichrysomallinae, Otitesellinae, Sycoecinae, and Sycoryctinae) and new subfamilies have been instated (Kradibiinae and Tetrapusiinae). Then the subfamily Sycophaginae have been placed within the family Agaonidae. Within the Sycophaginae, some changes were made after the molecular phylogeny of the subfamily: the genus Apocryptophagus has been synonymined under the genus Sycophaga.
Wasps from the three subfamilies Agaoninae, Kradibiinae and Tetrapusiinae are pollinating fig wasps. On the other hand, Sycophaginae are parasites of the Ficus, developing in the fruits after other wasps have pollinated them. Nevertheless, some species in the genus Sycophaga have a controversial status; as they enter the fig by its ostiole, they possibly bring pollen inside the fig and might pollinate it.
The pollinating female fig wasps are winged and in general dark, while the males are mostly wingless and whitish. This difference of color is probably due to a clear split in the gender role. Once they have mated, male and female fig wasps have different fates. In some fig species, such as Ficus subpisocarpa or Ficus tinctoria, the males have to chew a hole for the females to leave their natal fig. The winged female wasps can fly over long distances before finding another fig to oviposit in it, while the male dies after chewing a hole. As the fig is closed by a tight ostiole, the female wasps have developed adaptations to enter. First, the mandibles of the female wasps have developed specialized mandibular appendages to help them crawl into the figs. These appendages are adapted to the host fig species, with for instance spiraled ostioles matched by spiral mandibular appendages. The nonpollinating wasps also have developed impressive morphological adaptations to deposit eggs inside the fig from the outside, in the form of an extremely long ovipositor.