We have produced the most comprehensive phylogeny of figs to date and this supports the idea that section Pharmacosycea is the oldest section in the genus. With a dense taxon sampling, our phylogenetic analyses support the monophyly of most fig sections, especially within the monoecious subgenera Urostigma and Pharmacosycea. With over 750 species, Ficus is a large genus, and more detailed studies of phylogenetic patterns and evolutionary processes in the fig–wasp interaction should focus on smaller, more manageable subsets of species such as sections of the genus. Knowing the monophyly of a group of figs is a prerequisite for evaluating possible co-speciation in the mutualism. Not all clades are well supported in our analysis and future molecular systematic work should focus on the relationship between monoecious and dioecious figs (particularly the relationships of sections Urostigma and Oreosycea) and the sectional classification of dioecious figs.
Two previous molecular studies have estimated the date of origin of figs and their pollinating wasp. Machado et al. (2001)
obtained an age interval of 75–100
Myr for the crown group of the wasps, a date that is older than available fossil evidence of Ficus
by at least 15
Myr. More recently, Datwyler & Weiblen (2004)
used three calibration points to date their phylogenetic tree of Moraceae based on ndhF
sequences of over 80 taxa representing 33 genera. They obtained an estimate of 83
Myr for the root node of Ficus
. We obtained confidence intervals of 98–105
Myr for the age of the root node of Ficus
and 66–101 for the age of the root node of the wasps. The crown group of Ficus
was constrained to 60
Myr by a fossil achene, and for the crown group of the wasps we obtained a confidence interval of 51–78
Myr (). Our results confirm previously published dates suggesting a time frame of 60–100
Myr ago for the origin of the fig–wasp association. However, the use of fossils for dating yields minimum age estimates, because the fossil record may not coincide with the earliest appearance. Confirmation of these dates could be given by analysing whether they are compatible with biogeographic scenarios for Ficus
(see Machado et al. 2001
; Zerega et al. in press
). If the age estimates we have obtained are correct, this could imply long distance oceanic dispersal being an important process explaining the present distribution of Ficus
. For instance, the south American section Pharmacosycea
would have separated from the rest of the figs only 60 million years ago (node 2 on ), which post-dates the separation of South America from Africa (about 90–100
Myr ago) during the break up of Gondwana. Likewise, the American section Americana
and the African section Galoglychia
would have separated around 40–50 million years ago (node 7 on ).
Phylogenetic double-dating has so far only been used to evaluate co-speciation between parasitic psyllids (Hemiptera) and their hosts in the genistoid legumes (Genisteae; Percy et al. 2004
). The authors found that all but one of the putative co-speciation events were in fact asynchronous, indicating that the psyllids colonized hosts that had already diversified rather than co-speciating contemporaneously with their hosts. By comparison, the fig-pollinating wasp system exhibits strong evidence for co-diversification in at least 10 interacting lineages.
Coevolution between mutualistic partners and between hosts and parasites is a long-held hypothesis, but the prevalence of coevolution between interacting taxa is unknown, largely because only a small number of associations have been studied in sufficient detail to document long-term coevolution.
The best-documented case is that between pocket gophers (Geomyidae) and their chewing lice (Phthiraptera; see Hafner et al. 2003
and references therein). Independent phylogenies of host and parasite lineages, based on sequences of the mitochondrial cox1
gene, show significant congruence both at high-taxonomic levels and within genera. Although lice may be transmitted horizontally between individuals, such dispersal relies on host-to-host contact, which is almost exclusively intraspecific among gophers. Other biological aspects, such as hair diameter, may also restrict the suitability of other potential host species for dispersing lice. Consequently, Hafner and co-workers suggest that the pattern of co-cladogenesis results primarily from lack of opportunity to colonize new host species.
Another classic system is the obligate pollination mutualism between the yucca (Agavaceae) and the yucca moth (Lepidoptera; Pellmyr 2003
), but no analysis of parallel cladogenesis has yet been conducted due to the lack of phylogenetic estimates for the host plants.
In addition, an obligate pollination mutualism between Glochidion
trees (Phyllantaceae) and Epicephala
moths (Gracillariidae) was recently described (Kato et al. 2003
). Several different methods for investigating the level of co-cladogenesis between phylogenies indicated that there is a greater degree of correlation between the Glochidion
phylogenetic trees than expected in a random association (Kawakita et al. 2004
). Coevolution with pollinators has also been suggested in Phyllanthus
, another genus in Phyllantaceae (Kawakita & Kato 2004
Likewise for palms, a diversity of insect pollination mutualisms have been described (Henderson 1986
), but not yet studied in a phylogenetic framework.
All of these systems show deviations from perfect phylogenetic congruence, which could be due to host-shifting, independent speciation and/or extinction events, and error associated with phylogeny estimation. A number of studies have provided evidence that various hemipteran insect taxa, such as mealybugs (Baumann & Baumann 2005
), white flies (Thao & Baumann 2004
) and their primary bacterial endosymbionts, share phylogenetic histories. These systems tend to show perfect congruence, but this is consistent with a single infection of the hosts with an ancestor of the endosymbionts followed by vertical transmission. Other studies have simply failed to demonstrate coevolution between associated partners. For instance, Desdevises et al. (2002)
found that host–parasite associations between Sparidae
(Teleostei) fishes and their parasites of the genus Lamellodiscus
(Monogenea) were due more to ecological factors than to coevolutionary processes.
Molecular dating showed that the yucca–yucca moth association arose at least 40 million years ago (Pellmyr 2003
) and long-term co-divergence was recently reported for Simian foamy RNA viruses and old World primates (Switzer et al. 2005
). The phylogenetic trees were remarkably congruent in both branching order and divergence times over 30 million years, strongly supporting co-speciation in this host–parasite system.
The strength of the relationship between the independently inferred ages of closely associated fig and pollinator lineages in the present study provides the most compelling evidence to date for long-term co-divergence in this now classical mutualism during at least the past 60 million years. Having established a scenario of parallel diversification of fig and wasp lineages, future studies should focus on the extent of co-speciation in the fig–wasp symbiosis based on manageable monophyletic groups of figs in comparison with the associated pollinators as exemplified by Weiblen & Bush (2002)
and the pollinating wasps of the genus Ceratosolen
. Another promising line of investigation would be to examine whether the dates obtained in the present study are compatible with biogeographic scenarios and dates obtained for other groups and what implications these dates have for explaining the present distribution of figs and fig pollinators.