Hosts and their symbionts often have major effects on each other's evolution. Indeed, many symbioses show coevolution of key traits, such as parasite virulence and host resistance and, in some cases, may also manifest cospeciation. A classic example of a coevolved mutualism is provided by the obligate relationship between fig trees (Ficus species) and fig-pollinating wasps (Hymenoptera:Agaonidae). Female wasps enter receptive fig syconia (inflorescences) via a narrow opening called the ostiole, pollinate the flowers and lay their eggs inside developing fig ovules. The fig wasp offspring develop and then mate inside the syconium, before the next generation of females disperses carrying pollen to other, receptive syconia. Agaonid wasps are the only vectors for fig pollen, and fig syconia the only breeding ground for the wasps, making this an obligate association for both partners. As expected, there are clear examples of coadaptation between corresponding fig and pollinator traits (e.g. [1-5]).
There are over 750 species of figs worldwide [6] and most have only one recorded pollinator species [4,7]. Similarly, most wasp species have only one recorded fig host, leading to the famous 1:1 rule of reciprocal partner specificity. Comparisons of the phylogenies of figs and fig wasps support a long history of co-radiation [8] and also show that cospeciation has played a significant role [9]. However, they do not support strict cospeciation, as is found in some symbioses, such as that between aphids and Buchnera bacteria [10]. In addition, recent work has highlighted biases against detecting cases that break the 1:1 specificity rule [11] and revealed many cases where a single fig species hosts two (or occasionally more) pollinator species [12-15]. It now appears that a substantial minority of fig species have two or more co-pollinators [11,15]. In some cases, they are largely allopatric, but in many they coexist in sympatry [11,12,15].
In some cases, co-pollinators have been identified during taxonomic revisions following extended field sampling [13], while in others they were initially identified via surprising patterns of genetic variation within what was thought to be a single wasp species [14]. Regardless of how they are identified, co-pollinators have important consequences. First, they change our view of host specificity and make coevolutionary dynamics more complex [11,14,15]. Second, their coexistence in the same specialised niche poses a problem for ecological competition theory [16]. Third, fig wasps provide a model system for sex ratio studies and past work has involved accidental pooling of members of two species [14,17].
The occurrence of co-pollinators raises the question of how they evolved. They may be sister species that speciated on the current host plant, or less closely related because one underwent a host-shift from another fig species. While host-shifting has been important in the radiation of many herbivorous insect taxa (e.g. [18-20]), it is less clear how a fig-pollinating wasp might speciate without a host-shift or host plant speciation event. One potentially important agent is Wolbachia, an alpha-proteobacterium that often causes reproductive incompatibilities between infected and uninfected hosts, or between populations with different mutually incompatible infections. In theory, these can facilitate – or even cause – host speciation [21-25]. Fig-pollinating wasps have the highest known incidence of Wolbachia infection for any insect taxon with ca. 70% of Australian and Panamanian species harbouring infections [26,27]. Interestingly, we have previously detected variation in infection status in the fig wasp Pleistodontes imperialis during a wide survey of fig wasp species [27].
Most previous studies of fig/pollinator specificity have been either general literature surveys [7,28,29], or detailed studies of a few species at one or a few sites (e.g. [13,14]). These, respectively, revealed geographic variation in pollinator species and local coexistence of alternative pollinators. Here, we combined these two approaches by studying one fig species (Ficus rubiginosa) with a large geographic range, and collecting many fig-pollinating wasps (Pleistodontes imperialis) from several sites across that range. We used sequences from four different genetic markers – one mitochondrial (cytochrome b) and two nuclear (28S and wingless) wasp genes and one Wolbachia (wsp) gene to explore the genetic variation in P. imperialis across the large geographic range of its host plant.
Ficus rubiginosa occurs naturally along the Eastern Coast of Australia (roughly 2500 km North-South and up to 200 km inland) and is found in diverse habitats, including rainforest, granite outcrops and rocky coastal areas (Fig. 1; [30]). It is also commonly planted in parks and there are introduced populations in other parts of Australia (e.g. Adelaide and Melbourne), as well as in New Zealand [31], Hawaii [32], California and Mediterranean Europe (JMC, pers. obs.). In a recent taxonomic revision of species in Ficus section Malvanthera, F. rubiginosa was considered to have two forms with one difference: form rubiginosa has leaves that are variously hairy, while form glabrescens [30] lacks hairs. However, individual leaves of form rubiginosa may also lack hairs. Form rubiginosa has a natural distribution from Cape York down the East Coast of Australia to Southern New South Wales (NSW), while form glabrescens has the same northern distribution, but does not extend south into NSW (Fig. 1). Only one pollinator wasp species, Pleistodontes imperialis, has been recorded, despite extensive sampling and a recent taxonomic revision of the wasp genus [13], which led to the description of four new Pleistodontes species from other fig species. Most P. imperialis females are black, but a yellow form is found around Townsville in N. Queensland. Morphological analysis revealed no clear differences, except for colour, and they are considered to be the same species [13]. Pleistodontes imperialis has not been recorded from any other fig species [13].
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