Diversification and spatial structuring in the mutualism between Ficus septica and its pollinating wasps in insular South East Asia

Abstract

BackgroundInterspecific interactions have long been assumed to play an important role in diversification. Mutualistic interactions, such as nursery pollination mutualisms, have been proposed as good candidates for diversification through co-speciation because of their intricate nature. However, little is known about how speciation and diversification proceeds in emblematic nursery pollination systems such as figs and fig wasps. Here, we analyse diversification in connection with spatial structuring in the obligate mutualistic association between Ficus septica and its pollinating wasps throughout the Philippines and Taiwan.Results Ceratosolen wasps pollinating F. septica are structured into a set of three vicariant black coloured species, and a fourth yellow coloured species whose distribution overlaps with those of the black species. However, two black pollinator species were found to co-occur on Lanyu island. Microsatellite data on F. septica indicates the presence of three gene pools that broadly mirrors the distribution of the three black clades. Moreover, receptive fig odours, the specific message used by pollinating wasps to locate their host tree, varied among locations.Conclusions F. septica and its black pollinator clades exhibited similar geographic structuring. This could be due originally to geographic barriers leading to isolation, local adaptation, and finally co-structuring. Nevertheless, the co-occurrence of two black pollinator species on Lanyu island suggests that the parapatric distribution of the black clades is now maintained by the inability of migrating individuals of black pollinators to establish populations outside their range. On the other hand, the distribution of the yellow clade strongly suggests an initial case of character displacement followed by subsequent range extension: in our study system, phenotypic or microevolutionary plasticity has allowed the yellow clade to colonise hosts presenting distinct odours. Hence, while variation in receptive fig odours allows specificity in the interaction, this variation does not necessarily lead to coevolutionary plant-insect diversification. Globally, our results evidence evolutionary plasticity in the fig-fig wasp mutualism. This is the first documentation of the presence of two distinct processes in pollinating fig wasp diversification on a host species: the formation of vicariant species and the co-occurrence of other species over large parts of their ranges probably made possible by character displacement.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-1034-8) contains supplementary material, which is available to authorized users.

Multiple parapatric pollinators have radiated across a continental fig tree displaying clinal genetic variation

“…More extensive sampling and molecular techniques that have facilitated separation of morphologically close (“cryptic”) species have revealed an increasing number of Ficus species with several pollinators (Darwell et al, ). However, we still know little about how genetic diversity is structured within Ficus species and how this is related to the distributions and genetic diversity among the fig wasp pollinators that it supports (Bain et al, ; Rodriguez et al, ; Wachi et al, ). Where several pollinator species share a single Ficus host, they are generally sister species (Yang et al, ).…”

“…More localized differentiation is evident among island populations of Ficus septica Burm. f., in the Philippines (Conchou, Cabioch, Rodriguez, & Kjellberg, ; Lin, Yeung, Fong, Tzeng, & Li, ; Rodriguez et al, ), and along elevation gradients (Segar et al, ; Souto‐Vilarós et al, ), where several different pollinators are present.…”

Sky islands as foci for divergence of fig trees and their pollinators in southwest China

“…Fig wasp colonization events followed by host switches have been reported among Ficus species (Wachi, Kusumi, Tzeng, & Su, ), but the northern, montane distribution of F. tikoua means that there is little range overlap with other Ficus species and fewer opportunities for host switching than would be the case for a tropical species. It is more common for fig wasps that share a host Ficus to be “cryptic” species that are difficult to tell apart morphologically (Chen et al, ; Darwell, Al‐Beidh, & Cook, ; Darwell & Cook, ; Rodriguez et al, ; Segar et al, ; Wachi et al, ; Wang, Cannon, & Chen, ; Yu, Tian, et al, ). They are typically sister species that have diverged during the history of their association with the plant (Souto‐Vilaros et al, ; Wang et al, ; Yang et al, ; Yu, Tian, et al, ).…”

“…However, caution is required regarding ages and any dates are very tentative. Despite this, a maximum difference of only 2.24% has accumulated in the pollinators of F. tikoua , compared with nucleotide differences of 7.2%–7.8% in the pollinators of F. septica (Lin, Yeung, & Li, ; Rodriguez et al, ). The deep divergence with less accumulation of variation suggests that large effective population sizes have persisted in Ceratosolen sp., which may reflect the high densities that F. tikoua populations can achieve.…”

Inferring Processes of Coevolutionary Diversification in a Community of Panamanian Strangler Figs and Associated Pollinating Wasps

“…They are capable dispersers, traveling many kilometers in search of a receptive fig (Nason et al 1998), with some species of fig wasps having been recorded dispersing over 160 km (Ahmed et al 2009). Many fig species have broad distributions, and in cases where pollinators have been sampled from throughout their range, multiple pollinator species have been found, typically in different geographic areas (e.g., Haine et al 2006;Chen et al 2012;Bain et al 2016;Rodriguez et al 2017). For example, Darwell et al (2014) explored pollinator species diversity on Ficus rubiginosa distributed from northern Queensland to New South Wales in Australia.…”