Dataset Information

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

ABSTRACT:

Background

Interspecific 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.

SUBMITTER: Rodriguez LJ

PROVIDER: S-EPMC5576367 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

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

Rodriguez Lillian Jennifer LJ Bain Anthony A Chou Lien-Siang LS Conchou Lucie L Cruaud Astrid A Gonzales Regielene R Hossaert-McKey Martine M Rasplus Jean-Yves JY Tzeng Hsy-Yu HY Kjellberg Finn F

BMC evolutionary biology 20170829 1

<h4>Background</h4>Interspecific 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 ...[more]

PMID: 28851272

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Project description:BACKGROUND:Biotic interactions are ubiquitous and require information from ecology, evolutionary biology, and functional genetics in order to be understood. However, study systems that are amenable to investigations across such disparate fields are rare. Figs and fig wasps are a classic system for ecology and evolutionary biology with poor functional genetics; Caenorhabditis elegans is a classic system for functional genetics with poor ecology. In order to help bridge these disciplines, here we describe the natural history of a close relative of C. elegans, Caenorhabditis inopinata, that is associated with the fig Ficus septica and its pollinating Ceratosolen wasps. RESULTS:To understand the natural context of fig-associated Caenorhabditis, fresh F. septica figs from four Okinawan islands were sampled, dissected, and observed under microscopy. C. inopinata was found in all islands where F. septica figs were found. C.i nopinata was routinely found in the fig interior and almost never observed on the outside surface. C. inopinata was only found in pollinated figs, and C. inopinata was more likely to be observed in figs with more foundress pollinating wasps. Actively reproducing C. inopinata dominated early phase figs, whereas late phase figs with emerging wasp progeny harbored C. inopinata dauer larvae. Additionally, C. inopinata was observed dismounting from Ceratosolen pollinating wasps that were placed on agar plates. C. inopinata was not found on non-pollinating, parasitic Philotrypesis wasps. Finally, C. inopinata was only observed in F. septica figs among five Okinawan Ficus species sampled. CONCLUSION:These are the first detailed field observations of C. inopinata, and they suggest a natural history where this species proliferates in early phase F. septica figs and disperses from late phase figs on Ceratosolen pollinating fig wasps. While consistent with other examples of nematode diversification in the fig microcosm, the fig and wasp host specificity of C. inopinata is highly divergent from the life histories of its close relatives and frames hypotheses for future investigations. This natural co-occurrence of the fig/fig wasp and C. inopinata study systems sets the stage for an integrated research program that can help to explain the evolution of interspecific interactions.

Project description:Local mate competition (LMC) favours female biased clutch sex ratios because it reduces competition between brothers and provides extra mating opportunities for sons. Fig wasps seem to fit LMC model assumptions and lay female-biased sex ratios as predicted. These female biased sex ratios increase fitness greatly. In line with predictions, their sex ratios become less female-biased as the number of mothers laying in the same fig increases. However, this variation results in comparatively small fitness benefits compared to just biased ratios and data suggest substantial mismatches with LMC theory. The mismatches are due to several factors. (1) Multiple foundresses typically lay too many daughters. (2) Single foundress sex ratios are explained by sequential oviposition and ladies-last models. (3) Mortality that typically exceeds 10% may decouple the link between primary sex ratios, the focus of model predictions, and secondary sex ratios of adult wasps that are counted by researchers. (4) Model assumptions are frequently violated: (a) clutch sizes are unequal, (b) oviposition may not be simultaneous (c) cryptic/multiple wasp species inhabit the same host, (d) foundress numbers are systematically undercounted, (e) inbreeding coefficient calculations are inaccurate, and (f) male wasps sometimes disperse. These data and calculations suggest that alternative explanations must be considered seriously. Substantial data show that wasps typically lay most of their male eggs first followed by mostly female eggs require a new approach. These "slope" strategies result in more accurate sex ratios that are automatically adjusted to foundress number, own and relative clutch sizes and to sequential clutches. This effect will alter sex ratios in all species once the egg capacity of a fig is crossed or when interference reduces clutch sizes. In addition to this passive response, the females of about half the studied species have a conditional response that reduces female bias under higher foundress numbers by laying more sons. Therefore, wasps seem to use a very simple strategy that increases their fitness. Natural selection could have optimized parameters of the slope strategy and possibly the existence of the slope strategy itself. Variation in the slope strategy that is the result of natural selection is adaptive. Research should therefore focus on quantifying variables of this slope strategy. Currently, it is unclear how much of the variation is adaptive as opposed to being coincidental by-products.

Project description:It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant-insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by >750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale cophylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on an average, wasps had sequences from 77% of 6 genes (5.6 kb), figs had sequences from 60% of 5 genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based cophylogenetic analyses further support the codiversification hypothesis. Biogeographic analyses indicate that the present-day distribution of fig and pollinator lineages is consistent with a Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant-insect interactions of coordinated dispersal and long-term codiversification. [Biogeography; coevolution; cospeciation; host switching; long-branch attraction; phylogeny.].

Dataset Information

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

Background

Results

Conclusions

Publications

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

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