Plant geographic phenotypic variation drives diversification in its associated community of a phytophagous insect and its parasitoids

International audienceBackground: While the communities constituted by phytophageous insects and their parasites may represent half of all terrestrial animal species, understanding their diversification remains a major challenge. A neglected idea is that geographic phenotypic variation in a host plant may lead to heterogeneous evolutionary responses of the different members of the associated communities. This could result in diversification on a host plant by ecological speciation in some species, leading to geographic variation in community composition. In this study we investigated geographic variation of inflorescence receptacle size in a plant, Ficus hirta, and how the hymenopteran community feeding in the inflorescences has responded. Our predictions were:1) Inflorescence size variation affects wasp species differently depending on how they access oviposition sites.2) In some affected lineages of wasps, we may observe vicariant, parapatric species adapted to different inflorescence sizes.Results: We show that fig (the enclosed inflorescence of Ficus) wall thickness varies geographically. The fig-entering pollinating wasp was not affected, while the parasites ovipositing through the fig wall were. Two parapatric species of Philotrypesis, exhibiting strikingly different ovipositor lengths, were recorded. One species of Sycoscapter was also present, and it was restricted, like the shorter-ovipositor Philotrypesis, to the geographic zone where fig walls were thinner.Conclusions: Previous work on fig wasps suggested that parapatric geographic ranges among congenerics were due to adaptation to variation in abiotic factors, complemented by interspecific competition. Our results show that parapatric ranges may also result from adaptation to variation in biotic factors. Within an insect community, differences among species in their response to geographic phenotypic variation of their host plant may result in geographically heterogeneous community structure. Such heterogeneity leads to heterogeneous interaction networks among sites. Our results support the hypothesis that plant geographic phenotypic variation can be a driver of diversification in associated insect communities, and can complement other diversification processes

Cyto-nuclear discordance in the phylogeny of Ficus section Galoglychia and host shifts in plant-pollinator associations

<p>Abstract</p> <p>Background</p> <p>Hybridization events are relatively common in vascular plants. However, the frequency of these events is unevenly distributed across the plant phylogeny. Plant families in which individual species are pollinated by specific pollinator species are predicted to be less prone to hybridization than other families. However, exceptions may occur within these families, when pollinators shift host-plant species. Indeed, host shifts are expected to increase the rate of hybridization events. Pollinators of <it>Ficus </it>section <it>Galoglychia </it>are suspected to have changed host repeatedly, based on several cases of incongruence between plant phylogeny and taxonomy, and insect phylogeny and taxonomy. We tracked cyto-nuclear discordance across section <it>Galoglychia </it>as evidence for hybridization. To achieve a proper global view, we first clarified the monophyly of section <it>Galoglychia </it>as it had been questioned by recent phylogenetic studies. Moreover, we investigated if fig size could be a factor facilitating host shifts.</p> <p>Results</p> <p>Phylogenetic chloroplast and nuclear results demonstrated the monophyly of section <it>Galoglychia</it>. Within section <it>Galoglychia</it>, we detected several cases of statistically significant cyto-nuclear discordance. Discordances concern both terminal nodes of the phylogenetic trees and one deep node defining relationships between subsections. Because nuclear phylogeny is congruent with morphological taxonomy, discordances were caused by the chloroplast phylogeny. Introgressive hybridization was the most likely explanation for these discordances. We also detected that subsections pollinated by several wasp genera had smaller figs and were pollinated by smaller wasps than subsections pollinated by a single wasp genus.</p> <p>Conclusion</p> <p>As hypothesized, we discovered evidences of past hybridization in <it>Ficus </it>section <it>Galoglychia</it>. Further, introgression was only detected in subsections presenting incongruence between plant and pollinator phylogenies and taxonomy. This supports the hypothesis that host shift is the cause for plant-pollinator incongruence. Moreover, small fig size could facilitate host shifts. Eventually, this study demonstrates that non-coding chloroplast markers are valuable to resolve deep nodes in <it>Ficus </it>phylogeny.</p

Traditional agroecosystems as conservatories and incubators of cultivated plant varietal diversity: the case of fig (Ficus carica L.) in Morocco

<p>Abstract</p> <p>Background</p> <p>Traditional agroecosystems are known to host both large crop species diversity and high within crop genetic diversity. In a context of global change, this diversity may be needed to feed the world. Are these agroecosystems museums (i.e. large core collections) or cradles of diversity? We investigated this question for a clonally propagated plant, fig (<it>Ficus carica</it>), within its native range, in Morocco, but as far away as possible from supposed centers of domestication.</p> <p>Results</p> <p>Fig varieties were locally numerous. They were found to be mainly highly local and corresponded to clones propagated vegetatively. Nevertheless these clones were often sufficiently old to have accumulated somatic mutations for selected traits (fig skin color) and at neutral loci (microsatellite markers). Further the pattern of spatial genetic structure was similar to the pattern expected in natural population for a mutation/drift/migration model at equilibrium, with homogeneous levels of local genetic diversity throughout Moroccan traditional agroecosystems.</p> <p>Conclusions</p> <p>We conclude that traditional agroecosystems constitue active incubators of varietal diversity even for clonally propagated crop species, and even when varieties correspond to clones that are often old. As only female fig is cultivated, wild fig and cultivated fig probably constitute a single evolutionary unit within these traditional agroecosystems. Core collections, however useful, are museums and hence cannot serve the same functions as traditional agroecosystems.</p

Pollinating fig wasps’ simple solutions to complex sex ratio problems : a review

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 ft LMC model assumptions and lay femalebiased sex ratios as predicted. These female biased sex ratios increase ftness greatly. In line with predictions, their sex ratios become less female-biased as the number of mothers laying in the same fg increases. However, this variation results in comparatively small ftness benefts 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 coefcient 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 frst 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 efect will alter sex ratios in all species once the egg capacity of a fg 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 ftness. 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.SUPPLEMENTARY INFORMATION: ADDITIONAL FILE 1. Supplementary text and figures. Explanation of methods, derivation of ESS sex ratio, analysis of wasp size and supplementary figures. ADDITIONAL FILE 2. Figure 4 data. Observed (± 95% CI) and expected sex ratios in 36 studies of 25 species. ADDITIONAL FILE 3. Figures 8 and 9 data. Clutch composition in 33 studies on 25 species. ADDITIONAL FILE 4. Figure 10 data. Single Foundress sex ratios, fraction of single foundress figs and clutch size of 39 species.https://frontiersinzoology.biomedcentral.com/dm2022BiochemistryGeneticsMicrobiology and Plant Patholog

A New Case of Ants Nesting within Branches of a Fig Tree: the Case of Ficus subpisocarpa in Taiwan

Ficus is one of many plant genera involved in interactions with ants. The interaction is however little documented. We show here that ants, belonging mainly to the genus Crematogaster, nest in hollow internodes of young branches of Ficus subpisocarpa, a monoecious fig species studied in Taiwan. The ants feed on the mutualistic fig-pollinating wasps as well as on parasitic non-pollinating fig wasps. Nevertheless fig-wasps may not constitute a sufficient food source to ensure permanent presence of ants on the tree as the ants were observed to be frequently associated with hemipterans such as coccids and aphids. Fig wasps seem to constitute a reliable and sufficient food source on some dioecious Ficus species. On the contrary, in monoecious Ficus species, resident ants have always been observed to tend homopteran in addition to feeding on fig wasps. Frequent fruiting, prolonged fruit ripening period, ramiflory and rapid growth could constitute traits facilitating strong association based on fig-wasps' consumption of the monoecious F. subpisocarpa with ants. Despite these traits, ants were observed to tend hemipterans, and F. subpisocarpa does not seem to have evolved specialized morphological traits to facilitate the association

An extreme case of plant-insect co-diversification: figs and fig-pollinating wasps

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 co-phylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on average, wasps had sequences from 77% of six genes (5.6kb), figs had sequences from 60% of five 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 co-phylogenetic analyses further support the co-diversification hypothesis. Biogeographic analyses indicate that the presentday distribution of fig and pollinator lineages is consistent with an 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 co-diversification

Phylogeny and evolution of life-history strategies in the Sycophaginae non-pollinating fig wasps (Hymenoptera, Chalcidoidea)

<p>Abstract</p> <p>Background</p> <p>Non-pollinating Sycophaginae (Hymenoptera, Chalcidoidea) form small communities within <it>Urostigma </it>and <it>Sycomorus </it>fig trees. The species show differences in galling habits and exhibit apterous, winged or dimorphic males. The large gall inducers oviposit early in syconium development and lay few eggs; the small gall inducers lay more eggs soon after pollination; the ostiolar gall-inducers enter the syconium to oviposit and the cleptoparasites oviposit in galls induced by other fig wasps. The systematics of the group remains unclear and only one phylogeny based on limited sampling has been published to date. Here we present an expanded phylogeny for sycophagine fig wasps including about 1.5 times the number of described species. We sequenced mitochondrial and nuclear markers (4.2 kb) on 73 species and 145 individuals and conducted maximum likelihood and Bayesian phylogenetic analyses. We then used this phylogeny to reconstruct the evolution of Sycophaginae life-history strategies and test if the presence of winged males and small brood size may be correlated.</p> <p>Results</p> <p>The resulting trees are well resolved and strongly supported. With the exception of <it>Apocrytophagus</it>, which is paraphyletic with respect to <it>Sycophaga</it>, all genera are monophyletic. The Sycophaginae are divided into three clades: (i) <it>Eukoebelea</it>; (ii) <it>Pseudidarnes</it>, <it>Anidarnes </it>and <it>Conidarnes </it>and (iii) <it>Apocryptophagus</it>, <it>Sycophaga </it>and <it>Idarnes</it>. The ancestral states for galling habits and male morphology remain ambiguous and our reconstructions show that the two traits are evolutionary labile.</p> <p>Conclusions</p> <p>The three main clades could be considered as tribes and we list some morphological characters that define them. The same biologies re-evolved several times independently, which make Sycophaginae an interesting model to test predictions on what factors will canalize the evolution of a particular biology. The ostiolar gall-inducers are the only monophyletic group. In 15 Myr, they evolved several morphological adaptations to enter the syconia that make them strongly divergent from their sister taxa. Sycophaginae appears to be another example where sexual selection on male mating opportunities favored winged males in species with small broods and wingless males in species with large broods. However, some species are exceptional in that they lay few eggs but exhibit apterous males, which we hypothesize could be due to other selective pressures selecting against the re-appearance of winged morphs.</p