Cryptic species of fig-pollinating wasps: implications for the evolution of the fig-wasp mutualism, sex allocation, and precision of adaptation.
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ABSTRACT:
SUBMITTER: Molbo D
PROVIDER: S-EPMC156293 | biostudies-literature | 2003 May
REPOSITORIES: biostudies-literature
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Cryptic species of fig-pollinating wasps: implications for the evolution of the fig-wasp mutualism, sex allocation, and precision of adaptation.
Molbo Drude D Machado Carlos A CA Sevenster Jan G JG Keller Laurent L Herre Edward Allen EA
Proceedings of the National Academy of Sciences of the United States of America 20030424 10
Fig-pollinating wasps have provided model systems for developing and testing theories of the evolution of mutualism, sex allocation, and precision of adaptation. With few exceptions, previous studies have assumed one species of pollinator wasp per host fig species. Here we report genetic data demonstrating the coexistence of previously undetected cryptic fig wasp species in at least half of the host fig species surveyed. The substantial mitochondrial sequence differences (4.2-6.1%) imply old div ...[more]
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Project description:A striking property of the ancient and obligate mutualism between figs and their pollinating wasps is that fig wasps consistently oviposit in the inner flowers of the fig syconium (gall flowers, which develop into galls that house developing larvae), but typically do not use the outer ring of flowers (seed flowers, which develop into seeds). To better understand differences between gall and seed flowers that might influence oviposition choices, and the unknown mechanisms underlying gall formation, we used a metatranscriptomic approach to analyze eukaryotic gene expression within fig flowers at the time of oviposition choice and early gall development. Consistent with the unbeatable seed hypothesis, which posits that only a portion of fig flowers are physiologically capable of responding to gall induction or supporting larval development, we found significant differences in gene expression assigned to defense and metabolism between gall- and seed flowers in receptive syconia. Transcripts assigned to flavonoids and defense were especially prevalent in receptive gall flowers, and carbohydrate metabolism was significantly up-regulated relative to seed flowers. In turn, high expression of the venom gene icarapin during wasp embryogenesis within galled flowers distinguishes it as a candidate gene for gall initiation. In response to galling, the fig significantly up-regulates the expression of chalcone synthase, which previously has been connected to gall formation in other plants. This study simultaneously evaluates the gene expression profile of both mutualistic partners in a plant-insect mutualism and provides evidence for a stability mechanism in the ancient fig-fig wasp association.
2015-03-05 | GSE55700 | GEO
Project description:A striking property of the ancient and obligate mutualism between figs and their pollinating wasps is that fig wasps consistently oviposit in the inner flowers of the fig syconium (gall flowers, which develop into galls that house developing larvae), but typically do not use the outer ring of flowers (seed flowers, which develop into seeds). To better understand differences between gall and seed flowers that might influence oviposition choices, and the unknown mechanisms underlying gall formation, we used a metatranscriptomic approach to analyze eukaryotic gene expression within fig flowers at the time of oviposition choice and early gall development. Consistent with the unbeatable seed hypothesis, which posits that only a portion of fig flowers are physiologically capable of responding to gall induction or supporting larval development, we found significant differences in gene expression assigned to defense and metabolism between gall- and seed flowers in receptive syconia. Transcripts assigned to flavonoids and defense were especially prevalent in receptive gall flowers, and carbohydrate metabolism was significantly up-regulated relative to seed flowers. In turn, high expression of the venom gene icarapin during wasp embryogenesis within galled flowers distinguishes it as a candidate gene for gall initiation. In response to galling, the fig significantly up-regulates the expression of chalcone synthase, which previously has been connected to gall formation in other plants. This study simultaneously evaluates the gene expression profile of both mutualistic partners in a plant-insect mutualism and provides evidence for a stability mechanism in the ancient fig-fig wasp association. We examined two different Ficus flower types at two different time points. Each sample contained a pool of hundreds of individual flowers from multiple sycomia.
2015-03-05 | E-GEOD-55700 | biostudies-arrayexpress
Project description:BACKGROUND:Figs and fig-pollinating wasps are obligate mutualists that have coevolved for ca. 90 million years. They have radiated together, but do not show strict cospeciation. In particular, it is now clear that many fig species host two wasp species, so there is more wasp speciation than fig speciation. However, little is known about how fig wasps speciate. RESULTS:We studied variation in 71 fig-pollinating wasps from across the large geographic range of Ficus rubiginosa in Australia. All wasps sampled belong to one morphological species (Pleistodontes imperialis), but we found four deep mtDNA clades that differed from each other by 9-17% nucleotides. As these genetic distances exceed those normally found within species and overlap those (10-26%) found between morphologically distinct Pleistodontes species, they strongly suggest cryptic fig wasp species. mtDNA clade diversity declines from all four present in Northern Queensland to just one in Sydney, near the southern range limit. However, at most sites multiple clades coexist and can be found in the same tree or even the same fig fruit and there is no evidence for parallel sub-division of the host fig species. Both mtDNA data and sequences from two nuclear genes support the monophyly of the "P. imperialis complex" relative to other Pleistodontes species, suggesting that fig wasp divergence has occurred without any host plant shift. Wasps in clade 3 were infected by a single strain (W1) of Wolbachia bacteria, while those in other clades carried a double infection (W2+W3) of two other strains. CONCLUSION:Our study indicates that cryptic fig-pollinating wasp species have developed on a single host plant species, without the involvement of host plant shifts, or parallel host plant divergence. Despite extensive evidence for coevolution between figs and fig wasps, wasp speciation may not always be linked strongly with fig speciation.
| S-EPMC1626083 | biostudies-literature
Project description:Fig wasp is one of the most well known model systems in examining whether or not the parents could adjust their offspring sex ratio to maximize their gene frequency transmission in next generations. Our manipulative experiments showed that, in all of the five pollinator wasps of figs (Agaonidae) that have different averages of foundress numbers per syconium, almost the same proportions of male offspring are produced in the experiment that foundresses deposit one hour then are killed with ether (66.1%-70.1%) and over the lifespan of each foundress (14.0%-21.0%). The foundresses tend to deposit their male eggs prior to female eggs. The observed increase in the proportion of male offspring as a function of foundress number results from density-dependent interference competition among the foundresses. These results showed that the selection of gene frequency transmission through the behavioral adjustment in the evolution of sex ratio does not exist in these five fig wasps. The results here implied that genetic adjustment mechanisms of the sex ratio of fig wasps can only be triggered to be on or off and that the foundresses can not quantitatively adjust their sex ratio according to increased environmental selection pressure.
| S-EPMC4543974 | biostudies-literature
Project description:Fig trees are pollinated by fig wasps, which also oviposit in female flowers. The wasp larvae gall and eat developing seeds. Although fig trees benefit from allowing wasps to oviposit, because the wasp offspring disperse pollen, figs must prevent wasps from ovipositing in all flowers, or seed production would cease, and the mutualism would go extinct. In Ficus racemosa, we find that syconia ('figs') that have few foundresses (ovipositing wasps) are underexploited in the summer (few seeds, few galls, many empty ovules) and are overexploited in the winter (few seeds, many galls, few empty ovules). Conversely, syconia with many foundresses produce intermediate numbers of galls and seeds, regardless of season. We use experiments to explain these patterns, and thus, to explain how this mutualism is maintained. In the hot summer, wasps suffer short lifespans and therefore fail to oviposit in many flowers. In contrast, cooler temperatures in the winter permit longer wasp lifespans, which in turn allows most flowers to be exploited by the wasps. However, even in winter, only in syconia that happen to have few foundresses are most flowers turned into galls. In syconia with higher numbers of foundresses, interference competition reduces foundress lifespans, which reduces the proportion of flowers that are galled. We further show that syconia encourage the entry of multiple foundresses by delaying ostiole closure. Taken together, these factors allow fig trees to reduce galling in the wasp-benign winter and boost galling (and pollination) in the wasp-stressing summer. Interference competition has been shown to reduce virulence in pathogenic bacteria. Our results show that interference also maintains cooperation in a classic, cooperative symbiosis, thus linking theories of virulence and mutualism. More generally, our results reveal how frequency-dependent population regulation can occur in the fig-wasp mutualism, and how a host species can 'set the rules of the game' to ensure mutualistic behavior in its symbionts.
| S-EPMC2771911 | biostudies-literature
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.
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Project description:Microbial symbionts can influence a myriad of insect behavioral and physiological traits. However, how microbial communities may shape or be shaped by insect interactions with plants and neighboring species remains underexplored. The fig-fig wasp mutualism system offers a unique model to study the roles of microbiome in the interactions between the plants and co-habiting insects because a confined fig environment is shared by two fig wasp species, the pollinator wasp (Eupristina altissima and Eupristina verticillata) and the cheater wasp (Eupristina sp1 and Eupristina sp2). Here, we performed whole genome resequencing (WGS) on 48 individual fig wasps (Eupristina spp.) from Yunnan, China, to reveal the phylogenetic relationship and genetic divergence between pollinator and congeneric cheater wasps associated with the Ficus trees. We then extracted metagenomic sequences to explore the compositions, network structures, and functional capabilities of microbial communities associated with these wasps. We found that the cheaters and pollinators from the same fig species are sister species, which are highly genetically divergent. Fig wasps harbor diverse but stable microbial communities. Fig species dominate over the fig wasp genotype in shaping the bacterial and fungal communities. Variation in microbial communities may be partially explained by the filtering effect from fig and phylogeny of fig wasps. It is worth noting that cheaters have similar microbial communities to their sister pollinators, which may allow cheaters to coexist and gain resources from the same fig species. In terms of metabolic capabilities, some bacteria such as Desulfovibrio and Lachnospiraceae are candidates involved in the nutritional uptake of fig wasps. Our results provide novel insights into how microbiome community and metabolic functions may couple with the fig-wasp mutualistic systems.
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Project description:Theory identifies factors that can undermine the evolutionary stability of mutualisms. However, theory's relevance to mutualism stability in nature is controversial. Detailed comparative studies of parasitic species that are embedded within otherwise mutualistic taxa (e.g., fig pollinator wasps) can identify factors that potentially promote or undermine mutualism stability. We describe results from behavioral, morphological, phylogenetic, and experimental studies of two functionally distinct, but closely related, Eupristina wasp species associated with the monoecious host fig, Ficus microcarpa, in Yunnan Province, China. One (Eupristina verticillata) is a competent pollinator exhibiting morphologies and behaviors consistent with observed seed production. The other (Eupristina sp.) lacks these traits, and dramatically reduces both female and male reproductive success of its host. Furthermore, observations and experiments indicate that individuals of this parasitic species exhibit greater relative fitness than the pollinators, in both indirect competition (individual wasps in separate fig inflorescences) and direct competition (wasps of both species within the same fig). Moreover, phylogenetic analyses suggest that these two Eupristina species are sister taxa. By the strictest definition, the nonpollinating species represents a "cheater" that has descended from a beneficial pollinating mutualist. In sharp contrast to all 15 existing studies of actively pollinated figs and their wasps, the local F. microcarpa exhibit no evidence for host sanctions that effectively reduce the relative fitness of wasps that do not pollinate. We suggest that the lack of sanctions in the local hosts promotes the loss of specialized morphologies and behaviors crucial for pollination and, thereby, the evolution of cheating.
| S-EPMC8364199 | biostudies-literature
Project description:Nucleotide sequences from the cytochrome oxidase I (COI) gene were used to reconstruct phylogenetic relationships among 15 genera of fig-pollinating wasps. We present evidence supporting broad-level co-cladogenesis with respect to most but not all of the corresponding groups of figs. Using fossil evidence for calibrating a molecular clock for these data, we estimated the origin of the fig-wasp mutualism to have occurred ca. 90 million years ago. The estimated divergence times among the pollinator genera and their current geographical distributions corresponded well with several features of the break-up of the southern continents during the Late Cretaceous period. We then explored the evolutionary trajectories of two characteristics that hold profound consequences for both partners in the mutualism: the breeding system of the host (monoecious or dioecious) and pollination behaviour of the wasp (passive or active). The fig wasp mutualism exhibits extraordinarily long-term evolutionary stability despite clearly identifiable conflicts of interest between the interactors, which are reflected by the very distinct variations found on the basic mutualistic theme.
| S-EPMC1088657 | biostudies-other
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.].
| S-EPMC3478567 | biostudies-literature