Non-quantitative adjustment of offspring sex ratios in pollinating fig wasps.
Ontology highlight
ABSTRACT:
SUBMITTER: Wang RW
PROVIDER: S-EPMC4543974 | biostudies-literature |
REPOSITORIES: biostudies-literature
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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.
| S-EPMC8756665 | 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: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 divergences ( approximately 1.5-5.1 million years ago) among these species. Furthermore, some cryptic species pairs seem to be sister taxa, whereas others clearly are not, indicating both long-term coexistence on shared hosts and the colonization of novel fig species. These findings undermine the prevalent notion of strict one-to-one specificity between cospeciating figs and their pollinators, thereby challenging existing theory concerning the evolution and stability of mutualisms. Moreover, the incorporation of the genetic information significantly improves the fit of the observed sex ratios to predictions of local mate-competition theory, further strengthening support for sex allocation theory and the precision of adaptation.
| S-EPMC156293 | biostudies-literature
Project description:BackgroundNon-pollinating Sycophaginae (Hymenoptera, Chalcidoidea) form small communities within Urostigma and Sycomorus 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.ResultsThe resulting trees are well resolved and strongly supported. With the exception of Apocrytophagus, which is paraphyletic with respect to Sycophaga, all genera are monophyletic. The Sycophaginae are divided into three clades: (i) Eukoebelea; (ii) Pseudidarnes, Anidarnes and Conidarnes and (iii) Apocryptophagus, Sycophaga and Idarnes. The ancestral states for galling habits and male morphology remain ambiguous and our reconstructions show that the two traits are evolutionary labile.ConclusionsThe 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.
| S-EPMC3145598 | biostudies-literature
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
Project description:Population genomics and structure of several fig species and corresponding fig wasps along the Mount Wilhelm altitudinal gradient, Papua New Guinea. Raw sequence reads
| PRJNA445222 | ENA
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: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 has always been thought the species-specific pollinator for their host fig (Moraceae, Ficus) and constitute a model system with its host to study co-evolution and co-speciation. The availability of a high-quality genome will help to further reveal the mechanisms underlying these characteristics. Here, we present a high-quality chromosome-level genome for Valisa javana developed by a combination of PacBio long-read and Illumina short-read. The assembled genome size is 296.34 Mb from 13 contigs with a contig N50 length of 26.76 kb. Comparative genomic analysis revealed expanded and positively selected genes related to biological features that aid fig wasps living in syconium of its highly specific host. Protein-coding genes associated with chemosensory, detoxification and venom genes were identified. Several differentially expressed genes in transcriptome data of V. javana between odor-stimulated samples and the controls have been identified in some olfactory signal transduction pathways, e.g. olfactory transduction, cAMP, cGMP-PKG, Calcim, Ras and Rap1. This study provides a valuable genomic resource for a fig wasp, and sheds insight into further revealing the mechanisms underlying their adaptive traits to their hosts in different places and co-speciation with their host.
| S-EPMC9160881 | biostudies-literature
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.
| S-EPMC9715610 | biostudies-literature