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Asteromyia carbonifera (A) adult, (B) eggs, and (C) larvae within a dissected gall. Adults and mature larvae are about 1–2 mm in length. Scale bar on (B) is 200 μm and eggs are typically 180–240 μm long. See online colour version.
Source publication
The Ambrosia gall midge [Asteromyia carbonifera (Osten Sacken) (Diptera: Cecidomyiidae: Alycaulini)] consists, in part, of a complex of genetically differentiated populations that have diverged in gall morphology on the host plant Solidago altissima L. (Asteraceae). This divergence appears to be an incipient adaptive radiation that may be driven by...
Contexts in source publication
Context 1
... eggs of A. carbonifera are laid on the underside of the leaf in the vicinity of the meristem ( Figure 1B). Females have up to 300 eggs at the time of emergence and fecundity appears to differ by morphotype (JJ Heath, unpubl.). ...
Context 2
... have up to 300 eggs at the time of emergence and fecundity appears to differ by morphotype (JJ Heath, unpubl.). The larvae ( Figure 1C) hatch and the fungal spores germinate (Figure 2) within a few days of oviposition and begin to burrow ⁄ grow into the leaf tissue within a few millimetres of the ovipositional site. Once the larva has penetrated the leaf tissue, fungal growth becomes evident on the bottom and then the top of the leaf. ...
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Citations
... Likewise, microscopic observations of the female abdomen showed the existence of a bag (mycangia) associated with the terminal segments of the abdomen next to the ovipositor; moreover, B. dothidea conidia were observed in these bags. The scientific literature indicates that many species of cecidomyiids carry this specialized structure (mycangia) where the female incorporates the conidia or mycelia of the mutualistic fungi [44][45][46][47]. In the Lasiopterini tribe, this structure is found in the eighth abdominal segment [48,49]. ...
... In the Lasiopterini tribe, this structure is found in the eighth abdominal segment [48,49]. The fact that certain species of midges, in the relationship between these insects and associated fungi, carry mycangia on their abdomen or ovipositor reinforces the concept of mutualism rather than opportunism [45,46,48,50]. In accordance with this concept, the results of the present study suggest that the relationship between B. dothidea and P. berlesiana could be mutualistic, with the cecidomyiid acting as a vector of the pathogen. ...
Escudete, which is caused by Botryosphaeria dothidea, is a disease that is widely distributed in the Mediterranean basin, but is of little general importance. Nevertheless, serious attacks have been observed on occasion, which have caused a considerable reduction in the quality of table olives. The incidence of the pathogen has been associated with damage caused by the olive fly (Bactrocera oleae) and the presence of a possible vector agent, i.e., the midge Prolasioptera berlesiana, whose larvae can feed on fly eggs (although the role the midge may play in the spread of this disease is not well known). Therefore, it is necessary to clarify these interactions to adopt appropriate disease control measures. Studies were conducted in olive orchards planted with the Gordal Sevillana, Picudo, and Hojiblanca olive cultivars. Field surveys were carried out in order to sample their fruits for laboratory analysis, and several bioassays were also performed. Moreover, the population of B. oleae adults was monitored using traps that were baited with food attractants. The results indicated that the three agents developed and evolved in parallel under field conditions. Thus, the midges were attracted by the oviposition punctures caused in fruits by olive fruit flies, regardless of whether the punctures contained eggs. All the investigated olive fruits in which midges were present inside punctures created by olive fruit flies exhibited typical symptoms of escudete, which is necessary for the development of this disease. Forty-eight hours after fly punctures were artificially simulated in the olive fruits, 48.0% of them contained a midge, whereas no midges appeared in the artificially created shapeless wounds in the fruits. This indicates that an olive fly egg is not required for the development of midges; however, they do prefer punctures made by B. oleae. Moreover, when the olive fruits were incubated in a humid chamber, the B. dothidea fungus only appeared in those fruits that contained midges, thus indicating a close relationship between these two agents. Additionally, the midges were able to complete their entire development from egg to adult under controlled conditions, and they fed on the pure cultures of the B. dothidea fungus. Furthermore, although no pathogens were present in the immature midges, some of the pathogens could have been isolated from the inner tissues of the adult female midges. The fact that mycangia is present in the abdomen of P. berlesiana supports the hypothesis that their relationship with B. dothidea may be mutualistic and that they may act as a vector for the fungus.
... In particular, Physalospora piricola (P. piricola), which infects apple branches, fruit, and leaves, has a serious impact on the growth and yield of fruit trees and is the main causal agent of apple ring rot [6]. It is widely distributed in most apple-growing areas in the country but is most severe in eastern China (Liaoning, Shandong, Henan, and Hebei provinces), where summer temperatures and rainfall are high. ...
... Chemical shifts were measured relative to residual solvent peaks of CDCl 3 ( 1 H: δ = 7.26 ppm; 13 C: δ = 77.0 ppm) and DMSO-d 6 ( 1 H: δ = 2.5 and 3.3 ppm; 13 C: δ = 39.9 ppm) as internal standards. The following abbreviations are used to designate chemical shift multiplicities: s = singlet, d = doublet, dd = doublet of doublets, t = triplet, m = multiplet, and brs = broad singlet. ...
Plant diseases caused by pathogenic fungi or oomycetes seriously affect crop growth and the quality and yield of products. A series of novel 1,2,4-triazole derivatives containing carboxamide fragments based on amide fragments widely used in fungicides and the commercialized mefentrifluconazole were designed and synthesized. Their antifungal activities were evaluated against seven kinds of phytopathogenic fungi/oomycete. Results showed that most compounds had similar or better antifungal activities compared to mefentrifluconazole’s inhibitory activity against Physalospora piricola, especially compound 6h (92%), which possessed outstanding activity. Compound 6h (EC50 = 13.095 μg/mL) showed a better effect than that of mefentrifluconazole (EC50 = 39.516 μg/mL). Compound 5j (90%) displayed outstanding anti-oomycete activity against Phytophthora capsici, with an EC50 value of 17.362 μg/mL, far superior to that of mefentrifluconazole (EC50 = 75.433 μg/mL). The result of molecular docking showed that compounds 5j and 6h possessed a stronger affinity for 14α-demethylase (CYP51). This study provides a new approach to expanding the fungicidal spectrum of 1,2,4-triazole derivatives.
... Pencil drawing illustrations by Mariana Barcoto. Xyphidria (Kukor and Martin, 1983;Heath and Stireman, 2010;Pažoutová et al., 2010). (ii) Advanced fungiculture, that involve active maintenance of fungal crops by fungusgrowing insects, is hypothesized to have arisen during the Paleogene (66-24 Million years ago; Roberts et al., 2016). ...
... Intriguing fungus cultivation systems for which the fungal metabolism of plant components remains to be elucidated were not detailed as well. These encompass the leafrolling weevil Euops chinensis (Coleoptera: Attelabidae) that cultivates a garden of Penicillium herquei for antimicrobial protection of the larvae (Wang et al., 2015), and gall-forming midges (Diptera: Cecidomyiidae) associated with fungi in the family Botryosphaeriaceae (Rohfritsch, 2008;Heath and Stireman, 2010). Whenever possible, we attempted to focus on aspects related to plant-degrading potential of the fungiculture system, to emphasize metabolic pathways that, while supporting insects' ecology and evolution, could also be applied in biotechnological processes. ...
Anthropogenic activities have extensively transformed the biosphere by extracting and disposing of resources, crossing boundaries of planetary threat while causing a global crisis of waste overload. Despite fundamental differences regarding structure and recalcitrance, lignocellulose and plastic polymers share physical-chemical properties to some extent, that include carbon skeletons with similar chemical bonds, hydrophobic properties, amorphous and crystalline regions. Microbial strategies for metabolizing recalcitrant polymers have been selected and optimized through evolution, thus understanding natural processes for lignocellulose modification could aid the challenge of dealing with the recalcitrant human-made polymers spread worldwide. We propose to look for inspiration in the charismatic fungal-growing insects to understand multipartite degradation of plant polymers. Independently evolved in diverse insect lineages, fungiculture embraces passive or active fungal cultivation for food, protection, and structural purposes. We consider there is much to learn from these symbioses, in special from the community-level degradation of recalcitrant biomass and defensive metabolites. Microbial plant-degrading systems at the core of insect fungicultures could be promising candidates for degrading synthetic plastics. Here, we first compare the degradation of lignocellulose and plastic polymers, with emphasis in the overlapping microbial players and enzymatic activities between these processes. Second, we review the literature on diverse insect fungiculture systems, focusing on features that, while supporting insects' ecology and evolution, could also be applied in biotechnological processes. Third, taking lessons from these microbial communities, we suggest multidisciplinary strategies to identify microbial degraders, degrading enzymes and pathways, as well as microbial interactions and interdependencies. Spanning from multiomics to spectroscopy, microscopy, stable isotopes probing, enrichment microcosmos, and synthetic communities, these strategies would allow for a systemic understanding of the fungiculture ecology, driving to application possibilities. Detailing how the metabolic landscape is entangled to achieve ecological success could inspire sustainable efforts for mitigating the current environmental crisis.
... Considering that several gall midges depend on their symbiotic interaction with symbiotic fungi for gall development and host manipulation (Heath and Stireman, 2010;Stireman et al., 2010), these ...
... Statistical significance at p < 0.05 are highlighted with an asterisk. Cecidogenic insects, with the aid of their microbiome, are capable of gall induction and "hijacking" the biochemistry of the host plant, being protected and sustained at the expense of plant resources (Fernandes et al., 2012;Heath and Stireman, 2010;Martini et al., 2019;Raman, 2005;Schultz et al., 2019;Stireman et al., 2010;Stone and Schönrogge, 2003). This is achieved despite (and against) the defensive capabilities of the host plant, thanks to intricate changes in plant physiology and biochemistry (Carneiro et al., 2014;Silva et al., 2019;. ...
Changes in plant secondary metabolism due to insect galls are one of the frontiers in knowledge of plant-insect interactions, especially concerning volatile organic compounds (VOCs). Here we studied the in vivo VOCs released from healthy apical branches of Haplopappus foliosus DC. (Asteraceae) and compared these volatiles to the VOCs obtained from apical bud galls produced in this host plant when attacked by the gall midge Hap-lopappusmyiia gregaria (Cecidomyiidae). We field-collected VOCs by dynamic headspace and identified them by gas chromatography coupled to mass spectrometry. We found changes in the relative proportions of different classes of VOC in apical branches vs. apical bud galls. H. foliosus VOCs had mainly monoterpene hydrocarbons such as p-cymene, a recognized herbivore deterrent. We also found oxygenated monoterpenes and sesquiterpenes in the H. foliosus volatile mixture. H. foliosus modifies its fragrance composition when parasitized by gall midges, showing an increased proportion of some monoterpene hydrocarbons, e.g. limonene and camphene, while others such as α-thujene, p-cymene and γ-terpinene were down-expressed in apical bud gall VOCs. We discuss these results considering gall signaling and chemical ecology hypotheses, including the potential role of plant defenses as well as gall midge-derived modification for host plant VOCs, and comment on the ecological relevance of our findings.
... There has been debate regarding the role of the fungus and how it enters the gall chamber. Some researchers have speculated that female gall midges deliberately inject fungal conidia into the host plant with their eggs (Borkent and Bissett 1985;Heath and Stireman 2010;Kobune et al. 2012;Rohfritsch 2008), however, the female gall midge has rarely been recorded in the act of ovipositing to confirm or refute this suggestion. ...
The hidden diversity and interactions of gall midges (Cecidomyiidae), their associated microfungal symbiont(s), and parasitoid wasps in temperate saltmarshes have been little studied in Australia. Over a period of two years, we investigated the gall-associated communities of the dominant saltmarsh plants, Tecticornia arbuscula and Salicornia quinqueflora, across south-eastern Australian coastal and inland salt-lake sites. We discovered that i) many gall midge species are more widely distributed than previously thought; ii) co-distribution of species affecting different plant organs on the same host is also widespread; iii) diversity of gall midges (6 species previously named; 5 species identified here as new) and parasitoid wasps (17 sp. prov.) is likely higher than we uncovered; iv) parasitoid wasps associated with gall midges belonged to diverse lineages and appear to be widespread generalists; v) while the microfungus usually associated with most Cecidomyiinae larval chambers is Botryosphaeria dothidea, we discovered a provisional new species of Botryosphaeria associated with a novel Asphondylia sp. in western South Australia. We also show that targeted amplicon sequencing is a valuable tool for investigating all components of multi-trophic level systems. Our research has contributed to a greater understanding of the basic biology of gall midge interactions within temperate saltmarsh ecosystems in southern Australia, and highlights the value of investigating all trophic levels in these complex interactions simultaneously.
... (Hansford 1956) (formerly Mycosphaerella molleriana) and Zasmidium pseudovespa (Carnegie) U. Braun, C. Nakash., Videira & Crous (Videira 2017) (formerly M. pseudovespa) have been isolated from wasp galls on leaves of E. globulus and E. biturbinata in Australia (Carnegie et al. 2007). Some of the gall midges are considered mycophagous (Bisset and Borkent 1988;Veenstra-Quah et al. 2007;Heath and Stireman 2010) and this may also be the case with Z. mangrovei. However, whether the fungus is vectored by the gall midges or is an endophyte of the host plant, remains unknown. ...
During studies to investigate the health of mangrove trees in South Africa, high numbers of Avicennia marina were found with leaf galls caused by unidentified adults and larvae of midges (Cecidomyiidae). Fungal fruiting structures were commonly observed on the abaxial areas of the galls. To determine the identity of the fungi associated with the gall midges, phylogenetic analyses using multigene sequence data were used. The nuclear large subunit (LSU), internal transcribed spacer (ITS), and a portion of the actin gene region (ACT), were amplified and analyzed. The results revealed that the fungal fruiting structures represent a new taxon in the Mycosphaerellaceae described here as Zasmidium mangrovei sp. nov. This is the first report of a species in the Mycosphaerellaceae associated with cecidomyiid leaf galls on A. marina.
... (Hansford 1956) (formerly Mycosphaerella molleriana) and Zasmidium pseudovespa (Carnegie) U. Braun, C. Nakash., Videira & Crous (Videira 2017) (formerly M. pseudovespa) have been isolated from wasp galls on leaves of E. globulus and E. biturbinata in Australia (Carnegie et al. 2007). Some of the gall midges are considered mycophagous (Bisset and Borkent 1988;Veenstra-Quah et al. 2007;Heath and Stireman 2010) and this may also be the case with Z. mangrovei. However, whether the fungus is vectored by the gall midges or is an endophyte of the host plant, remains unknown. ...
During studies to investigate the health of mangrove trees in South Africa, high numbers of Avicennia marina were found with leaf galls caused by unidentified adults and larvae of midges (Cecidomyi-idae). Fungal fruiting structures were commonly observed on the abaxial areas of the galls. To determine the identity of the fungi associated with the gall midges, phylogenetic analyses using multi-gene sequence data were used. The nuclear large subunit (LSU), internal transcribed spacer (ITS), and a portion of the actin gene region (ACT), were amplified and analyzed. The results revealed that the fungal fruiting structures represent a new taxon in the Mycosphaerellaceae described here as Zasmidium mangrovei sp. nov. This is the first report of a species in the Mycosphaerellaceae associated with cecido-myiid leaf galls on A. marina.
... Non-bacterial microbes could, in theory, have symbiotic associations with gall inducers and these were not specifically targeted by our 16S rRNA gene sequencing approach. For example, many gall midges are associated with fungal symbionts that serve as an important food source inside the gall (Rohfritsch 2008;Heath and Stireman 2010). However, our data tentatively suggest that this was not the case among the insect species we surveyed. ...
A diverse array of organisms induce plants to form galls. This phenomenon is one of the most striking instances of convergent evolution, yet the underlying mechanism is only well understood in gall-inducing microbes. To determine if gall induction by insects is associated with bacterial symbiosis, we used 16S rRNA gene sequencing to examine the microbiome of a variety of gall-inducing and non-gall-inducing insects. Overall, we did not find any bacterial signature of gall induction among the insect species we surveyed. There were no specific bacterial taxa that were consistently associated with gall induction. Microbiome diversity differed significantly among species of host insects, but not between gall- and non-gall-inducing insect species. Bacterial community composition also differed strongly among insect species, but not in a systematic way between gall-inducing and non-gall-inducing species. Furthermore, two gall-inducing species harbored highly variable microbiomes with relatively few bacterial sequences, characteristics that suggest a lack of abundant bacterial symbionts. Together, these findings argue that gall induction is not consistently mediated by a bacterial symbiont or bacterial community and may be symbiont-independent, at least in some insect species. While symbionts may still contribute to gall induction in specific instances, we suggest that the convergent evolution of gall induction is more typically driven by endogenous mechanisms, with potential contributions from horizontal gene transfer.
... We avoid the term "endophytophagy" because others have accepted the term "phytophagy" to mean "feeding on living tissue of higher plants" ("higher plants" being a synonym for "vascular plants" ;Strong et al., 1984;Mitter et al., 1988) and we want to include in our discussion insects that have found a way to live in and feed upon any plant or fungal tissue of a live plant. By focusing on plant or fungal feeding, our definition includes mutualisms between insects and fungi (e.g., ambrosia galls) in which the insect indirectly feeds upon plants by eating fungi, which consume the plant; these often-symbiotic fungi have facilitated endophytic lifestyles for some taxa (e.g., Hymenoptera, Coleoptera, Diptera; Bissett and Borkent, 1988;Hanson, 1995;Farrell, 1998;Heath and Stireman, 2010). Our definition excludes predation or parasitoidism, animal-animal interactions which can occur within plant tissue but are obviously not plant feeding. ...
Herbivorous feeding inside plant tissues, or endophagy, is a common lifestyle across Insecta, and occurs in insect taxa that bore, roll, tie, mine, gall, or otherwise modify plant tissues so that the tissues surround the insects while they are feeding. Some researchers have developed hypotheses to explain the adaptive significance of certain endophytic lifestyles (e.g., miners or gallers), but we are unaware of previous efforts to broadly characterize the adaptive significance of endophagy more generally. To fill this knowledge gap, we characterized the limited set of evolutionary selection pressures that could have encouraged phytophagous insects to feed inside plants, and then consider how these factors align with evidence for endophagy in the evolutionary history of orders of herbivorous insects. Reviewing the occurrence of endophytic taxa of various feeding guilds reveals that the pattern of evolution of endophagy varies strongly among insect orders, in some cases being an ancestral trait (e.g., Coleoptera and Lepidoptera) while being more derived in others (e.g., Diptera). Despite the large diversity of endophagous lifestyles and evolutionary trajectories that have led to endophagy in insects, our consideration of selection pressures leads us to hypothesize that nutritionally based factors may have had a stronger influence on evolution of endophagy than other factors, but that competition, water conservation, and natural enemies may have played significant roles in the development of endophagy.
... Molecular Phylogenetics and Evolution 140 (2019) 106602 obligatory association with specific fungi that line the inside walls of the galls, similar to the galleries of wood-boring Ambrosia beetles, and therefore they are often referred to as 'ambrosia gallers' (Neger, 1910, Bisset andBorkent, 1988). The nature of this association is not entirely clear but it has been suggested that the fungus is vital at least for gall initiation and in some cases the gall-midge larvae may actually feed on it inside the gall (Bisset and Borkent, 1988, Rohfritsch, 2008, Heath and Stireman, 2010). Yet another type of herbivory that evolved multiple times in the Cecidomyiinae is inquilinism, whereby species that are not capable of gall induction themselves develop in galls that were formed by other cecidomyiids, sometimes killing the gall inducer as a result of competition for gall resources or for physical space (Osgood and Gagné, 1978, Dorchin et al., 2007, 2015b. ...
... Molecular Phylogenetics and Evolution 140 (2019) 106602 Camptoneuromyiini in the Lasioperidi, Anadiplosini, Centrodiplosini and Hormomyiini in the Cecidomyiidi). Second, the role of the fungus in ambrosia galls is unclear, and while in Asteromyia carbonifera (Alycaulini) it has been shown that the larvae actually consume the fungus (Heath and Stireman, 2010) this may be an exception because, unlike other ambrosia gallers, galls of this species are composed of fungal tissue. It is unclear whether other taxa of 'ambrosia gall-midges' feed on their symbiotic fungi. ...
Gall midges (Cecidomyiidae) constitute one of the largest and most diverse families of Diptera, with close to 6600 described species and thousands of undescribed species worldwide. The family is divided into six subfamilies, the five basal ones comprising only fungivorous taxa, whereas the largest, youngest and most diverse subfamily Cecidomyiinae includes fungivorous as well as herbivorous and predatory species. The currently accepted classification of the Cecidomyiinae is morphology-based, and the few phylogenetic inferences that have previously been suggested for it were based on fragmentary or limited datasets. In a first comprehensive phylogenetic analysis of the Cecidomyiinae we sampled 142 species representing 88 genera of 13 tribes from all feeding guilds and zoogeographic regions in order to test the validity of the systematic division of the subfamily and gain insight into patterns of diversification and the evolution of feeding modes. We used sequences from five mitochondrial and nuclear genes to reconstruct maximum likelihood and Bayesian, time-calibrated phylogenies and conducted ancestral state reconstruction of feeding modes. Our results corroborate to a great extent the morphology-based classification of the Cecidomyiinae, with strong support for all supertribes and tribes, all were apparently established in the Upper Cretaceous concordant with the major radiation of angiosperms. We infer that transitions from fungus-feeding to plant-feeding occurred only once or twice in the evolution of the subfamily and that predation evolved only once, contrary to previous hypotheses. All herbivorous clades in the subfamily are very species rich and have diversified at a significantly greater rate than expected, but we found no support for the assertion that herbivorous clades associated with symbiotic fungi in their galls diversify faster than clades that do not have such associations. Currently available data also do not support the hypothesis that symbiotic clades have broader host ranges than non-symbiotic clades.
