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- Braga, Mariana P., et al.
(författare)
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Phylogenetic reconstruction of ancestral ecological networks through time for pierid butterflies and their host plants
- 2021
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Ingår i: Ecology Letters. - : Wiley. - 1461-023X .- 1461-0248. ; 24:10, s. 2134-2145
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Tidskriftsartikel (refereegranskat)abstract
- The study of herbivorous insects underpins much of the theory that concerns the evolution of species interactions. In particular, Pieridae butterflies and their host plants have served as a model system for studying evolutionary arms races. To learn more about the coevolution of these two clades, we reconstructed ancestral ecological networks using stochastic mappings that were generated by a phylogenetic model of host-repertoire evolution. We then measured if, when, and how two ecologically important structural features of the ancestral networks (modularity and nestedness) evolved over time. Our study shows that as pierids gained new hosts and formed new modules, a subset of them retained or recolonised the ancestral host(s), preserving connectivity to the original modules. Together, host-range expansions and recolonisations promoted a phase transition in network structure. Our results demonstrate the power of combining network analysis with Bayesian inference of host-repertoire evolution to understand changes in complex species interactions over time.
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| 4. |
- Gobbo, Erik, et al.
(författare)
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From Inquilines to Gall Inducers : Genomic Signature of a Life-Style Transition in Synergus Gall Wasps
- 2020
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Ingår i: Genome Biology and Evolution. - : Oxford University Press (OUP). - 1759-6653 .- 1759-6653. ; 12:11, s. 2060-2073
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Tidskriftsartikel (refereegranskat)abstract
- Gall wasps (Hymenoptera: Cynipidae) induce complex galls on oaks, roses, and other plants, but the mechanism of gall induction is still unknown. Here, we take a comparative genomic approach to revealing the genetic basis of gall induction. We focus on Synergus itoensis, a species that induces galls inside oak acorns. Previous studies suggested that this species evolved the ability to initiate gall formation recently, as it is deeply nested within the genus Synergus, whose members are mostly inquilines that develop inside the galls of other species. We compared the genome of S. itoensis with that of three related Synergus inquilines to identify genomic changes associated with the origin of gall induction. We used a novel Bayesian selection analysis, which accounts for branch-specific and gene-specific selection effects, to search for signatures of selection in 7,600 single-copy orthologous genes shared by the four Synergus species. We found that the terminal branch leading to S. itoensis had more genes with a significantly elevated dN/dS ratio (positive signature genes) than the other terminal branches in the tree; the S. itoensis branch also had more genes with a significantly decreased dN/dS ratio. Gene set enrichment analysis showed that the positive signature gene set of S. itoensis, unlike those of the inquiline species, is enriched in several biological process Gene Ontology terms, the most prominent of which is “Ovarian Follicle Cell Development.” Our results indicate that the origin of gall induction is associated with distinct genomic changes, and provide a good starting point for further characterization of the genes involved.
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- Gobbo, Erik, 1990-
(författare)
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Gall induction in gall wasps (Cynipidae s. lat.) : Insights from comparative genomics
- 2022
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Doktorsavhandling (övrigt vetenskapligt/konstnärligt)abstract
- Cynipidae are a family of wasps (Hymenoptera), whose larval stages develop inside plant galls, that is, abnormal plant structures formed in response to the presence of foreign organisms. Most cynipids are gall inducers and are often capable of notable levels of host manipulation. Others are inquilines, meaning they are dependent on other species for the initiation of the gall. Their larvae then develop inside the gall, often killing the original inducer and modifying the gall in the process. The biochemical mechanism of gall induction is still shrouded in mystery. In this thesis, various approaches are implemented to try to shed some light on the process. In Paper I, we used shotgun sequencing to investigate the bacterial association of larvae of different species inhabiting the bedeguar gall on roses, and showed that neither the inquiline nor the gall inducer inhabiting this gall are associated with symbiotic bacteria that are likely to be involved in gall induction, despite earlier speculations to that effect. In Paper II, I used comparative genomic analysis of a recently evolved gall inducer in the genus Synergus and three related inquilines to identify candidate genes involved in gall initiation. Specifically, I used a new method relying on genome-wide analyses to control for confounding factors, implemented in the software Bayescode. Then, I used Gene Onthology (GO) analysis to show that the candidate genes are associated with specific functions, such as “egg follicle development” and “neural development”. In paper III, we used genomic and transcriptomic data to infer the phylogeny of the family. The analysis confirmed that the phytophagous Cynipidae fall into two distinct lineages, as suggested by a recent phylogenomic analysis based on ultraconserved elements. We propose that these families be recognized as Cynipidae s. str. (oak gallers and relatives) and Diplolepididae (rose gallers and relatives). Finally, in paper IV, I applied the same methods as in Paper II to genomes of the Cynipidae s. str. to identify candidate genes associated with gall secondary structures. I inferred that these genes are often associated with GO terms relative to egg development and cell movement. In conclusion, the data presented here can provide a useful starting point for future research on cynipids.
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- Gobbo, Erik, et al.
(författare)
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Host manipulation by oak gall wasps: Insights from evolutionary signatures in the gall-wasp genome
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Annan publikation (övrigt vetenskapligt/konstnärligt)abstract
- The oak gall-wasps (Cynipidae: Cynipini) make some of the most complex plant galls found in nature. The shape of the outer gall varies spectacularly among species, and is characterised by traits that appear to have evolved to defend the larva or larvae inside in an intense evolutionary arms race with predators and parasitoids. It is still unclear how the oak gall-wasps achieve this unusual level of host manipulation. Here, we take a comparative genomic approach to gain some insight into the underlying mechanisms, assuming that the arms race should result in unusually rapid evolution in the proteins involved. Specifically, we compared genomes of Cynipini species making complex and diverse outer galls to those of related lineages making simple galls. We analysed over 5,000 orthologous genes using the recent Bayescode tool, which controls for the background levels of evolution in the genes and lineages involved using a whole-genome approach. We then used gene set enrichment analysis to identify which Gene Ontology terms were more often associated with genes that had an unusually high rate of nonsynonymous evolution in the complex gallers. The complex gallers did not have an elevated number of such genes. However, the genes that had elevated rates in complex gallers were associated with biological-process gene ontology terms related to the formation of the egg follicle and to cell movement, suggesting that these genes may play a role in the formation of complex outer galls, and that they would be interesting target genes for experimental studies.
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- Gobbo, Erik, 1990-, et al.
(författare)
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Shotgun sequencing of hymenopteran inhabitants of rose galls reveals a surprising lack of bacteria
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Annan publikation (övrigt vetenskapligt/konstnärligt)abstract
- In recent years, our knowledge of the microbiomes associated with insects has increased rapidly thanks to new sequencing methods, but the taxonomic and biological diversity of the studied insect species is still limited. Insects inhabiting galls represent a particularly interesting ecological guild that has not yet had its microbiome fully characterized, although it is well known that many gall insects are infected by Wolbachia. Here, we use shotgun sequencing to characterize the microbiome of the larvae of four hymenopteran species inhabiting bedeguar galls on roses: the gall inducer (Diplolepis rosae, Cynipidae), a phytophagous inquiline (Periclistus brandtii, Cynipidae), and two parasitoids (Torymus bedeguaris, Torymidae, and Orthopelma mediator, Ichneumonidae). Analyses with Metaphlan2 detected the presence of Wolbachia in two of the larvae (one of three Diplolepis larvae, and one of two Torymus larvae); three other bacteria detected by Metaphlan2 in high abundance could be shown to be false positives. An annotation screen of the assembled genomes gave similar results. Almost all contigs that were likely to be of bacterial origin matched Wolbachia; the few remaining ones were likely false positives. Matching the assemblies to proteomes of candidate symbionts showed that the two infected larvae contained a substantial portion of the Wolbachia genome while the other Diplolepis and Torymus larvae only contained small sections of it. Our results suggest that the bedeguar gall is largely devoid of bacteria except for Wolbachia. This could potentially be related to previous reports that galls induced by cynipids produce antibiotics. Our results fail to support the much-discussed hypothesis that symbiotic bacteria are involved in gall induction in cynipids.
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| 9. |
- Hartop, Emily, 1983-, et al.
(författare)
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Towards Large-Scale Integrative Taxonomy (LIT) : Resolving the Data Conundrum for Dark Taxa
- 2022
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Ingår i: Systematic Biology. - : Oxford University Press (OUP). - 1063-5157 .- 1076-836X. ; 71:6, s. 1404-1422
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Tidskriftsartikel (refereegranskat)abstract
- New, rapid, accurate, scalable, and cost-effective species discovery and delimitation methods are needed for tackling “dark taxa,” here defined as groups for which <<10%% of all species are described and the estimated diversity exceeds 1,000 species. Species delimitation for these taxa should be based on multiple data sources (“integrative taxonomy”) but collecting multiple types of data risks impeding a discovery process that is already too slow. We here develop large-scale integrative taxonomy (LIT), an explicit method where preliminary species hypotheses are generated based on inexpensive data that can be obtained quickly and cost-effectively. These hypotheses are then evaluated based on a more expensive type of “validation data” that is only obtained for specimens selected based on objective criteria applied to the preliminary species hypotheses. We here use this approach to sort 18,000 scuttle flies (Diptera: Phoridae) into 315 preliminary species hypotheses based on next-generation sequencing barcode (313 bp) clusters (using objective clustering [OC] with a 3%% threshold). These clusters are then evaluated with morphology as the validation data. We develop quantitative indicators for predicting which barcode clusters are likely to be incongruent with morphospecies by randomly selecting 100 clusters for in-depth validation with morphology. A linear model demonstrates that the best predictors for incongruence between barcode clusters and morphology are maximum p-distance within the cluster and a newly proposed index that measures cluster stability across different clustering thresholds. A test of these indicators using the 215 remaining clusters reveals that these predictors correctly identify all clusters that are incongruent with morphology. In our study, all morphospecies are true or disjoint subsets of the initial barcode clusters so that all incongruence can be eliminated by varying clustering thresholds. This leads to a discussion of when a third data source is needed to resolve incongruent grouping statements. The morphological validation step in our study involved 1,039 specimens (5.8%% of the total). The formal LIT protocol we propose would only have required the study of 915 (5.1%%: 2.5 specimens per species), as we show that clusters without signatures of incongruence can be validated by only studying two specimens representing the most divergent haplotypes. To test the generality of our results across different barcode clustering techniques, we establish that the levels of incongruence are similar across OC, Automatic Barcode Gap Discovery (ABGD), Poisson Tree Processes (PTP), and Refined Single Linkage (RESL) (used by Barcode of Life Data System to assign Barcode Index Numbers [BINs]). OC and ABGD achieved a maximum congruence score with the morphology of 89%% while PTP was slightly less effective (84%%). RESL could only be tested for a subset of the specimens because the algorithm is not public. BINs based on 277 of the original 1,714 haplotypes were 86%% congruent with morphology while the values were 89%% for OC, 74%% for PTP, and 72%% for ABGD.
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| 10. |
- Hearn, Jack, et al.
(författare)
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Phylogenomic analysis of protein-coding genes resolves complex gall wasp relationships
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Annan publikation (övrigt vetenskapligt/konstnärligt)abstract
- The phylogeny of gall wasps (Cynipidae) and their parasitic relatives has attracted considerable attention in recent years. The family is now widely recognized to fall into thirteen natural lineages, designated tribes, but the relationships among them have remained elusive. This has stymied any progress in understanding how cynipid gall inducers evolved from insect parasitoids, and what role inquilinism (development as a herbivore inside galls induced by other cynipids) might have played in this transition. A recent analysis of ultraconserved elements (UCEs) represents the first attempt at resolving these questions using phylogenomics. Here, we present the first analysis based on protein-coding sequences from genome and transcriptome assemblies. To address potential problems due to model misfit, we focus on models that accommodate site-specific amino-acid profiles and that are less sensitive than standard models to long-branch attraction. Our results show that the Cynipidae as previously circumscribed are not monophyletic. Specifically, the Paraulacini and a clade formed by Diplolepidini + Pediaspidini both fall outside a core clade (Cynipidae s. str.), which is more closely related to Figitidae. This result is robust to the exclusion of long-branch taxa that could potentially mislead the analysis, and it is consistent with the UCE analysis. Given this, we propose that the Cynipidae be divided into three families: the Paraulacidae, Diplolepididae and Cynipidae (s. str.). Our results suggest that the Eschatocerini are the sister group of the remaining Cynipidae (s. str.). Within the latter, our results are consistent with the UCE analysis but place two additional tribes: (1) the Aylacini (s. str.), more closely related to the oak gall wasps (Cynipini) and some of their inquilines (Ceroptresini) than to other herb gallers (Aulacideini and Phanacidini); and (2) the Qwaqwaiini, likely the sister group to Synergini (s. str.) + Rhoophilini. Several alternative scenarios for the evolution of cynipid life histories are compatible with the relationships suggested by our analysis, but all are complex and require multiple shifts between parasitoids, inquilines and gall inducers. Linking the different types of life-history transitions to specific genomic signatures may be one of the best ways of differentiating among these alternative scenarios. Our study represents the first step towards enabling such analyses.
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