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Diversity, speciation and evolutionary history of the twisted-winged parasite genus Stylops (Strepsiptera): A genomic approach
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0001-9868-3134
2025 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Despite their captivating peculiarity, the insect order Strepsiptera, commonly known as twisted-winged parasites, remains relatively poorly known. Advancements in molecular methods have provided researchers with new tools to address evolutionary questions about the order previously difficult to resolve due to the challenging morphology of Strepsipterans. Stylops, one of the largest genera of Strepsiptera, has had its fair share of these challenges. Stylops are obligate endoparasites of Andrena mining bees, and taxonomists working with the genus have used species concepts with varying degrees of host specificity. This has led to conflicting species hypotheses and unresolved phylogenetic relationships. Furthermore, key evolutionary processes, such as host coevolution and drivers of speciation, have largely remained unexplored. In this thesis, I use genomic-scale data to both clarify the taxonomy of Stylops and to investigate the evolutionary history and processes within the genus. In chapter I, we apply whole-genome sequencing to produce a comprehensive molecular data set focused on West Palaearctic Stylops species. Over 2000 genes were used in species delimitation analyses to evaluate existing and conflicting species hypotheses. We found justification for synonymization of multiple species, indications of undescribed species, and confirmed new host-parasite relationships, clarifying the West Palaearctic species diversity of Stylops. In chapter II, we infer a phylogeny of the genus based on thousands of loci, including newly sequenced Nearctic species. Additionally, we assess the biogeographic history and coevolutionary patterns with their host. The used inference methods produced fully resolved phylogenies with high support values and only minor topological differences between the methods. We found Stylops to originate in the West Palaearctic or West Palaearctic and Nearctic in the early Neogene or late Palaeogene and diversification of Stylops to be shaped by both coevolution and host-shifting. In chapter III we investigate what drives divergence in six species or species groups of Stylops using a genome-wide SNP dataset. We found that, depending on the species, both geographic distance and host association each play important roles for genetic differentiation, highlighting how contrasting processes may shape speciation even in closely related species. In chapter IV, we review the Nordic Strepsiptera fauna based on the current taxonomic knowledge and describe two new Stylops species that were identified as undescribed species in earlier chapters. Additionally, we gather an extensive species occurrence record set of Strepsiptera from the Nordic countries based on museum and private collections, and online databases. The overall aim of this thesis is to apply genomic data to answer questions of species diversity, host association, drivers of speciation and evolutionary history of the genus Stylops to increase our knowledge and understanding of these fascinating insects.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2025. , p. 39
Keywords [en]
Stylops, Strepsiptera, Species delimitation, Phylogenomics, Coevolution, Speciation
National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
URN: urn:nbn:se:su:diva-236989ISBN: 978-91-8107-054-5 (print)ISBN: 978-91-8107-055-2 (electronic)OAI: oai:DiVA.org:su-236989DiVA, id: diva2:1919665
Public defence
2025-02-07, Lilla Hörsalen, Naturhistoriska riksmuseet, Frescativägen 40, Stockholm, 13:00 (English)
Opponent
Supervisors
Available from: 2025-01-15 Created: 2024-12-09 Last updated: 2024-12-20Bibliographically approved
List of papers
1. Phylogenomic species delimitation of the twisted-winged parasite genus Stylops (Strepsiptera)
Open this publication in new window or tab >>Phylogenomic species delimitation of the twisted-winged parasite genus Stylops (Strepsiptera)
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2024 (English)In: Systematic Entomology, ISSN 0307-6970, E-ISSN 1365-3113, Vol. 49, no 2, p. 294-313Article in journal (Refereed) Published
Abstract [en]

The twisted-winged parasite genus Stylops has a history of different species concepts with varying host specificity resulting in diverse species diversity estimates in different regions of the Holarctic. The adoption of a supergeneralist species concept in Europe, proposing synonymization of all Western Palaearctic Stylops species, did not facilitate taxonomic clarity and obscured the available life-history data in the region for decades. Lack of molecular data has allowed divergent opinions on species hypotheses and little opportunity for evaluating them in this morphologically challenging genus. To solve these discrepancies and gain novel information about host associations, we applied whole-genome sequencing to 163 specimens, representing a significant portion of putative European species. We evaluate the existing and conflicting species hypotheses with molecular species delimitation using Species bOundry Delimitation using Astral (SODA) and use a maximum likelihood phylogeny to investigate host associations of the species. Furthermore, we evaluate the effect of a number of loci used in SODA for the number of inferred species. We find justification for synonymization of multiple species and indications of undescribed species, as well as new host–parasite relationships. We show that the number of inferred species in SODA is exceedingly and positively correlated with the number of loci used, urging for cautious application. The results of our study bring clarity to the Western Palaearctic species diversity of Stylops. Furthermore, the comprehensive molecular dataset generated in this study will be a valuable resource for future studies on Stylops and the evolution of parasites in general. 

Keywords
phylogenomics, SODA, species delimitation, Strepsiptera, Stylops, whole-genome sequencing
National Category
Biological Systematics
Identifiers
urn:nbn:se:su:diva-225756 (URN)10.1111/syen.12618 (DOI)001124183100001 ()2-s2.0-85179330581 (Scopus ID)
Available from: 2024-01-23 Created: 2024-01-23 Last updated: 2024-12-09Bibliographically approved
2. Phylogenomic analysis of Stylops reveals the evolutionary history of a Holarctic Strepsiptera radiation parasitizing wild bees
Open this publication in new window or tab >>Phylogenomic analysis of Stylops reveals the evolutionary history of a Holarctic Strepsiptera radiation parasitizing wild bees
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2024 (English)In: Molecular Phylogenetics and Evolution, ISSN 1055-7903, E-ISSN 1095-9513, Vol. 195, article id 108068Article in journal (Refereed) Published
Abstract [en]

Holarctic Stylops is the largest genus of the enigmatic insect order Strepsiptera, twisted winged parasites. Members of Stylops are obligate endoparasites of Andrena mining bees and exhibit extreme sexual dimorphism typical of Strepsiptera. So far, molecular studies on Stylops have focused on questions on species delimitation. Here, we utilize the power of whole genome sequencing to infer the phylogeny of this morphologically challenging genus from thousands of loci. We use a species tree method, concatenated maximum likelihood analysis and Bayesian analysis with a relaxed clock model to reconstruct the phylogeny of 46 Stylops species, estimate divergence times, evaluate topological consistency across methods and infer the root position. Furthermore, the biogeographical history and coevolutionary patterns with host species are assessed. All methods recovered a well resolved topology with close to all nodes maximally supported and only a handful of minor topological variations. Based on the result, we find that included species can be divided into 12 species groups, seven of them including only Palaearctic species, three Nearctic and two were geographically mixed. We find a strongly supported root position between a clade formed by the spretathwaitesi and gwynanae species groups and the remaining species and that the sister group of Stylops is Eurystylops or Eurystylops + Kinzelbachus. Our results indicate that Stylops originated in the Western Palaearctic or Western Palaearctic and Nearctic in the early Neogene or late Paleogene, with four independent dispersal events to the Nearctic. Cophylogenetic analyses indicate that the diversification of Stylops has been shaped by both significant coevolution with the mining bee hosts and host-shifting. The well resolved and strongly supported phylogeny will provide a valuable phylogenetic basis for further studies into the fascinating world of Strepsipterans.

Keywords
Phylogenomics, Strepsiptera, Stylops, Coevolution, Parasitism, Whole-genome sequencing
National Category
Evolutionary Biology Genetics and Genomics
Identifiers
urn:nbn:se:su:diva-232517 (URN)10.1016/j.ympev.2024.108068 (DOI)001227813000001 ()38554985 (PubMedID)2-s2.0-85190277934 (Scopus ID)
Available from: 2024-08-20 Created: 2024-08-20 Last updated: 2025-02-01Bibliographically approved
3. Geography and host-association drive genetic differentiation in Stylops twisted-winged parasites
Open this publication in new window or tab >>Geography and host-association drive genetic differentiation in Stylops twisted-winged parasites
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(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:su:diva-237153 (URN)
Available from: 2024-12-12 Created: 2024-12-12 Last updated: 2024-12-12
4. Review of the Strepsiptera fauna of Nordic countries with the description of two new species of Stylops Kirby (Stylopidae)
Open this publication in new window or tab >>Review of the Strepsiptera fauna of Nordic countries with the description of two new species of Stylops Kirby (Stylopidae)
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(English)Manuscript (preprint) (Other academic)
National Category
Biological Systematics
Identifiers
urn:nbn:se:su:diva-237156 (URN)
Available from: 2024-12-12 Created: 2024-12-12 Last updated: 2024-12-12

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Lähteenaro, Meri

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