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RESEARCH ARTICLE

UCE-based phylogenomics of the lepidopteran endoparasitoid wasp subfamily Rogadinae (Hymenoptera: Braconidae) unveils a new Neotropical tribe

Eduardo M. Shimbori https://orcid.org/0000-0003-4655-2591 A B C D , Rubén Castañeda-Osorio https://orcid.org/0000-0003-0507-5477 A , Jovana M. Jasso-Martínez https://orcid.org/0000-0001-6497-7150 A E , Angélica M. Penteado-Dias https://orcid.org/0000-0002-8371-5591 B , Sian S. Gadelha https://orcid.org/0000-0002-6612-6672 F , Seán G. Brady https://orcid.org/0000-0003-0468-940X E , Donald L. J. Quicke https://orcid.org/0000-0003-4471-6775 G , Robert R. Kula H and Alejandro Zaldívar-Riverón https://orcid.org/0000-0001-5837-1929 A *
+ Author Affiliations
- Author Affiliations

A Colección Nacional de Insectos, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico.

B Departamento de Ecologia e Biologia Evolutiva, Universidade Federal de São Carlos, São Carlos, São Paulo, Brazil.

C Centre de coopération internationale en recherche agronomique pour lle développement (CIRAD), Centre de Biologie pour la Gestion de Populations (CBGP), Montpellier, F-34398, France.

D CIRAD, CBGP, Institute National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAe), Institut Agro, Institut de Recherche pour le Développement (IRD), Université de Montpellier, Montpellier, France.

E Department of Entomology, Smithsonian Institution, National Museum of Natural History, 10th Street & Constitution Avenue NW, Washington, DC 20560, USA.

F Laboratório de Biologia e Diversidade de Insetos, Universidade Federal de Rondônia, Porto Velho, Rondônia, Brazil.

G Integrative Insect Ecology Research Unit, Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok, Thailand.

H Systematic Entomology Laboratory, Beltsville Agricultural Research Center, Agricultural Research Service, US Department of Agriculture, c/o Department of Entomology, Smithsonian Institution, National Museum of Natural History, Washington, DC, USA.

* Correspondence to: azaldivar@ib.unam.mx

Handling Editor: Andy Austin

Invertebrate Systematics 38, IS24040 https://doi.org/10.1071/IS24040
Submitted: 3 May 2024  Accepted: 16 July 2024  Published: 8 August 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

During the past two decades, the phylogenetic relationships and higher-level classification of the subfamily Rogadinae have received relevant contributions based on Sanger, mitogenome and genome-wide nuclear DNA sequence data. These studies have helped to update the circumscription and tribal classification of this subfamily, with six tribes currently recognised (Aleiodini, Betylobraconini, Clinocentrini, Rogadini, Stiropiini and Yeliconini). The tribal relationships within Rogadinae, however, are yet to be fully resolved, including the status of tribe Facitorini, previously regarded as betylobraconine, with respect to the members of Yeliconini. We conducted a phylogenomic analysis among the tribes of Rogadinae based on genomic ultraconserved element (UCE) data and extensive taxon sampling including three undescribed genera of uncertain tribal placement. Our almost fully supported estimate of phylogeny confirmed the basal position of Rogadini within the subfamily and a Facitorini clade (Yeliconini + Aleiodini) that led us to propose the former group as a valid rogadine tribe (Facitorini stat. res.). Stiropiini, however, was recovered for the first time as sister to the remaining rogadine tribes except Rogadini, and Clinocentrini as sister to a clade with Betylobraconini + the three undescribed genera. The relationships recovered and morphological examination of the material included led us to place the latter three new genera and recently described genus Gondwanocentrus within a new rogadine tribe, Gondwanocentrini Shimbori & Zaldívar-Riverón trib. nov. We described these genera (Ghibli Shimbori & Zaldívar-Riverón gen. nov., Racionais Shimbori & Zaldívar-Riverón gen. nov. and Soraya Shimbori gen. nov.) with two or three new species each (G. miyazakii Shimbori & Zaldívar-Riverón sp. nov., G. totoro Shimbori & Zaldívar-Riverón sp. nov., R. brunus Shimbori & Zaldívar-Riverón sp. nov., R. kaelejay Shimbori & Zaldívar-Riverón sp. nov., R. superstes Shimbori & Zaldívar-Riverón sp. nov., S. alencarae Shimbori sp. nov. and S. venus Shimbori & Zaldívar-Riverón sp. nov.). A new species of Facitorini, Jannya pasargadae Gadelha & Shimbori sp. nov., is also described. Our newly proposed classification expands the number of tribes and genera within Rogadinae to 8 and 66 respectively.

ZooBank: urn:lsid:zoobank.org:pub:51951C78-069A-4D8B-B5F0-7EBD4D9D21CE

Keywords: cyclostome, Ichneumonoidea, Neotropics, Parasitica, phylogenetics, phylogenomics, taxonomic classification, ultraconserved elements.

References

Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19(5), 455-477.
| Crossref | Google Scholar | PubMed |

Belokobylskij SA, Zaldívar-Riverón A, Maetô K, Sáez AG (2008) Asian Betylobraconinae (Hymenoptera, Braconidae), with description of a new genus and phylogenetic affinities of the tribe Facitorini. Insect Systematics and Evolution 39, 133-154.
| Crossref | Google Scholar |

Blumenstiel B, Cibulskis K, Fisher S, DeFelice M, Barry A, Gabriel S (2010) Targeted exon sequencing by in-solution hybrid selection. Current Protocols in Human Genetics 66(1), 18.4.1-18.4.24.
| Crossref | Google Scholar |

Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15), 2114-2120.
| Crossref | Google Scholar | PubMed |

Branstetter MG, Longino JT, Ward PS, Faircloth BC, Price S (2017) Enriching the ant tree of life: enhanced UCE bait set for genome-scale phylogenetics of ants and other Hymenoptera. Methods in Ecology and Evolution 8(6), 768-776.
| Crossref | Google Scholar |

Butcher BA, Quicke DL (2015) A remarkable new genus and species of Rogadinae (Hymenoptera: Braconidae) of uncertain tribal placement, from Papua New Guinea, resembling Betylobraconini stat. nov. Journal of Natural History 49, 2045-2054.
| Crossref | Google Scholar |

Butcher BA, Zaldivar-Riverón A, Van De Kamp T, Dos Santos Rolo T, Baumbach T, Quicke DLJ (2014) Extension of historical range of Betylobraconinae (Hymenoptera: Braconidae) into Palaearctic Region based on a Baltic amber fossil, and description of a new species of Mesocentrus Szépligeti from Papua New Guinea. Zootaxa 3860, 449-463.
| Crossref | Google Scholar | PubMed |

Butcher BA, Quicke DLJ, Shreevihar S, Ranjith AP (2016) Major range extensions for two genera of the parasitoid subtribe Facitorina, with a new generic synonymy (Braconidae, Rogadinae, Yeliconini). ZooKeys 584, 109-120.
| Crossref | Google Scholar | PubMed |

Cameron P (1911) On the Hymenoptera of the Georgetown Museum, British Guiana. Part II. Timehri 1, 306-330.
| Google Scholar |

Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540-552.
| Crossref | Google Scholar | PubMed |

Ceccarelli FS, Sharkey MJ, Zaldívar-Riverón A (2012) Species identification in the taxonomically neglected, highly diverse, neotropical parasitoid wasp genus Notiospathius (Braconidae: Doryctinae) based on an integrative molecular and morphological approach. Molecular Phylogenetics and Evolution 62, 485-495.
| Crossref | Google Scholar | PubMed |

Chen XX, Piao MH, Whitfield J, He JH (2003) A molecular phylogeny of the subfamily Rogadinae (Hymenoptera: Braconidae) based on the D2 variable region of 28S ribosomal RNA. Acta Entomologica Sinica 46, 209-217.
| Google Scholar |

Faircloth BC (2016) PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics 32(5), 786-788.
| Crossref | Google Scholar | PubMed |

Fortier JC, Shaw SR (1999) Cladistics of the Aleiodes lineage of the subfamily Rogadinae (Hymenoptera: Braconidae). Journal of Hymenoptera Research 8, 204-237.
| Google Scholar |

Gillespie JJ, Munro JB, Heraty JM, Yoder MJ, Owen AK, Carmichael AE (2005) A secondary structural model of the 28S rRNA expansion segments D2 and D3 for chalcidoid wasps (Hymenoptera: Chalcidoidea). Molecular Biology and Evolution 22(7), 1593-1608.
| Crossref | Google Scholar |

Glenn TC, Nilsen RA, Kieran TJ, Sanders JG, Bayona-Vásquez NJ, Finger JW, Pierson TW, Bentley KE, Hoffberg SL, Louha S, Garcia-De Leon FJ, Del Rio Portilla MA, Reed KD, Anderson JL, Meece JK, Aggrey SE, Rekaya R, Alabady M, Belanger M, Winker K, Faircloth BC (2019) Adapterama I: universal stubs and primers for 384 unique dual-indexed or 147,456 combinatorially indexed Illumina libraries (iTru & iNext). PeerJ 7, e7755 PMCID: PMC6791352.
| Crossref | Google Scholar | PubMed |

Harris RA (1979) A glossary of surface sculpturing. Occasional Papers in Entomology 28, 1-31.
| Crossref | Google Scholar |

Heath TA, Hedtke SM, Hillis DM (2008) Taxon sampling and the accuracy of phylogenetic analyses. Journal of Systematics and Evolution 46(3), 239-257.
| Google Scholar |

Hebert PDN, Ratnasingham S, De Waard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London – B. Biological Sciences 270(Suppl.), S96-S99.
| Crossref | Google Scholar | PubMed |

Hoang DT, Chernomor O, Von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35, 518-522.
| Crossref | Google Scholar | PubMed |

Jasso-Martínez JM, Quicke DLJ, Belokobylskij SA, Meza-Lázaro RN, Zaldívar- Riverón A (2021) Phylogenomics of the lepidopteran endoparasitoid wasp subfamily Rogadinae (Hymenoptera: Braconidae) and related subfamilies. Systematic Entomology 46, 83-95.
| Crossref | Google Scholar |

Jasso-Martínez JM, Quicke DLJ, Belokobylskij SA, Santos BF, Fernández-Triana JL, Kula RR, Zaldívar-Riverón A (2022a) Mitochondrial phylogenomics and mitogenome organization in the parasitoid wasp family Braconidae (Hymenoptera: Ichneumonoidea). BMC Ecology and Evolution 22(1), 46.
| Crossref | Google Scholar | PubMed |

Jasso-Martínez JM, Santos BF, Zaldívar-Riverón A, Fernández-Triana JL, Sharanowski BJ, Richter R, et al. (2022b) Phylogenomics of braconid wasps (Hymenoptera, Braconidae) sheds light on classification and the evolution of parasitoid life history traits. Molecular Phylogenetics and Evolution 173, 107452.
| Crossref | Google Scholar | PubMed |

Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587-589.
| Crossref | Google Scholar | PubMed |

Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30(4), 772-780.
| Crossref | Google Scholar | PubMed |

Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059-3066.
| Crossref | Google Scholar | PubMed |

Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable, and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35, 4453-4455.
| Crossref | Google Scholar | PubMed |

Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772-773.
| Crossref | Google Scholar |

Maeto K, Arakaki N (2005) Gregarious emergence of Macrostomion sumatranum (Hymenoptera: Braconidae; Rogadinae) from the mummified, full‐grown larvae of Theretra silhetensis (Lepidoptera: Sphingidae). Entomological Science 8(2), 131-132.
| Crossref | Google Scholar |

Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, Von Haeseler A, Lanfear R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37(5), 1530-1534.
| Crossref | Google Scholar | PubMed |

Quicke DLJ, Butcher BA (2015) Description of a new Betylobraconini-like parasitoid wasp genus and species (Hymenoptera: Braconidae: Rogadinae) from Chile. Zootaxa 4021, 459-466.
| Crossref | Google Scholar | PubMed |

Quicke DLJ, Shaw MR (2006) First host records for the rogadine genera Rogasodes Chen & He and Canalirogas van Achterberg & Chen (Hymenoptera: Braconidae) with description of a new species and survey of mummy types within Rogadinae s. str. Journal of Natural History 39, 3525-3542.
| Crossref | Google Scholar |

Quicke DLJ, Smith MA, Miller SE, Hrcek J, Butcher B (2012a) Colastomion Baker (Braconidae, Rogadinae): nine new species from Papua New Guinea reared from Crambidae. Journal of Hymenoptera Research 28, 85-121.
| Crossref | Google Scholar |

Quicke DLJ, Smith MA, van Achterberg C, Miller SE, Hrcek J (2012b) A new genus and three new species of parasitoid wasp from Papua New Guinea and redescription of Trigonophatnus Cameron (Hymenoptera, Braconidae, Rogadinae). Journal of Natural History 46, 1369-1385.
| Crossref | Google Scholar |

Quicke DLJ, Shaw MR, van , Achterberg C, Bland KP, Butcher BA, Lyszkowski R, Zhang YM (2014) A new Australian genus and five new species of Rogadinae (Hymenoptera: Braconidae), one reared as a gregarious endoparasitoid of an unidentified limacodid (Lepidoptera). Zootaxa 3881, 237-257.
| Crossref | Google Scholar | PubMed |

Quicke DLJ, Belokobylskij SA, Smith MA, Rota J, Hrcek J, Butcher BA (2016) A new genus of rhysipoline wasp (Hymenoptera: Braconidae) with modified wing venation from Africa and Papua New Guinea, parasitoid on Choreutidae (Lepidoptera). Annales Zoologici 66(2), 173-192.
| Crossref | Google Scholar |

Quicke DLJ, Kuslitzky W, Butcher BA (2018) First host record for Old World Yelicones (Hymenoptera: Braconidae: Rogadinae) adds to evidence that they are strictly parasitoids of Pyralidae (Lepidoptera). Israel Journal of Entomology 48, 33-40.
| Google Scholar |

Quicke DLJ, Ward DF, Belokobylskij SA, Butcher BA (2020) Zealastoa Quicke & Ward, gen. nov., a new basal cyclostome braconid wasp (Hymenoptera: Braconidae) from New Zealand. Austral Entomology 59, 455-466.
| Crossref | Google Scholar |

Quicke DLJ, Fagan-Jeffries EP, Jasso-Martínez JM, Zaldívar-Riverón A, Shaw MR, Butcher BA (2021) A molecular phylogeny of the parasitoid wasp subfamily Rogadinae (Hymenoptera: Ichneumonoidea: Braconidae) with descriptions of three new genera. Systematic Entomology 46, 1019-1044.
| Crossref | Google Scholar |

Sakagami K, Shimizu S, Fujie S, Maeto K (2020) Revisiting the host use and phylogeny of Colastomion Baker (Hymenoptera, Braconidae, Rogadinae), with a new host record from Japan. Journal of Hymenoptera Research 77, 175-186.
| Crossref | Google Scholar |

Sharanowski BJ, Dowling APG, Sharkey MJ (2011) Molecular phylogenetics of Braconidae (Hymenoptera: Ichneumonoidea), based on multiple nuclear genes, and implications for classification. Systematic Entomology 36, 549-572.
| Crossref | Google Scholar |

Sharkey MJ (1997)Key to New World subfamilies of the family Braconidae. In ‘Manual of the New World genera of the family Braconidae’. (Eds RA Wharton, PM Marsh, MJ Sharkey) Special publication of the International Society of Hymenopterists, vol. 1, pp. 39–63. (International Society of Hymenopterists: Washington, DC, USA)

Sharkey MJ, Wharton RA (1997). Morphology & terminology. In ‘Manual of the New World genera of the family Braconidae’. (Eds RA Wharton, PM Marsh, MJ Sharkey) Special publication of the International Society of Hymenopterists, vol. 1, pp. 19–37. (International Society of Hymenopterists: Washington, DC, USA)

Sharkey M, Athey KJ, Fernández-Triana JL, Penteado-Dias AM, Monckton SK, Quicke DLJ (2023) Key to the New World subfamilies of the family Braconidae (Hymenoptera). Canadian Journal of Arthropod Identification 2023, 49.
| Crossref | Google Scholar |

Shaw MR (1983) On evolution of endoparasitism: the biology of some genera of Rogadinae (Braconidae). Contributions of the American Entomological Institute 20, 307-328.
| Google Scholar |

Shaw SR (1997) Subfamily Rogadinae s.s. In ‘Manual of the New World genera of the family Braconidae’. (Eds RA Wharton, PM Marsh, MJ Sharkey) Special publication of the International Society of Hymenopterists, vol. 1, pp. 403–412. (International Society of Hymenopterists: Washington, DC, USA)

Shaw MR (2002) A new species of Macrostomion Szépligeti (Hymenoptera: Braconidae: Rogadinae) from Papua New Guinea, with notes on the biology of the genus. Zoologische Mededelingen, Leiden 76(14), 133-140.
| Google Scholar |

Shaw MR, Huddleston T (1991) Classification and biology of braconid wasps (Hymenoptera: Braconidae). In ‘Handbooks for the identification of British insects. Vol. 7’. (Eds WR Dolling, RR Askew) pp. 1–126. (Royal Entomological Society of London: London, UK)

Shaw SR, Marsh PM, Fortier JC (1998) Revision of North American Aleiodes (part 2): the apicalis species-group in the New World. Journal of Hymenoptera Research 7, 62-73.
| Google Scholar |

Tagliacollo VA, Lanfear R (2018) Estimating improved partitioning schemes for ultraconserved elements. Molecular Biology and Evolution 35, 1798-1811.
| Crossref | Google Scholar | PubMed |

Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564-577.
| Crossref | Google Scholar | PubMed |

van Achterberg C (1988) Revision of the subfamily Blacinae Foerster (Hymenoptera: Braconidae). Zoologische Verhandelingen 249, 1-324.
| Google Scholar |

van Achterberg C (1993) Illustrated key to the subfamilies of the Braconidae (Hymenoptera: Ichneumonoidea). Zoologische Verhandelingen 283, 1-189.
| Google Scholar |

van Achterberg C (1995) Generic revision of the subfamily Bethylobraconinae (Hymenoptera: Braconidae) and other groups with modified fore tarsus. Zoologische Verhandelingen 298, 1-242.
| Google Scholar |

van Achterberg C (1997) Subfamily Betylobraconinae. In ‘Manual of the New World genera of the family Braconidae’. (Eds RA Wharton, PM Marsh, MJ Sharkey) Special publication of the International Society of Hymenopterists, vol. 1, pp. 137–139. (International Society of Hymenopterists: Washington, DC, USA)

van Achterberg C, Shaw MR, Quicke DLJ (2020) Revision of the western Palaearctic species of Aleiodes Wesmael (Hymenoptera, Braconidae, Rogadinae). Part 2: revision of the A. apicalis group. ZooKeys 919, 1-259.
| Crossref | Google Scholar | PubMed |

Whitfield JB (1992) The polyphyletic origin of endoparasitism in the cyclostome lineages of Braconidae (Hymenoptera). Systematic Entomology 17, 273-286.
| Crossref | Google Scholar |

Zaldívar-Riverón A, Mori M, Quicke DLJ (2006) Systematics of the cyclostome subfamilies of braconid parasitic wasps (Hymenoptera: Ichneumonoidea): a simultaneous molecular and morphological Bayesian approach. Molecular Phylogenetics and Evolution 38, 130-145.
| Crossref | Google Scholar | PubMed |

Zaldívar-Riverón A, Shaw MR, Sáez AG, Mori M, Belokoblylskij SA, Shaw SR, Quicke DLJ (2008) Evolution of the parasitic wasp subfamily Rogadinae (Braconidae): phylogeny and evolution of lepidopteran host ranges and mummy characteristics. BMC Evolutionary Biology 8, 329.
| Crossref | Google Scholar | PubMed |

Zwickl DJ, Hillis DM (2002) Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology 51, 588-598.
| Crossref | Google Scholar | PubMed |