Phylogenetic affinities of the non-cyclostome subfamilies Amicrocentrinae and Dirrhopinae (Hymenoptera, Braconidae) confirmed by ultraconserved element data
Authors/Creators
- 1. Smithsonian Institution, National Museum of Natural History, Washington D.C., United States of America
Description
The subfamilies Amicrocentrinae and Dirrhopinae (Hymenoptera, Braconidae) are two small, monogeneric braconid subfamilies whose species exclusively attack lepidopteran larvae. The phylogenetic placement of Amicrocentrinae as a member of the helconoid complex of subfamilies has been supported by morphological and nuclear Sanger sequence data. The subfamilial status of Dirrhopinae on the other hand has been subject to debate, although it has been suggested as closely related to the microgastroid complex based on morphology only. Here we generated for the first time genomic ultraconserved element data for members of the above subfamilies (Amicrocentrum seyrigi van Achterberg and Dirrhope americana Muesebeck) to assess their phylogenetic affinities using exhaustive taxon sampling that includes all but one of the currently valid braconid subfamilies. Our results strongly confirm the placement of both taxa within the non-cyclostome helconoid and microgastroid complexes, respectively.
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References
- Banks JC, Whitfield JB (2006) Dissecting the ancient rapid radiation of microgastrine wasp genera using additional nuclear genes. Molecular Phylogenetics and Evolution 4: 690–703. https://doi.org/10.1016/j.ympev.2006.06.001
- Belokobylskij SA (1989) Eastern Palaearctic braconid species of the genera Dirrhope and Mirax (Hymenoptera, Braconidae, Miracinae). Vestnik Zoologii 4: 34–46.
- Belokobylskij SA, Iqbal M, Austin AD (2003) First record of the subfamily Dirrhopinae (Hymenoptera: Braconidae) from the Australian region, with a discussion of relationships and biology. Australian Journal of Entomology 42: 260–265. https://doi.org/10.1046/j.1440-6055.2003.00362.x
- Belshaw R, Fitton M, Herniou E, Gimeno C, Quicke DLJ (1998) A phylogenetic reconstruction of the Ichneumonoidea (Hymenoptera) based on the D2 variable region of 28S ribosomal RNA. Systematic Entomology 23: 109–123. https://doi.org/10.1046/j.1365-3113.1998.00046.x
- Blaimer BB, Santos BF, Cruaud A, Gates MW, Kula RR, Mikó I, Rasplus JY, Smith DR, Talamas EJ, Brady SG, Buffington ML (2023) Key innovations and the diversification of Hymenoptera. Nature Communications 14: 1212. https://doi.org/10.1038/s41467-023-36868-4
- Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120. https://doi.org/10.1093/bioinformatics/btu170
- Branstetter MG, Longino JT, Ward PS, Faircloth BC (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: 768–776. https://doi.org/10.1111/2041-210X.12742
- Capek M (1970) A new classification of the Braconidae (Hymenoptera) based on the cephalic structure of the final instar larvae and biological evidence. The Canadian Entomologists 102: 846–875. https://doi.org/10.4039/Ent102846-7
- Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
- Dangerfield PC, Austin AD (1998) Biology of the Mesostoa kerri Austin and Wharton (Insecta: Hymenoptera: Braconidae: Mesostoinae), an endemic Australian wasp that causes stem galls on Banksia marginata. Australian Journal of Botany 46: 559–569. https://doi.org/10.1071/BT97042
- Del Fabbro C, Scalabrin S, Morgante M, Giorgi FM (2013) An extensive evaluation of read trimming effects on Illumina NGS data analysis. PLoS ONE 8: e85024. https://doi.org/10.1371/journal.pone.0085024
- Dowton M, Austin AD (1998) Phylogenetic relationships among the microgastroid wasps (Hymenoptera: Braconidae): combined analysis of 16S and 28S rDNA genes and morphological data. Molecular Phylogenetics and Evolution 10: 354–366. https://doi.org/10.1006/mpev.1998.0533
- Dowton M, Belshaw R, Austin AD, Quicke DLJ (2002) Simultaneous molecular and morphological analysis of braconid relationships (Insecta: Hymenoptera: Braconidae) indicates independent mt-tRNA gene inversions within a single wasp family. Journal of Molecular Evolution 54: 210–226. https://doi.org/10.1007/s00239-001-0003-3
- Faircloth BC (2013) Illumiprocessor: A Trimmomatic Wrapper for Parallel Adapter and Quality Trimming. https://doi.org/10.6079/J9ILL
- Faircloth BC (2016) PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics 32(7): 86–788. https://doi.org/10.1093/bioinformatics/btv646
- Glenn TC, Nilsen RA, Kieran TJ, Sanders JG, Bayona-Vásquez N, Finger JW, Pierson TW, Bentley KE, Hoffberg SL, Louha S, García-De Leon FJ, del Río Portilla MA, Reed KD, Anderson JL, Meece JK, Aggrey SE, Rekaya R, Alabady M, Belanger M, Winker K, Faircloth BC (2016) Adapterama I: universal stubs and primers for thousands of dual-indexed Illumina libraries (iTru and iNext). PeerJ 7: e7755. https://doi.org/10.7717/peerj.7755
- Infante F, Hanson P, Wharton R (1995) Phytophagy in the genus Monitoriella (Hymenoptera: Braconidae) with description of new species. Annals of the Entomological Society of America 88: 406–415. https://doi.org/10.1093/aesa/88.4.406
- Jasso-Martínez JM, Santos BF, Zaldívar-Riverón A, Fernández-Triana JL, Sharanowski BJ, Richter R, Dettman JR, Blaimer BB, Brady SG, Kula RR (2022a) Phylogenomics of braconid wasps (Hymenoptera, Braconidae) sheds light on classification and the evolution of parasitoid life history traits. Molecular Phylogenetics and Evolution 173: 107452. https://doi.org/10.1016/j.ympev.2022.107452
- Jasso-Martínez JM, Quicke DLJ, Belokobylskij SA, Santos BF, Fernández-Triana JL, Kula RR, Zaldívar-Riverón A (2022b) Mitochondrial phylogenomics and mitogenome organization in the parasitoid wasp family Braconidae (Hymenoptera: Ichneumonoidea). BMC Ecology and Evolution 22: 46. https://doi.org/10.1186/s12862-022-01983-1
- Kalyaanamoorthy S, Min BQ, Wong TK, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589. https://doi.org/10.1038/nmeth.4285
- Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
- Kittel RN, Austin AD, Klopfstein S (2016) Molecular and morphological phylogenetics of chelonine parasitoid wasps (Hymenoptera: Braconidae), with a critical assessment of divergence time estimations. Molecular Phylogenetics and Evolution 101: 224–241. https://doi.org/10.1016/j.ympev.2016.05.016
- Marsh PM (1979) Family Braconidae. In: Krombein KV, Hurd PD, Smith DR, Burks BD (Eds) Catalog of the Hymenoptera in America North of Mexico. Smithsonian Institution Press (Washington, D.C.), 144–313.
- Mason WRM (1983) A new South African subfamily related to Cardiochilinae (Hymenoptera: Braconidae). Contributions of the American Entomological Institute 2: 49–62.
- 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: 1530–1534. https://doi.org/10.1093/molbev/msaa015
- Muesebeck CFW (1935) On two little known genera of Braconidae (Hymenoptera). Proceedings of the Entomological Society of Washington 37: 173–177.
- Murphy N, Banks J, Whitfield JB, Austin A (2008) Phylogeny of the parasitic microgastroid subfamilies (Hymenoptera: Braconidae) based on sequence data from seven genes, with an improved time estimate of the origin of the lineage. Molecular Phylogenetics and Evolution 47: 378–395. https://doi.org/10.1016/j.ympev.2008.01.022
- Nixon GEJ (1965) A reclassification of the tribe Microgasterini (Hymenoptera: Braconidae). Bulletin of the British Museum (Natural History) Entomology 2: 284. https://doi.org/10.5962/p.144036
- Pitz KM, Dowling APG, Sharanowski BJ, Boring CA, Seltmann KC, Sharkey MJ (2007) Phylogenetic relationships among the Braconidae (Hymenoptera: Ichneumonoidea): A reassessment of Shi et al. (2005). Molecular Phylogenetics and Evolution 43: 338–343. https://doi.org/10.1016/j.ympev.2006.11.010
- Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A (2020) Using SPAdes de novo assembler. Current Protocols in Bioinformatics 70: e102. https://doi.org/10.1002/cpbi.102
- Quick DLJ (2015) The braconid and ichneumonid parasitoid wasps: biology, systematics, evolution and ecology. John Wiley & Sons (Chichester): 1–537. https://doi.org/10.1002/9781118907085
- Quicke DLJ, van Achterberg C (1990) Phylogeny of the subfamilies of the family Braconidae (Hymenoptera). Zoologische Verhandelingen 258: 1–95. https://doi.org/10.1111/j.1096-0031.1992.tb00068.x
- Quicke DLJ, Fitton MG, Harris J (1995) Ovipositor steering mechanisms in braconid wasps. Journal of Hymenoptera Research 4: 110–120.
- Rahman MH, Fitton MG, Quicke DLJ (1998) Ovipositor internal microsculpture in the Braconidae (Insecta, Hymenoptera). Zoologica Scripta 27: 319–331. https://doi.org/10.1111/j.1463-6409.1998.tb00464.x
- Ranjith AP, Quicke DLJ, Saleem UKA, Butcher BA, Zaldívar-Riverón A, Nasser M (2016) Entomophytophagy ('Sequential predatory, then phytophagous behaviour') in an Indian braconid 'parasitoid' wasp (Hymenoptera): specialized larval morphology, biology and description of a new species. PLoS ONE 11: e0156997. https://doi.org/10.1371/journal.pone.0156997
- Sharanowski BJ, Dowling AP, Sharkey MJ (2011) Molecular phylogenetics of Braconidae (Hymenoptera: Ichneumonoidea), based on multiple nuclear genes, and implications for classification. Systematic Entomology 36: 549–572. https://doi.org/10.1111/j.1365-3113.2011.00580.x
- Sharanowski BJ, Ridenbaugh RD, Piekarski PK, Broad GR, Burke GR, Deans AR, Lemmon AR, Moriarty Lemmon EC, Diehl GJ, Whitfiel JB, Hines HM (2021) Phylogenomics of Ichneumonoidea (Hymenoptera) and implications for evolution of mode of parasitism and viral endogenization. Molecular Phylogenetics and Evolution 156: 107023. https://doi.org/10.1016/j.ympev.2020.107023
- Sharkey MJ (1993) Family Braconidae. In: Goulet H, Huber JT (Eds) Hymenoptera of the World: An Identification Guide to Families. Research Branch Agriculture Canada Publication, Ottawa, 362–395.
- Sharkey MJ, Wharton RA (1997) Morphology and Terminology. In: Wharton RA, Marsh PM, Sharkey MJ (Eds) Manual of the New World Genera of the Family Braconidae (Hymenoptera). Special Publication of The International Society of Hymenopterists,Washington, D.C., 19–37.
- Shaw SR (1997) Subfamily Cheloninae. In: Wharton RA, Marsh PM, Sharkey MJ (Eds) Manual of the New World Genera of the Family Braconidae (Hymenoptera). Special Publication of The International Society of Hymenopterists, Washington, D.C., 193–201.
- Tagliacollo VA, Lanfear R (2018) Estimating improved partitioning schemes for ultraconserved elements. Molecular Biology and Evolution 35: 1798–1811. https://doi.org/10.1093/molbev/msy069
- Telenga NA (1955) Fauna of the U.S.S.R. Hymenoptera. Braconidae: Microgastrinae and Agathidinae. Izvestiya Rossiiskoi Akademii Nauk. Seruya Geofraficheskaya 5: 4. [In Russian]
- Tobias VI (1967) A review of the classification, phylogeny and evolution of the family Braconidae (Hym.). Entomological Review 46: 387–399.
- Tobias VI (1986) Keys to the insects of the European part of the USSR. III. Hymenoptera. Akademia Nauk Leningrad 4: 1–501. [In Russian]
- van Achterberg C (1979) A revision of the species of Amicrocentrinae, a new subfamily (Hymenoptera, Braconidae), with a description of the final larval instar of Amicrocentrum curvinervis by J.R.T. Short. Tijdschrift voor Entomologie 122: 1–28.
- van Achterberg C (1984) Essay on the phylogeny of Braconidae (Hymenoptera: Ichneumonoidea). Entomologisk Tidskrift 105: 41–58.
- Wharton RA (1993) Bionomics of the Braconidae. Annual Review of Entomology 38: 121–143. https://doi.org/10.1146/annurev.en.38.010193.001005
- Wharton RA, Shaw SR, Sharkey MJ, Wahl DB, Woolley JB, Whitfield JB, Marsh PM, Johnson W (1992) Phylogeny of the subfamilies of the family Braconidae (Hymenoptera: Ichneumonoidea): a reassessment. Cladistics 8: 199–235. https://doi.org/10.1111/j.1096-0031.1992.tb00068.x
- Whitfield JB (1997a) Molecular and morphological data suggest a common origin for the polydnaviruses among braconid wasps. Naturwissenschaften 34: 502–507. https://doi.org/10.1007/s001140050434
- Whitfield JB (1997b) Subfamily Dirrhopinae. In: Wharton RA, Marsh PM, Sharkey MJ (Eds) Manual of the New World Genera of the Family Braconidae (Hymenoptera). Special Publication of The International Society of Hymenopterists, Washington, D.C., 203–204.
- Whitfield JB, Wagner DL (1991) Annotated key to the genera of Braconidae (Hymenoptera) attacking leaf-mining Lepidoptera in the Holarctic Region. Journal of Natural History 25: 733–754. https://doi.org/10.1080/00222939100770481
- Whitfield JB, Mason WRM (1994) Mendesellinae, a new subfamily of braconid wasps (Hymenoptera: Braconidae) with a review of relationships within the microgastroid assemblage. Systematic Entomology 19: 61–76. https://doi.org/10.1111/j.1365-3113.1994.tb00579.x
- Yu DS, van Achterberg C, Horstmann K (2016) Taxapad 2016, Ichneumonoidea 2015. Database on flash-drive, Ottawa.
- 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. https://doi.org/10.1016/j.ympev.2005.08.006
- Zaldívar-Riverón A, Martínez JJ, Belokobylskij SA, Pedraza-Lara CS, Shaw SR, Hanson PE, Varela-Hernández F (2014) Systematics and evolution of gall formation in the plant-associated genera of the wasp subfamily Doryctinae (Hymenoptera: Braconidae). Systematic Entomology 39: 633–659. https://doi.org/10.1111/syen.12078