Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Mitogenome architecture supports the non-monophyly of the cosmopolitan parasitoid wasp subfamily Doryctinae (Hymenoptera: Braconidae) recovered by nuclear and mitochondrial phylogenomics

Rubén Castañeda-Osorio https://orcid.org/0000-0003-0507-5477 A B , Sergey A. Belokobylskij https://orcid.org/0000-0002-3646-3459 C , Jovana M. Jasso-Martínez https://orcid.org/0000-0001-6497-7150 A D , Ernesto Samacá-Sáenz https://orcid.org/0000-0001-6922-7703 E , Robert R. Kula F and Alejandro Zaldívar-Riverón https://orcid.org/0000-0001-5837-1929 A *
+ Author Affiliations
- Author Affiliations

A Colección Nacional de Insectos, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, 3er circuito exterior s/n, Ciudad Universitaria, Coyoacán, Ciudad de México, México.

B Posgrado en Ciencias Biológicas, Unidad de Posgrado, Edificio A, 1er Piso, Circuito de Posgrados, Universidad Nacional Autónoma de México, Ciudad de México, México.

C Zoological Institute of the Russian Academy of Sciences, Universitetskaya Naberezhnaya 1, Saint Petersburg, Russian Federation.

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

E Instituto de Investigaciones Biomédicas, Departamento de Biología Celular y Fisiología, Universidad Nacional Autónoma de México, 3er Circuito Exterior s/n, Ciudad Universitaria, Coyoacán, Ciudad de México, México.

F 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, IS24029 https://doi.org/10.1071/IS24029
Submitted: 17 March 2024  Accepted: 23 April 2024  Published: 13 May 2024

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

Abstract

Mitochondrial DNA gene organisation is an important source of phylogenetic information for various metazoan taxa at different evolutionary timescales, though this has not been broadly tested for all insect groups nor within a phylogenetic context. The cosmopolitan subfamily Doryctinae is a highly diverse group of braconid wasps mainly represented by ectoparasitoids of xylophagous beetle larvae. Previous molecular studies based on Sanger and genome-wide (ultraconserved elements, UCE; and mitochondrial genomes) sequence data have recovered a non-monophyletic Doryctinae, though the relationships involved have always been weakly supported. We characterised doryctine mitogenomes and conducted separate phylogenetic analyses based on mitogenome and UCE sequence data of ~100 representative doryctine genera to assess the monophyly and higher-level classification of the subfamily. We identified rearrangements of mitochondrial transfer RNAs (tRNAs) that support a non-monophyletic Doryctinae consisting of two separate non-related clades with strong geographic structure (‘New World’ and ‘Old World’ clades). This geographic structure was also consistently supported by the phylogenetic analyses preformed with mitogenome and UCE sequence data. These results highlight the utility of the mitogenome gene rearrangements as a potential source of phylogenetic information at different evolutionary timescales.

Keywords: Hymenoptera, mitochondrial DNA, mitochondrial genome, molecular phylogenetics, molecular systematics, morphology, nuclear DNA, phylogeny.

References

Belokobylskij SA (1993) On the classification and phylogeny of the braconid wasps of subfamilies Doryctinae and Exothecinae (Hymenoptera, Braconidae). Part I. On the classification, 1. Entomological Review 72, 109-137 [English translation, original Russian text in Энтомологическое обозрение 71, 900–928 (1992)].
| Google Scholar |

Belokobylskij SA, Zaldívar-Riverón A, Quicke DLJ (2004) Phylogeny of the genera of the parasitic wasps subfamily Doryctinae (Hymenoptera: Braconidae) based on morphological evidence. Zoological Journal of the Linnean Society 142, 369-404.
| Crossref | Google Scholar |

Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: Improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution 69, 313-319.
| Crossref | Google Scholar | PubMed |

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

Braet Y, van Achterberg C (2003) New species of Pambolus Haliday and Phaenocarpa Foerster (Hymenoptera: Braconidae: Pambolinae, Alysiinae) from French Guyana, Suriname and Panama. Zoologische Mededelingen 77, 153-179.
| Google Scholar |

Braet Y, Rousse P, Sharkey MJ (2012) New data on African Cheloninae (Hymenoptera, Braconidae) show a strong biogeographic signal for taxa with spined propodea. Zootaxa 3385, 1-32.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar |

Branstetter MG, Müller A, Griswold TL, Orr MC, Zhu CD (2021) Ultraconserved element phylogenomics and biogeography of the agriculturally important mason bee subgenus Osmia (Osmia). Systematic Entomology 46, 453-472.
| Crossref | Google Scholar |

Bushmanova E, Antipov D, Lapidus A, Prjibelski AD (2019) rnaSPAdes: a de novo transcriptome assembler and its application to RNA-Seq data. GigaScience 8, giz100.
| Crossref | Google Scholar | PubMed |

Cameron SL (2014) Insect mitochondrial genomics: implications for evolution and phylogeny. Annual Review of Entomology 59, 95-117.
| Crossref | Google Scholar | PubMed |

Cameron SL, Yoshizawa K, Mizukoshi A, Whiting MF, Johnson KP (2011) Mitochondrial genome deletions and minicircles are common in lice (Insecta: Phthiraptera). BMC Genomics 12, 394.
| Crossref | Google Scholar | PubMed |

Carapelli A, Vannini L, Nardi F, Boore JL, Beani L, Dallai R, Frati F (2006) The mitochondrial genome of the entomophagous endoparasite Xenos vesparum (Insecta: Strepsiptera). Gene 376, 248-259.
| Crossref | Google Scholar | PubMed |

Castañeda-Osorio R, Belokobylskij SA, Braet Y, Zaldívar-Riverón A (2019) Systematics and evolution of the parasitoid wasp genera of the tribe Holcobraconini (Hymenoptera: Braconidae: Doryctinae). Organisms Diversity and Evolution 19, 409-422.
| Crossref | 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 X, Belokobylskij SA, Van Achterberg C, Whitfield JB (2004) Cornutorogas, a new genus with four new species of the subfamily Rogadinae (Hymenoptera: Braconidae) from the Oriental region. Journal of Natural History 38, 2211-2223.
| Crossref | Google Scholar |

Chen SC, Wei DD, Shao R, Shi JX, Dou W, Wang JJ (2014) Evolution of multipartite mitochondrial genomes in the booklice of the genus Liposcelis (Psocoptera). BMC Genomics 15, 861.
| Crossref | Google Scholar |

Chen L, Chen PY, Xue XF, Hua HQ, Li YX, Zhang F, Wei SJ (2018) Extensive gene rearrangements in the mitochondrial genomes of two egg parasitoids, Trichogramma japonicum and Trichogramma ostriniae (Hymenoptera: Chalcidoidea: Trichogrammatidae). Scientific Reports 8, 7034.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar | PubMed |

Dowton M (1999) Relationships among the cyclostome braconid (Hymenoptera: Braconidae) subfamilies inferred from a mitochondrial tRNA gene rearrangement. Molecular Phylogenetics and Evolution 11, 283-287.
| Crossref | Google Scholar | PubMed |

Dowton M, Austin AD (1999) Evolutionary dynamics of a mitochondrial rearrangement “hotspot” in the Hymenoptera. Molecular Biology and Evolution 16, 298-309.
| Crossref | Google Scholar | PubMed |

Dowton M, Castro LR, Austin AD (2002a) Mitochondrial gene rearrangements as phylogenetic characters in the invertebrates: the examination of genome ‘morphology’. Invertebrate Systematics 16, 345-356.
| Crossref | Google Scholar |

Dowton M, Belshaw R, Austin AD, Quicke DLJ (2002b) 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.
| Crossref | Google Scholar |

Dowton M, Cameron SL, Austin AD, Whiting MF (2009) Phylogenetic approaches for the analysis of mitochondrial genome sequence data in the Hymenoptera – a lineage with both rapidly and slowly evolving mitochondrial genomes. Molecular Phylogenetics and Evolution 52, 512-519.
| Crossref | Google Scholar | PubMed |

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

Faircloth BC, McCormack JE, Crawford NG, Harvey MG, Brumfield RT, Glenn TC (2012) Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales. Systematic Biology 61, 717-726.
| Crossref | Google Scholar | PubMed |

Faircloth BC, Branstetter MG, White ND, Brady SG (2015) Target enrichment of ultraconserved elements from arthropods provides a genomic perspective on relationships among Hymenoptera. Molecular Ecology Resources 15, 489-501.
| Crossref | Google Scholar | PubMed |

Fischer M (1981) Versuch einer systematischen gliederung der Doryctinae, insbesondere der Doryctini, und redeskription nach material aus den Naturwissenschaftlichen Museum in Budapest (Hymenoptera, Braconidae). Polskie Pismo Entomologiczne 51, 41-99.
| 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.
| Crossref | Google Scholar | PubMed |

Haran J, Timmermans MJTN, Vogler AP (2013) Mitogenome sequences stabilize the phylogenetics of weevils (Curculionoidea) and establish the monophyly of larval ectophagy. Molecular Phylogenetics and Evolution 67, 156-166.
| Crossref | Google Scholar | PubMed |

Harris RS (2007) Improved pairwise alignment of genomic DNA. PhD thesis, The Pennsylvania State University, State College, PA, USA.

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, 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.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar |

Jin JJ, Yu WB, Yang JB, Song Y, dePamphilis CW, Yi TS, Li DZ (2020) GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biology 21, 241.
| Crossref | Google Scholar |

Jones OR, Purvis A, Baumgart E, Quicke DLJ (2009) Using taxonomic revision data to estimate the geographic and taxonomic distribution of undescribed species richness in the Braconidae (Hymenoptera: Ichneumonoidea). Insect Conservation and Diversity 2, 204-212.
| Crossref | Google Scholar |

Kalyaanamoorthy S, Minh BQ, Wong TK, 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, 772-780.
| Crossref | Google Scholar | PubMed |

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649.
| Crossref | Google Scholar | PubMed |

Kocher A, Kamilari M, Lhuillier E, Coissac E, Péneau J, Chave J, Murienne J (2014) Shotgun assembly of the assassin bug Brontostoma colossus mitochondrial genome (Heteroptera, Reduviidae). Gene 552, 184-194.
| Crossref | Google Scholar | PubMed |

Li Q, Wei SJ, Tang P, Wu Q, Shi M, Sharkey MJ, Chen XX (2016) Multiple lines of evidence from mitochondrial genomes resolve phylogenetic relationships of parasitic wasps in Braconidae. Genome Biology and Evolution 8, 2651-2662.
| Crossref | Google Scholar | PubMed |

Mao M, Gibson T, Dowton M (2015) Higher-level phylogeny of the Hymenoptera inferred from mitochondrial genomes. Molecular Phylogenetics and Evolution 84, 34-43.
| Crossref | Google Scholar | PubMed |

Marsh PM (1965) The Nearctic Doryctinae. I. A review of the subfamily with a taxonomic revision of the tribe Hecabolini (Hymenoptera: Braconidae). Annals of the Entomological Society of America 58, 668-699.
| Crossref | Google Scholar |

Marsh PM (1997) Subfamily Doryctinae. In ‘Manual of the New World Genera of the Family Braconidae (Hymenoptera)’. (Eds RA Wharton, PM Marsh, MJ Sharkey) pp. 206–233. (International Society of Hymenopterists: Washington, DC, USA)

Marsh PM (2002) The Doryctinae of Costa Rica (excluding the genus Heterospilus). Memoirs of the American Entomological Institute 70, 1-216.
| Google Scholar |

Martínez JJ, Zaldívar-Riverón A (2013) Seven new species of Allorhogas (Hymenoptera: Braconidae: Doryctinae) from Mexico. Revista Mexicana de Biodiversidad 84, 117-139.
| Crossref | Google Scholar |

Meza-Lázaro RN, Poteaux C, Bayona-Vásquez NJ, Branstetter MG, Zaldívar-Riverón A (2018) Extensive mitochondrial heteroplasmy in the neotropical ants of the Ectatomma ruidum complex (Formicidae: Ectatomminae). Mitochondrial DNA – A. DNA Mapping, Sequencing, and Analysis 29, 1203-1214.
| Crossref | Google Scholar | PubMed |

Morales-Silva T, Modesto-Zampieron SL (2017) Occurrence of Allorhogas sp. (Hymenoptera: Braconidae: Doryctinae) associated with galls on seeds of Inga vera (Fabaceae) in Brazil. Brazilian Journal of Biology 78, 178-179.
| Crossref | Google Scholar | PubMed |

Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268-274.
| Crossref | Google Scholar | PubMed |

Nunes JF, Zaldívar-Riverón A, de Castro CS, Marsh PM, Penteado-Dias AM, Briceño R, Martínez JJ (2012) Doryctopambolus Nunes & Zaldívar-Riverón (Braconidae), a new neotropical doryctine wasp genus with propodeal spines. ZooKeys 223, 53-67.
| Crossref | Google Scholar | PubMed |

Park JS, Kim MJ, Jeong SY, Kim SS, Kim I (2016) Complete mitochondrial genomes of two gelechioids, Mesophleps albilinella and Dichomeris ustalella (Lepidoptera: Gelechiidae), with a description of gene rearrangement in Lepidoptera. Current Genetics 62, 809-826.
| Crossref | Google Scholar | PubMed |

Quicke DLJ (2015) Chapter 12. Phylogeny and systematics of the Braconidae. In ‘The Braconid and Ichneumonid Parasitoid Wasps: Biology, Systematics, Evolution and Ecology’. (Ed. DLJ Quicke) pp. 201–340. (Wiley–Blackwell)

Quicke DLJ, Tunstead J, Falco JV, Marsh PM (1992a) Venom gland and reservoir morphology in the Doryctinae and related braconid wasps (Insecta, Hymenoptera, Braconidae). Zoologica Scripta 21, 403-416.
| Crossref | Google Scholar |

Quicke DLJ, Ficken LC, Fitton MG (1992b) New diagnostic ovipositor characters for doryctine wasps (Hymenoptera, Braconidae). Journal of Natural History 26, 1035-1046.
| Crossref | Google Scholar |

Rahman H, Fitton MG, Quicke DLJ (1998a) Ovipositor internal microsculpture in the Braconidae (Insecta, Hymenoptera). Zoologica Scripta 27, 319-331.
| Crossref | Google Scholar |

Rahman H, Fitton MG, Quicke DLJ (1998b) Ovipositor internal microsculpture and other features in doryctine wasps (Insecta, Hymenoptera, Braconidae). Zoologica Scripta 27, 333-343.
| Crossref | Google Scholar |

Raposo do Amaral F, Neves LG, Resende Jr MF, Mobili F, Miyaki CY, Pellegrino KCM, Biondo C (2015) Ultraconserved elements sequencing as a low-cost source of complete mitochondrial genomes and microsatellite markers in non-model amniotes. PLoS One 10, e0138446.
| Crossref | Google Scholar | PubMed |

Sáenz-Manchola OF, Virrueta-Herrera S, D’Alessio LM, Yoshizawa K, García Aldrete AN, Johnson KP (2021) Mitochondrial genomes within bark lice (Insecta: Psocodea: Psocomorpha) reveal novel gene rearrangements containing phylogenetic signal. Systematic Entomology 46, 938-951.
| Crossref | Google Scholar |

Samacá-Sáenz E, Meza-Lázaro RN, Branstetter MG, Zaldívar-Riverón A (2019) Phylogenomics and mitochondrial genome evolution of the gall-associated doryctine wasp genera (Hymenoptera: Braconidae). Systematics and Biodiversity 17, 731-744.
| Crossref | Google Scholar |

Samacá-Sáenz E, Santos BF, Martínez JJ, Egan SP, Shaw SR, Hanson PE, Zaldívar-Riverón A (2022) Ultraconserved elements-based systematics reveals evolutionary patterns of host-plant family shifts and phytophagy within the predominantly parasitoid braconid wasp subfamily Doryctinae. Molecular Phylogenetics and Evolution 166, 107319.
| Crossref | Google Scholar | PubMed |

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 |

Simon S, Hadrys H (2013) A comparative analysis of complete mitochondrial genomes among Hexapoda. Molecular Phylogenetics and Evolution 69, 393-403.
| Crossref | Google Scholar | PubMed |

Singh TR (2008) Mitochondrial gene rearrangements: new paradigm in the evolutionary biology and systematics. Bioinformation 3, 95-97.
| Crossref | Google Scholar | PubMed |

Song SN, Tang P, Wei SJ, Chen XX (2016) Comparative and phylogenetic analysis of the mitochondrial genomes in basal hymenopterans. Scientific Reports 6, 20972.
| Crossref | Google Scholar | PubMed |

Ströher PR, Zarza E, Tsai WLE, McCormack JE, Feitosa RM, Pie MR (2017) The mitochondrial genome of Octostruma stenognatha and its phylogenetic implications. Insectes Sociaux 64, 149-154.
| Crossref | 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 |

Tang P, Zhu JC, Zheng BY, Wei SJ, Sharkey M, Chen XX, Vogler AP (2019) Mitochondrial phylogenomics of the Hymenoptera. Molecular Phylogenetics and Evolution 131, 8-18.
| Crossref | Google Scholar | PubMed |

Thao ML, Baumann L, Baumann P (2004) Organization of the mitochondrial genomes of whiteflies, aphids and pysillids (Hemiptera: Sternorrhyncha). BMC Evolutionary Biology 4, 25.
| Crossref | Google Scholar | PubMed |

Timmermans MJTN, Vogler AP (2012) Phylogenetically informative rearrangements in mitochondrial genomes of Coleoptera, and monophyly of aquatic elateriform beetles (Dryopoidea). Molecular Phylogenetics and Evolution 63, 299-304.
| Crossref | Google Scholar | PubMed |

Wei SJ, Shi M, Sharkey MJ, van Achterberg C, Chen XX (2010) Comparative mitogenomics of Braconidae (Insecta: Hymenoptera) and the phylogenetic utility of mitochondrial genomes with special reference to Holometabolous insects. BMC Genomics 11, 371.
| Crossref | Google Scholar | PubMed |

Wei SJ, Li Q, van Achterberg K, Chen XX (2014) Two mitochondrial genomes from the families Bethylidae and Mutillidae: independent rearrangement of protein-coding genes and higher-level phylogeny of the Hymenoptera. Molecular Phylogenetics and Evolution 77, 1-10.
| Crossref | Google Scholar | PubMed |

Yan D, Tang Y, Xue X, Wang M, Liu F, Fan J (2012) The complete mitochondrial genome of the western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae) contains triplicate putative control regions. Gene 506, 117-124.
| Crossref | Google Scholar | PubMed |

Yang J, Ye F, Huang Y (2016) Mitochondrial genomes of four katydids (Orthoptera: Phaneropteridae): New gene rearrangements and their phylogenetic implications. Gene 575, 702-711.
| Crossref | Google Scholar | PubMed |

Young AD, Gillung JP (2020) Phylogenomics – principles, opportunities and pitfalls of big‐data phylogenetics. Systematic Entomology 45, 225-247.
| Crossref | Google Scholar |

Zaldívar-Riverón A, Areekul B, Shaw MR, Quicke DLJ (2004) Comparative morphology of the venom apparatus in the braconid wasp subfamily Rogadinae (Insecta, Hymenoptera, Braconidae) and related taxa. Zoologica Scripta 33, 223-237.
| Crossref | Google Scholar | PubMed |

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 |

Zaldívar-Riverón A, Belokobylskij SA, León-Regagnon V, Martínez JJ, Briceño R, Quicke DLJ (2007) A single origin of gall association in a group of parasitic wasps with disparate morphologies. Molecular Phylogenetics and Evolution 44, 981-992.
| Crossref | Google Scholar | PubMed |

Zaldívar-Riverón A, Belokobylskij SA, León-Regagnon V, Briceño R, Quicke DLJ (2008) Molecular phylogeny and historical biogeography of the parasitic wasp subfamily Doryctinae (Hymenoptera: Braconidae). Invertebrate Systematics 22, 345-363.
| Crossref | Google Scholar |

Zaldívar-Riverón A, Martínez JJ, Belokobylskij SA, Pedraza-Lara C, 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.
| Crossref | Google Scholar |

Zaldívar-Riverón A, Martínez JJ, Hanson PE, Mayorga-Martínez C, Salinas-Ramos VB, Faria LDB (2018) New gall-associated species of Allorhogas (Hymenoptera: Braconidae), including a natural enemy of the weed Miconia calvescens (Melastomataceae). The Canadian Entomologist 150, 279-302.
| Crossref | Google Scholar |

Zhang YM, Williams JL, Lucky A (2019) Understanding UCEs: a comprehensive primer on using ultraconserved elements for arthropod phylogenomics. Insect Systematics and Diversity 3, 1-12.
| Crossref | Google Scholar |

Zhao J, Li H, Winterton SL, Liu Z (2013) Ancestral gene organization in the mitochondrial genome of Thyridosmylus langii (McLachlan, 1870) (Neuroptera: Osmylidae) and implications for lacewing evolution. PLoS One 8, e62943.
| Crossref | Google Scholar |