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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Molecular phylogeny and historical biogeography of the cosmopolitan parasitic wasp subfamily Doryctinae (Hymenoptera : Braconidae)

Alejandro Zaldivar-Riverón A G , Sergey A. Belokobylskij B C , Virginia León-Regagnon A , Rosa Briceño-G. D and Donald L. J. Quicke E F
+ Author Affiliations
- Author Affiliations

A Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, 3er. Circuito Exterior, Ciudad Universitaria, Ap. Postal 70-153, C. P. 04510, México D. F., México.

B Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg 199034, Russia.

C Museum and Institute of Zoology, PAN, Wilcza 64, Warsaw 00-679, Poland.

D Universidad Centroccidental ‘Lisandro Alvarado’, Decanato de Agronomía, Depto. de Ciencias Biológicas, Sección Entomología, Cabudare, Estado Lara, Venezuela.

E Division of Biology and Centre for Population Biology, Imperial College London, Silwood Park Campus, Ascot, Berkshire, SL5 7PY, UK.

F Department of Entomology, Natural History Museum, London, SW7 5BD, UK.

G Corresponding author. Email: azaldivar@mncn.csic.es

Invertebrate Systematics 22(3) 345-363 https://doi.org/10.1071/IS07028
Submitted: 25 June 2007  Accepted: 7 March 2008   Published: 18 June 2008

Abstract

The phylogenetic relationships among representatives of 64 genera of the cosmopolitan parasitic wasps of the subfamily Doryctinae were investigated based on nuclear 28S ribosomal (r) DNA (~650 bp of the D2–3 region) and cytochrome c oxidase I (COI) mitochondrial (mt) DNA (603 bp) sequence data. The molecular dating of selected clades and the biogeography of the subfamily were also inferred. The partitioned Bayesian analyses did not recover a monophyletic Doryctinae, though the relationships involved were only weakly supported. Strong evidence was found for rejecting the monophylies of both Doryctes Haliday, 1836 and Spathius Nees, 1818. Our results also support the recognition of the Rhaconotini as a valid tribe. A dispersal–vicariance analysis showed a strong geographical signal for the taxa included, with molecular dating estimates for the origin of Doryctinae and its subsequent radiation both occurring during the late Paleocene–early Eocene. The divergence time estimates suggest that diversification in the subfamily could have in part occurred as a result of continental break-up events that took place in the southern hemisphere, though more recent dispersal events account for the current distribution of several widespread taxa.


Acknowledgements

We thank the following people for donating material and/or helping: A. Austin, Y. Braet, J. Clavijo, M. Shaw, S. Shaw, and C. van Achterberg; H. Clebsh, and P. L. Baccei for support in the field; M. Brandley and T. Reeder for helping with the Bayesian approach for hypothesis testing; A. Wong for installing the UNIX version of MrBayes. This work was supported by a postdoctoral fellowship given by the Universidad Nacional Autónoma de México (UNAM-DGAPA) to AZR, a Natural Environment Research Council grant to DLJQ (NE/C519538), grants given by the Russian Foundation for Basic Research (No. 07-04-00454), the European Commission’s Research Infrastructure Action via the SYNTHESYS project at the MNCN, and the Presidium RAS Program ‘Origin and evolution of Biosphere, Subprogram II’ to SAB, and by two grants given by FONACIT-Venezuela (S1-2000000479, LAB-2000001593) to RB.


References


Ashmead H. W. (1900) Classification of the ichneumon flies, or the superfamily Ichneumonoidea. Proceedings of the United States Natural Museum 23, 1–220. open url image1

Barbalho S., Penteado-Dias A., Marsh P. M. (1999) Descriptions of new genera from Brazil in the tribes Heterospilini and Spathiini with similar wing venation (Hymenoptera: Braconidae). Journal of Hymenoptera Research 8, 139–153. open url image1

Basibuyuk H. H., Rasnitsyn A. P., van Achterberg C., Fitton M. G., Quicke D. L. J. (1999) A new putatively primitive Cretaceous fossil braconid subfamily from New Jersey amber (Hymenoptera: Braconidae). Zoologica Scripta 28, 211–214.
Crossref | GoogleScholarGoogle Scholar | open url image1

Beiko R. G., Keith J. M., Harlow T. J., Ragan M. A. (2006) Searching for convergence in phylogenetic Markov Chain Monte Carlo. Systematic Biology 55, 553–565.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Belokobylskij S. A. (1992) On the classification and phylogeny of the Braconid wasps subfamilies Doryctinae and Exothecinae (Hymenoptera, Braconidae). Part I. On the classification, 1. Entomologicheskoe Obozrenie 71, 900–928. (In Russian). English translation Entomological Review 72, 109–137. open url image1

Belokobylskij S. A. (1993a) On the classification and phylogeny of the braconid wasps subfamilies Doryctinae and Exothecinae (Hymenoptera: Braconidae). II. Phylogeny. Entomologicheskoe Obozreine 72, 891–914. (In Russian). English translation Entomological Review 73, 1–27. open url image1

Belokobylskij S. A. (1993b) East Asiatic species of the genus Neurocrassus (Hymenoptera: Braconidae). Zoosystematica Rossica 2, 161–172. open url image1

Belokobylskij S. A. (1994) A new tribe of the subfamily Doryctinae from Papua New Guinea (Hymenoptera: Braconidae). Zoosystematica Rossica 3, 141–145. open url image1

Belokobylskij S. A. (1995a) Two new genera and two new subgenera of the subfamilies Exothecinae and Doryctinae from the Old World (Hymenoptera: Braconidae). Zoologische Mededelingen Leiden 69, 37–52. open url image1

Belokobylskij S. A. (1995b) Main evolutionary transformations of the morphological structures in the subfamilies Doryctinae and Exothecinae (Hymenoptera, Braconidae). Entomologicheskoe Obozreine [in Russian] 74, 153–176. open url image1

Belokobylskij S. A. (2002) Two new Oriental genera of Doryctinae (Hymenoptera, Braconidae) from termite nests. Journal of Natural History 36, 953–962.
Crossref | GoogleScholarGoogle Scholar | open url image1

Belokobylskij S. A. (2004a) New genus and new subgenus of subfamily Doryctinae (Hymenoptera: Braconidae) from the Old World fauna. Annales de la Société Entomologique de France 40, 199–204. open url image1

Belokobylskij S. A. (2004b) Two new taxa of subtribe Rhaconotina (Hymenoptera, Braconidae, Doryctinae, Doryctini), from Africa, with a key to subtribe genera. Annales de la Société Entomologique de France 40, 205–210. open url image1

Belokobylskij S. A. (2006) Neoheterospilus gen. n., a new genus of the tribe Heterospilini (Hymenoptera: Braconidae: Doryctinae) with highly modified ovipositor and a worldwide distribution. Insect Systematics & Evolution 37, 149–178. open url image1

Belokobylskij S. A., Chen X. (2004) The species of the genus Rhaconotus Ruthe, 1854 (Hymenoptera: Braconidae: Doryctinae) from China with a key to species. Annales Zoologici 54, 319–359. open url image1

Belokobylskij S. A., Chen X. (2006) Hecabolomorpha n. gen., a new Asian genus from the tribe Hecabolini (Hymenoptera: Braconidae: Doryctinae). Annales de la Société Entomologique de France 42, 107–111. open url image1

Belokobylskij S. A., Iqbal M., Austin A. (2004a) Systematics, distribution and diversity of the Australian Doryctinae wasps (Hymenoptera, Braconidae, Doryctinae). Records of the South Australian Museum, Monographs series 8, 1–150. open url image1

Belokobylskij S. A., Zaldivar-Riverón A., Quicke D. L. J. (2004b) 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 | GoogleScholarGoogle Scholar | open url image1

Belshaw R., Quicke D. L. J. (1997) A molecular phylogeny of the Aphidiinae (Hymenoptera: Braconidae). Molecular Phylogenetics and Evolution 7, 281–293.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Belshaw R., Fitton M., Herniou E., Gimeno C., Quicke D. L. J. (1998) A phylogenetic reconstruction of the Ichneumonoidea (Hymenoptera) based on the D2 variable region of 28S ribosomal RNA. Systematic Entomology 23, 109–123.
Crossref | GoogleScholarGoogle Scholar | open url image1

Belshaw R., Dowton M., Quicke D. L. J., Austin A. D. (2000) Estimating ancestral geographic distributions: a Gondwanan origin for aphid parasitoids. Proceedings of the Royal Society of London. Series B. Biological Sciences 267, 491–496.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bossuyt F., Brown R. M., Hillis D. M., Cannatella D. C., Milinkovitch M. C. (2006) Phylogeny and biogeography of a cosmopolitan frog radiation: late Cretaceous diversification resulted in continent-scale endemism in the family Ranidae. Systematic Biology 55, 579–594.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brandley M. C., Schmitz A., Reeder T. W. (2005) Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Systematic Biology 54, 373–390.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Buckley T. R., Arensburger P., Simon C., Chambers G. K. (2002) Combined data, Bayesian phylogenetics, and the origin of the New Zealand cicada genera. Systematic Biology 51, 4–18.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Carpenter F. M. (1992). Part R. Arthropoda 4. Volume 4: superclass Exapoda. In ‘Treatise on Invertebrate Paleontology’. (Ed. R. L. Kaesler.) (The Geological Society of America, The University of Kansas: Boulder, CO, USA.)

Cushman R. A. (1923) A new subfamily of the Braconidae (Hymenoptera) from termite nests. Proceedings of the Entomological Society of Washington 25, 54–55. open url image1

Dietrich C. H., Rakitov R. A., Holmes J. L., Black W. C. (2001) Phylogeny of the major lineages of Membracoidea (Insecta: Hemiptera: Cicadomorpha). Molecular Phylogenetics and Evolution 18, 293–305.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dowton M., Belshaw R., Austin A. D., Quicke D. L. J. (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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Enderlein G. (1912) Zur Kenntnis der Spathiinen und einiger verwandter Gruppen. Archiv für Naturgeschicthe 78, 1–37. open url image1

Felsenstein J. (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution 17, 368–376.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fischer M. (1981) Versuch ainer systematischen Gliederung der Doryctinae, insbesondere der Doryctini, und Redeskiption nach Material aus den Naturwissenschaftlichen Museum in Budapest (Hymenoptera: Braconidae). Polskie Pismo Entomologiczne 51, 41–99. open url image1

Foerster A. (1862) Synopsis der Familien und Gattungen der Branconen. Verhandlungen des Naturhistorischen Vereins der Preussischen Rheinlande und Westfalens 19, 225–288. open url image1

Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
PubMed |
open url image1

Gillespie J. J. (2004) Characterizing regions of ambiguous alignment caused by the expansion and contraction of hairpin-stem loops in ribosomal RNA molecules. Molecular Phylogenetics and Evolution 33, 936–943.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gillespie J. J., Yoder M. J., Wharton R. A. (2005) Predicted secondary structure for 28S and 18S rRNA from Ichneumonoidea (Insecta: Hymenoptera: Apocrita): impact on sequence alignment and phylogeny estimation. Journal of Molecular Evolution 61, 114–137.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gomes S. A. G., Penteado-Dias A. M. (2007) Description of a new genus of Doryctinae wasps (Hymenoptera: Braconidae) from Brazil. Zoologische Mededeelingen 81, 115–119. open url image1

Huelsenbeck J. P., Ronquist F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Iturralde-Vinent M. A., MacPhee R. D. E. (1996) Age and paleogeographical origin of Dominican amber. Science 273, 1850–1852.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jost M. C., Shaw K. L. (2006) Phylogeny of Ensifera (Hexapoda: Orthoptera) using three ribosomal loci, with implications for the evolution of acoustic communication. Molecular Phylogenetics and Evolution 38, 510–530.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Labandeira C. C., Johnson K. R., Wilf P. (2002) Impact of the terminal Cretaceous event on plant–insect associations. Proceedings of the National Academy of Sciencies 99, 2061–2066.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lanave C. G., Preparata C., Saccone C., Serio G. (1984) A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution 20, 86–93.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lewis P. O. (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50, 913–925.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Maddison D. R., and Maddison W. P. (2000). ‘MacClade 4: Analysis of Phylogeny and Character Evolution.’ (Sinauer Associates: Sunderland, MA, USA.)

Mancini D., Priore R., Battaglia D., van Achterberg C. (2003) Caenopachys hartigii (Ratzeburg) confirmed for Italy, with notes on the status of the genus Caenopachys Foerster. Zoologische Mededelingen Leiden 77, 459–470. open url image1

Mardulyn P., Whitfield J. B. (1999) Phylogenetic signal in the COI, 16S, and 28S genes for inferring relationships among genera of Microgastrinae (Hymenoptera; Braconidae): evidence of a high diversification rate in this group of parasitoids. Molecular Phylogenetics and Evolution 12, 282–294.
Crossref | PubMed |
open url image1

Marsh P. M. (1976) The Nearctic Doryctinae, X. The genus Rhaconotus Ruthe (Hymenoptera: Braconidae). Proceedings of the Royal Entomological Society 78, 379–403. open url image1

Marsh P. M. (1997). Doryctinae. In ‘Manual of the New World genera of the family Braconidae (Hymenoptera)’. (Eds R. A. Wharton, P. M. Marsh and M. J. Sharkey.) Special Publication 1, pp. 207–233. (International Society of Hymenopterists.)

Marsh P. M. (2002) The Doryctinae of Costa Rica (excluding the genus Heterospilus). Memoirs of the American Entomological Institute 70, 1–319. open url image1

Marshall T. A. (1885) A monograph of British Braconidae Part I. Transactions of the Royal Entomological Society of London 1885, 1–280. open url image1

Muesebeck C. F. W. (1960) A fossil braconid wasp of the genus Ecphylus (Hymenoptera). Journal of Paleontology 34, 495–496. open url image1

Nixon G. E. J. (1943) A revision of the Spathiinae of the Old World (Hymenoptera: Braconidae). Transactions of the Royal Entomological Society of London 93, 173–456. open url image1

Nylander J. A. A. (2004). ‘MrModeltest v.1.0b.’ Available online at http://www.ebc.uu.se/systzoo/staff/nylander.html [Verified April 2008].

Nylander J. A. A., Ronquist F., Huelsenbeck J. P., Nieves-Aldrey J. L. (2004) Bayesian analysis of combined data. Systematic Biology 53, 47–67.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pollock D. D., Zwickl D. J., McGuire J. A., Hillis D. M. (2002) Increased taxon sampling is advantageous for phylogenetic inference. Systematic Biology 51, 664–671.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Quicke D. L. J. (1996) First record of Leptorhaconotus Granger (Hymenoptera: Braconidae) from South Africa, with the description of a remarkable new species and a discussion of the subfamilial placement of the genus. African Entomology 4, 111–116. open url image1

Quicke D. L. J., Marsh P. M. (1992) Two new Neotropical species of braconid wasps (Hymenoptera: Braconidae: Braconinae and Doryctinae) with remarkable ovipositors. Proceedings of the Entomological Society of Washington 94, 559–567. open url image1

Quicke D. L. J., van Achterberg C. (1990) Phylogeny of the subfamilies of the family Braconidae. (Hymenoptera: Ichneumonoidea). Zoologische Verhandelingen 258, 1–95. open url image1

Quicke D. L. J., Ficken L., Fitton M. G. (1992a) New diagnostic ovipositor characters for doryctine wasps (Hymenoptera, Braconidae). Journal of Natural History 26, 1035–1046.
Crossref | GoogleScholarGoogle Scholar | open url image1

Quicke D. L. J., Tunstead J., Falco J. V., Marsh P. M. (1992b) Venom gland and reservoir morphology in the Doryctinae and related braconid wasps (Insecta, Hymenoptera, Braconidae). Zoologica Scripta 21, 403–416.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reeder T. W. (2003) A phylogeny of the Australian Sphenomorphus group (Scincidae: Squamata) and the phylogenetic placement of the crocodile skinks (Tribolonotus): Bayesian approaches to assessing congruence and obtaining confidence in maximum likelihood inferred relationships. Molecular Phylogenetics and Evolution 27, 384–397.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ronquist F. (1997) Dispersal–vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology 46, 195–23.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ronquist F., Huelsenbeck J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sagegami-Oba R., Oba Y., Ôhira H. (2007) Phylogenetic relationships of click beetles (Coleoptera: Elateridae) inferred from 28S ribosomal DNA: insight into the evolution of bioluminescence in Elateridae. Molecular Phylogenetics and Evolution 42, 410–421.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sanderson M. J. (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution 19, 101–109.
PubMed |
open url image1

Sanderson M. J. (2004). ‘r8s, version 1.70. User’s Manual.’ Available online at http://loco.biosci.arizona.edu/r8s [Verified May 2008].

Sanmartín I., Ronquist F. (2004) Southern hemisphere biogeography inferred by event-based models: plant versus animal patterns. Systematic Biology 53, 216–243.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sanmartín I., Enghoff H., Ronquist F. (2001) Patterns of animal dispersal, vicariance and diversification in the Holarctic. Biological Journal of the Linnean Society 73, 345–390. open url image1

Saux C., Fisher B. L., Spicer G. S. (2004) Dracula ant phylogeny as inferred by nuclear 28S rDNA sequences and implications for ant systematics (Hymenoptera: Formicidae: Amblyoponinae). Molecular Phylogenetics and Evolution 33, 457–468.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schmitz J., Moritz F. A. (1998) Molecular phylogeny of Vespidae (Hymenoptera) and the evolution of sociality in wasps. Molecular Phylogenetics and Evolution 9, 183–191.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Seltmann K., Sharkey M. (2007) A new genus and species of apterous Doryctinae (Hymenoptera: Braconidae) from Costa Rica. Zootaxa 1415, 17–24. open url image1

Shaw S. R., Edgerly J. S. (1985) A new braconid genus (Hymenoptera) parasitising webspinners (Embiidina) in Trinidad. Psyche 92, 505–511.
Crossref |
open url image1

Shenefelt R. D., and Marsh P. M. (1976). Pars 13. Braconidae 9, Doryctinae. In ‘Hymenopterum catalogus (nova edito)’. (Eds J. van der Vecht and R. D. Shenefelt.) pp. 1263–1424. (Dr. W. Junk: The Hague, The Netherlands.)

Simon C., Frati F., Beckenbach A., Crespi B., Liu H., Flook P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 86, 651–701. open url image1

Swofford D. L. (2002). ‘PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods), version 4.0b10.’ (Sinauer: Sunderland, MA, USA.)

Tobias V. I. (1968). Problems of classification and phylogeny of the family Braconidae (Hymenoptera). In ‘Chteniya Pamyati N. A. Kholodkovskogo’. (Nauka: Moscow, Russia.) pp. 3–43. [In Russian]

van Achterberg C. (1974) The feature of the petiolar segment in some Braconidae (Hymenoptera). Entomologische Berichten 34, 213–214. open url image1

van Achterberg C. (1976) A preliminar key of the subfamilies of the Braconidae (Hymenoptera). Tijdschrift voor Entomologie 119, 33–78. open url image1

Wahlberg N. (2006) That awkward age for butterflies: insights from the age of the butterfly subfamily Nymphalinae. Systematic Biology 55, 703–714.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wharton R. A. (1993) Review of the Hormiini (Hymenoptera: Braconidae) with a description of new taxa. Journal of Natural History 27, 107–171.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wharton R. A., and Hanson P. E. (2005). Gall wasps in the family Braconidae (Hymenoptera). In ‘Biology, Ecology, and Evolution of Gall-inducing Arthropods’. (Eds A. Raman, W. C. Schaefer and T. M. Withers.) pp. 495–505. (Science Publishers: Enfield, NH, USA.)

Wiens J. J. (1998) Combining data sets with different phylogenetic histories. Systematic Biology 47, 568–581.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wiens J. J., Fetzner J. W., Parkinson C. L., Reeder T. W. (2005) Hylid frog phylogeny and sampling strategies for speciose clades. Systematic Biology 54, 719–748.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wilgenbusch J. C., Warren D. L., and Swofford D. L. (2004). AWTY: A system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. Available online at http://ceb.csit.fsu.edu/awty [Verified April 2008].

Woodburne M. O., Case J. A. (1996) Dispersal, vicariance, and the late Cretaceous to early tertiary land mammal biogeography from South America to Australia. Journal of Mammalian Evolution 3, 121–161.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zaldivar-Riverón A., Mori M., Quicke D. L. J. (2006) Systematics of the cyclostome subfamilies of braconid parasitic wasps (Hymenoptera: Ichenumonoidea): a simultaneous molecular and morphological Bayesian approach. Molecular Phylogenetics and Evolution 38, 130–145.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zaldivar-Riverón A., Belokobylskij S. A., León-Regagnon V., Martínez J. J., Briceño R., Quicke D. L. J. (2007) A single origin of gall association in a group of parasitic wasps with disparate morphologies. Molecular Phylogenetics and Evolution 44, 981–992.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zuparko R. L., Poinar G. O. (1997) Aivalykus dominicanus (Hymenoptera: Braconidae), a new species from Dominican amber. Proceedings of the Entomological Society of Washington 99, 744–747. open url image1

Zwickl D. J., Hillis D. M. (2002) Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology 51, 588–598.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1