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A Single Origin of Gall Association in a Group of Parasitic Wasps with Disparate Morphologies

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A Single Origin of Gall Association in a Group of Parasitic Wasps with Disparate Morphologies Molecular Phylogenetics and Evolution 44 (2007) 981–992 www.elsevier.com/locate/ympev A single origin of gall association in a group of parasitic wasps with disparate morphologies Alejandro Zaldivar-Rivero´n a,*, Sergey A. Belokobylskij b,c, Virginia Leo´n-Regagnon a, Juan Jose´ Martı´nez d, Rosa Bricen˜o e, Donald L.J. Quicke f,g a Departamento de Zoologı´a, Instituto de Biologı´a, Universidad Nacional Auto´noma de Me´xico, 3er. Circuito Exterior, Cd. Universitaria, Ap. Postal 70-153, C. P. 04510, Me´xico D. F., Mexico 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 Divisio´n de Entomologı´a, Museo Argentino de Ciencias Naturales ‘‘Bernardino Rivadavia’’, Av. Angel Gallardo 470, C1405DJR, Buenos Aires, Argentina e Universidad Centroccidental ‘‘Lisandro Alvarado’’, Decanato de Agronomı´a, Depto. de Ciencias Biolo´gicas, Seccio´n de Entomologı´a, Cabudare, Estado Lara, Venezuela f Division of Biology and Centre for Population Biology, Imperial College London, Silwood Park Campus, Ascot, Berkshire, SL5 7PY, UK g Department of Entomology, Natural History Museum, London SW7 5BD, UK Received 17 August 2006; revised 10 May 2007; accepted 17 May 2007 Available online 9 June 2007 Abstract The braconid wasp subfamily Doryctinae mainly comprises idiobiont ectoparasitoids of other insect larvae. In recent years, however, members of a few genera have been discovered to be associated with galls from various unrelated host plant families, with some of these being gall inducers whereas others are suspected as being predators of gallers. Because of their considerable morphological differences, these gall-associated taxa traditionally have been placed in separate tribes or even in other subfamilies. In this study, we investigate the phylogenetic relationships among representatives of a number of different doryctine genera, including five of its seven gall-associated genera using two genetic markers. Here we analyzed the length-variable 28S sequence data based on secondary structure both excising the unalignable regions and recoding them according to indel length. In addition, multiple alignments were carried out with a range of gap-opening and extension parameters. The combined (28S + CO1) phylogenetic hypotheses obtained, both excluding and recoding the unalignable regions, recover a clade comprising the five gall-associated genera, and most of the analyses using multiple alignments also support this relationship. These results support a scenario in which secondary phytophagy evolves from initially attacking primary gall- forming hosts. The relationships recovered are also more congruent with a model that explains the macroevolution of insect plant asso- ciation in the Doryctinae as reflecting geographic proximity rather than host plant relationships. Further, our phylogenetic hypotheses consistently show that one of the main morphological features employed in the higher level classification of the Doryctinae is actually highly homoplastic. Ó 2007 Elsevier Inc. All rights reserved. Keywords: Braconidae; Doryctinae; Cyclostomes; Character evolution, Molecular phylogeny; Secondary structure alignment; Multiple alignment 1. Introduction In the Hymenoptera, gall formation, predation of gall- inducers and inquilinism are related phenomena that occur * in several lineages, principally in the Chalcidoidea and Corresponding author. Address: Museo Nacional de Ciencias Naut- Cynipoidea, but which have also been discovered recently rales, Departamento de Biodiversidad y Biologı´a Evolutiva, C/Jose´ Gutie´rrez Abascal 2, 28006 Madrid, Spain. in a few members of the cyclostome group of the otherwise E-mail address: [email protected] (A. Zaldivar-Rivero´n). almost entirely parasitic family Braconidae (see Wharton 1055-7903/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2007.05.016 982 A. Zaldivar-Rivero´n et al. / Molecular Phylogenetics and Evolution 44 (2007) 981–992 and Hanson, 2005 for a review). Starting from the first shown by the different gall-associated doryctine genera. report of phytophagy in Allorhogas Gahan almost 20 years For this reason, these taxa have been placed in separate ago (Maceˆdo and Monteiro, 1989), cecidogenesis (i.e., gall and in some cases exclusive tribes (e.g., Labanini, Perc- development) in the Braconidae has subsequently been nobraconini) or even in other subfamilies (e.g., Monitoriel- confirmed only in other two cyclostome genera, Monitoriel- la: Wharton, 1993; but see Zaldivar-Rivero´n et al., 2006). It la Hedqvist (Infante et al., 1995) and Mesostoa van Achter- has been argued, however, that the external morphology of berg (Austin and Dangerfield, 1998). Some other braconid doryctine wasps is quite homoplastic (Belokobylskij et al., wasps have only ever been reared from galls, though some 2004b), and thus several features employed to differentiate of these appear to display various forms of gall association its higher taxa could have actually evolved separately in rather than being the primary gall-formers themselves. repeated occasions. Most of these gall-associated species belong to the large Recently, a simultaneous molecular and morphological and cosmopolitan subfamily Doryctinae, though this fea- phylogenetic analysis among representatives of the cyclo- ture is also displayed by species of three genera of the Mes- stome braconid subfamilies strongly supported the gall- ostoinae (sensu Zaldivar-Rivero´n et al., 2006)(Mesostoa, associated Labania and Monitoriella as being sister taxa Aspilodemon Fischer, and Hydrangeocola Bre´thes; Bre`thes, (Zaldivar-Rivero´n et al., 2006). That study, however, did 1927; Austin and Dangerfield, 1998; Oda et al., 2001). not sample other gall-associated doryctine genera and only Doryctine wasps are mainly idiobiont (i.e., they arrest included a scarce number of members of this group. Thus, the host development at the time of parasitization) ectopar- relationships both within the subfamily and among the asitoids of xylophagous Coleoptera larvae (Belokobylskij gall-associated genera were far from conclusive. et al., 2004a,b). However, gall association is exhibited by Different strategies have been proposed for aligning species of seven Neotropical doryctine genera, most of length-variable rDNA sequence data, though unalignable which have been reared from different unrelated host plant regions present in rDNA sequence alignments still are com- families. In Allorhogas, several species are known to induce monly excluded and therefore the results obtained are galls in seeds of species of Melastomataceae, Bignoniaceae based exclusively on regions that appear to be length-con- and at least four legume (Fabaceae) genera, though some served. In the case of secondary structure alignment other species are thought to be parasitoids of gall inhabit- (Gillespie, 2004), strict criteria of matched base-pairing ants (Maceˆdo and Monteiro, 1989; Maceˆdo et al., 1998; are used to delimit putatively homologiseable stem regions Marsh, 2002; Marsh et al., 2000). Moreover, the type spe- from ambiguously alignable loops and expansion zones. cies of Percnobracon Kieffer, Pe. stenopterus Kieffer, was However, coding approaches also exist that align length- reared from cecidomyiid (Diptera) galls on the legume variable regions conditionally based on indel length (e.g., Prosopis strombulifera (Lam.) Benth (Kieffer, 1910), and Simmons and Ochoterena, 2000; Lutzoni et al., 2000; recently this and two other species of the genus have been Zaldivar-Rivero´n et al., 2006). Alternatively, computer reared from the Argentinian endemic Pr. caldenia Burkart algorithms are often employed to find best matches (Martı´nez, 2006). Species of Monitoriella, on the other between bases in regions of ambiguous alignment, and hand, induce leaf galls on Philodendron Schott (Araceae) the incorporated variation may contribute to the phyloge- (Infante et al., 1995), whereas some members of Labania netic analysis performed. These include multiple alignment Hedqvist and Psenobolus Reinhard have been observed to (e.g., Clustal X, Thompson et al., 1997; MALIGN, develop in galls located on aerial roots and leaves, and Wheeler and Gladstein, 1994) and dynamic-based align- on the syconia of Ficus L. (Moraceae), respectively (Marsh, ments (e.g., POY, Wheeler, 1996; Gladstein and Wheeler, 2002; Ramirez and Marsh, 1996). Finally, the only 1996), and when using them it is increasingly common to described species of Donquickeia Marsh and Mononeuron use a ‘sensitivity’ approach, where the stability of the Fischer were reported to be reared from cecidomyiid galls results is assessed across a range of user-defined parame- of Mikania sp. (Asteraceae) and Eugenia rotundifolia Casar ters. Here we utilize three different alignment strategies, (Myrtaceae) (Penteado-Dias, 2000) and from a species of secondary structure alignment excluding unalignable Duguetia A.St.-Hil (Annonaceae) (Fischer, 1981), regions, secondary structure alignment with conditional respectively. alignment of indel regions, and multiple alignment using Since the process of host shift in phytophagous insects a range of parameters to assess the sensitivity of our results involves a number of genetic and ecological factors (e.g., to alignment procedure. secondary metabolites, competitors, predators; Thompson, In this study, we report a close relationship among most 1999), this is normally expected to occur more between clo- of the
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