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Phylogenetic Analysis of Eurytominae (Chalcidoidea: Eurytomidae) Based on Morphological Characters

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Phylogenetic Analysis of Eurytominae (Chalcidoidea: Eurytomidae) Based on Morphological Characters Blackwell Publishing LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082© 2007 The Linnean Society of London? 2007 1513 441510 Original Article PHYLOGENETIC ANALYSIS OF EURYTOMINAEH. LOTFALIZADEH ET AL. Zoological Journal of the Linnean Society, 2007, 151, 441–510. With 212 figures Phylogenetic analysis of Eurytominae (Chalcidoidea: Eurytomidae) based on morphological characters HOSSEINALI LOTFALIZADEH1, GÉRARD DELVARE2* and JEAN-YVES RASPLUS2 1Plant Pests and Diseases Research Institute, Evin, Tehran 19395–1454, Iran 2CIRAD – INRA, Centre de Biologie et de Gestion des Populations (CBGP), Campus International de Baillarguet, CS 30 016, F-34988 Montferrier-sur-Lez, France Received February 2006; accepted for publication December 2006 A phylogenetic study of the Eurytominae (Hymenoptera: Chalcidoidea) treating 178 taxa and based on 150 mor- phological characters is given. Several cladograms using the complete species sample, but obtained with different weightings, are presented. Local studies were also carried out to provide possible alternate topologies. The deep nodes of the trees were unstable and were never supported, but most of the superficial nodes were stable and robust. The results therefore provide support for a generic classification of the subfamily. The large genus Eurytoma – which includes about half of the described species of the subfamily – proved to be polyphyletic, and is redefined in a nar- rowed sense using putative synapomorphies. Bruchophagus and Prodecatoma were similarly redefined. The genera Philolema and Aximopsis are reconsidered and defined in a broader concept. A number of the species presently included in Eurytoma were transferred to these genera. Finally, 22 new generic synonymies are proposed and 33 spe- cies are transferred. The study also demonstrates that the Eurytomidae are polyphyletic. The results strongly sup- port a sister-group relationship between the Heimbrinae and the Chalcididae. The Rileyinae consist of two groups of unrelated taxa. A redefinition of the subfamily in a more restricted sense is supported by our results. The remain- ing group, consisting of the traditional Rileyinae, is included in the subfamily Buresiinae. Considered in this way they comprise the genera Buresium and Macrorileya, the latter being a senior synonym of Archirileya. The Buresi- inae appear as the sister group of the Eurytominae. We propose to restrict the family Eurytomidae to these two taxa. This sister-group relationship provides evidence to polarize the biological habits within Eurytominae. The common ancestor of Buresiinae is presumed to parasitize insects (mostly at the egg stage) living in grass stems. © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 151, 441–510. ADDITIONAL KEYWORDS: classification – Hymenotera – phylogeny. The Eurytomidae is one of the largest families of the strictly phytophagous species: Austrodecatoma, Chalcidoidea with 1457 nominal species in 83 genera Ausystole, Cathilaria, Prodecatoma (s.s.), Risbecoma, (Noyes, 2006; modified by Gates, 2007; Gates, Metz & Systole, and Tetramesa; their larvae develop in the Schauff, 2006). The family is present and common in stems of wild grasses, including cereal crops, or in all zoogeographical regions. Eurytomids exhibit a seeds of Umbelliferae, Leguminosae, Rosaceae, etc. wide range of biologies, but the majority of the larvae Others are gall formers in the roots and twigs of sev- are endophytic: as seed eaters, gall formers, or as par- eral plants, e.g. Aranedra and Foutsia develop in Neo- asitoids of phytophagous insects. Most eurytomids are tropical Philodendron spp. (Boudek, 1988; Noyes, primary or secondary parasitoids, attacking eggs, lar- 2002). However, it is difficult to assess the exact host– vae, or pupae of various arthropod groups (Diptera, parasitoid relationships for most endophytic species. Coleoptera, Hymenoptera, Lepidoptera, Orthoptera, One fraction of Eurytomidae that are supposed to and Araneae). The secondary parasitic eurytomids develop as parasitoids may well be inquilines. Various mostly attack Ichneumonoidea. Some genera include genera (Sycophila, Ficomila) reared from syconia of Ficus are actually inquilines in Epichrysomallinae galls. Moreover, some eurytomids, such as Eurytoma *Corresponding author. E-mail: [email protected] pachyneuron Girault, 1916 and Eurytoma parva Phil- © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 151, 441–510 441 442 H. LOTFALIZADEH ET AL. lips, 1918, are known to switch to phytophagy before to Gates (2007) the proposed names do not satisfy the and/or after consuming an insect host (Phillips, 1917; criteria for availability set in Article 13 (ICZN, 1999). Phillips, 1927). Another interesting case of biological Finally, Zerova (1988) used Ashmead’s system, but plasticity concerns species belonging to the Eurytoma placed Buresium in a separate subfamily, the Buresi- rosae aggregate. In this group, adults are morpholog- inae. Subba Rao (1978) broke away from Ashmead’s ically similar and impossible to segregate into mor- classification, and recognized only two subfamilies phospecies (Claridge & Askew, 1960). Their larvae, (Rileyinae and Eurytominae). Stage & Snelling (1986), however, show different behaviour according to the revising the Heimbrinae, added them to Subba Rao’s species. Whereas larvae of E. rosae predate on the classification and proposed the first classification inquiline cynipids associated with Rosa spp., Eury- based on a comparative morphological analysis. This toma brunniventris larvae are associated with oaks classification was followed by Boudek (1988), in his and feed both on the gall-forming cynipid larvae and monography of the Australasian chalcidoid fauna, on the gall tissue. This short account points to the DiGiulio (1997), and finally Noyes (2002), in his data- great diversity of the biology and the quick evolution base of World Chalcidoidea. Gates (2007) tabulated of diet habits and feeding behaviour in related taxa. the systems of classification previously used by differ- Because of their diversified biology Eurytomidae also ent authors. He also synonymized the Buresiinae with have contrasting economic importance. Most seed eat- the Eurytominae and revised the Rileyinae, which ers of cultivated plants (Bruchophagus, Systole, Eury- were defined more narrowly, i.e. the genera Archiri- toma of the amygdali group, etc.) are pest insects; leya, Buresium, and Macrorileya were excluded and however, some phytophagous species can be used for transferred to Eurytominae. biological control as they feed on weeds or invasive Consequently, two systems of classification conflict: plants (Burks, 1958; Simmonds, 1980). A biological con- either Eurytominae are split into five subtaxa, follow- trol program using Tetramesa romana (Walker, 1873), ing Ashmead (1904), or are kept undivided as pro- a gall-stem eurytomid wasp, is presently being devel- posed by Stage & Snelling (1986). Zerova (1988) oped to slow the expansion of the invading Arundo carried out a character analysis and postulated donax L., 1753 (Poaceae) in southern USA (A. Kirk, ground-plan features for Eurytomidae, but she neither pers. comm.). Finally, some beneficial Eurytomidae are described how she polarized the characters nor distin- used as biological control agents, e.g. Eurytoma guished between primitive and derived states in order oryzivora Delvare, 1988, which is a parasitoid of the tto define eurytomid taxa. stem borer Maliarpha separatella Ragonot, 1888 The generic classification is poorly supported. Fur- (Pyralidae) in tropical Africa (Delvare, 1988; Polaszek, thermore, over one half of the species are described in 1998). the genus Eurytoma and, conversely, 42 genera are Abundantly trapped in biodiversity surveys (Noyes, monospecific (Figs 1, 2). Generic distinctiveness is 1989) and easily reared from various plant structures, rarely clear despite recent attempts to improve our Eurytomidae seem to have an underestimated ecolog- knowledge (e.g. Burks, 1971; Boudek, 1988; Naren- ical importance. Their high diversity [more than dran, 1994; Zerova, 1995). Indeed autopomorphies can 25 000 species if the estimations provided by Noyes be postulated for the monospecific genera, but the (2000) and Heraty & Gates (2004) for the Chalcidoidea largest genera are not based on shared derived char- as a whole are correct], their relatively homogeneous acters. As Burks (1971) wrote: ‘Many species are habitus, the presence of complexes of cryptic species, and the lack of recent and reliable taxonomic revisions, combine to prevent reliable specific identification. As a result most published biological data are doubtful. The Eurytomidae have a quite distinct habitus among the other Chalcidoidea, and were recognized as a discrete group by Walker as early as 1832. Walker (1832) included four genera in the family: Eurytoma, Decatoma, Isosoma, and Systole. Ashmead (1904) described 23 new genera and erected the tribes Axi- mini, Eurytomini, Isosomini, Rileyini, and Decato- mini, which were accepted by Bugbee (1936). These tribes were raised to subfamily rank (Ferrière, 1950) and maintained by Nikol’skaya (1952), Claridge (1961b), and Peck (1963). Burks (1971, 1979) added Figure 1. Described species of Eurytomidae: classes of three new subfamilies (Heimbrinae, Prodecatominae, biodiversity (number of species described within each and Philoleminae) without any diagnoses. According genus) according to genus. Data from Noyes (2002). © 2007 The Linnean Society
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