Molecular Phylogeny and Evolution of Host-Plant Use in Conifer Seed Chalcids in the Genus Megastigmus (Hymenoptera: Torymidae)
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Systematic Entomology (2005), 31, 47–64 DOI: 10.1111/j.1365-3113.2005.00310.x Molecular phylogeny and evolution of host-plant use in conifer seed chalcids in the genus Megastigmus (Hymenoptera: Torymidae) MARIE-ANNE AUGER-ROZENBERG1 , CAROLE KERDELHUE´1, *, EMMANUELLE MAGNOUX1 , JEAN TURGEON2 , JEAN-YVES RASPLUS3 andALAIN ROQUES1 1INRA, Unite´de Zoologie Forestie` re, Ardon, Olivet, France, 2Natural Resources Canada – Canadian Forest Service, Great Lakes Forestry Centre, Ontario, Canada and 3INRA, CBGP, Campus International de Baillarguet, Montferrier-sur-Lez cedex, France Abstract. Phylogenetic relationships amongst Megastigmus species (Chalcidoidea: Torymidae) associated with conifer seeds were inferred from DNA sequence data. Twenty-nine species of seed chalcids were analysed using two different genes, cytochrome b (mitochondrial DNA) and the D2 domain of the 28S ribosomal DNA. Maximum-parsimony and maximum-likelihood analyses showed that taxa formed two monophyletic groups, one clade comprising all species associated with Cupressaceae and Taxodiaceae hosts with the exception of Chamaecyparis,andthe other clade composed of species associated with Pinaceae. Species infesting Cupressaceae and Taxodiaceae seemed to be specialized to particular host genera or even to be species specific, which was consistent with a taxonomic radiation following initial host adaptation. By contrast, Megastigmus species associated with Pinaceae appeared capable of shifting onto different congeneric species or even onto a new host genus, with their evolution apparently less constrained by plant association. We hypothesized that the Megastigmus groupassociatedwithPinaceaemay have a much higher invasive potential than that related to Cupressaceae. The study also confirmed the presence of invasive Nearctic species in the Palaearctic, and demonstrated the existence of a cryptic species complex. Introduction nine are seed feeders (Grissell, 1999). Other species, most of which occur in Australia, are presumed to be parasitoids, Most insects infesting cones and seeds of conifers are spe- gall-makers or have unknown hosts. Within the obligate cialists incapable of developing on other substrates seed-feeding group, forty-one species are associated with (Turgeon et al., 1994). An important group is the seed conifers (Pinaceae, Cupressaceae and Taxodiaceae), some chalcid wasp genus Megastigmus Dalman (Hymenoptera: being considered as economic pests, whereas the others Chalcidoidea: Torymidae: Megastigminae). More than 125 develop in seeds of angiosperms, especially Rosaceae and species of Megastigmus have been described, of which fifty- Anacardiaceae (Roques & Skrzypczynska, 2003). The spe- cies associated with conifers are considered to be highly specialized, being either species specific (even if several potential host species coexist in the same place) or restricted to a conifer genus. However, the degree of host specializa- Correspondence: Marie-Anne Auger-Rozenberg, INRA, Unite´ tion remains unclear for some species. For most phytopha- de Zoologie Forestie` re, BP20619 Ardon, 45166 Olivet cedex, gous insects, long-term association with a particular host France. E-mail: [email protected] eventually results in the loss of genetic variation for the ability *Present address: INRA, UMR Biogeco, Pierroton, Cestas, to use alternative hosts. Specialists thus might become con- France. strained irreversibly on a restricted set of host plant species # 2006 The Royal Entomological Society 47 48 M.-A. Auger-Rozenberg et al. considered to be chemically similar (Futuyma & Moreno, associated genetic variation. Cytochrome b (cyt. b)isa 1988; Becerra, 1997; Kelley & Farrell, 1998). Nevertheless, mitochondrial protein-coding gene used in molecular sys- recent studies have suggested that not only secondary plant tematics (Gimeno et al., 1997; Simmons & Weller, 2001). chemistry, but also a set of other parameters (biogeogra- The few studies that have used cyt. b to resolve systematic phical, genetic and ecological constraints), might explain relationships within Chalcidoidea indicate that it is appro- host shifts better than plant phylogeny and plant geogra- priate for the resolution of intrageneric and intraspecific phical distribution (Termonia et al., 2001). A few documen- relationships (Kerdelhue´et al., 1999; Lopez-Vaamonde ted cases on Megastigmus species have suggested that shifts et al., 2001). The nuclear 28S rDNA transcript evolves to new hosts of different genera may occur (Grissell, 1999; more slowly than cyt. b and may be appropriate in M.-A. Auger-Rozenberg, pers. obs.). However, wasp Hymenoptera for divergences ranging from closely related misidentifications and the possible occurrence of cryptic species to family level divergences (Belshaw et al., 1998; species may have confounded these observations. Rasplus et al., 1998; Gibson et al., 1999; Mardulyn & Megastigmus has a nearly worldwide distribution, but Whitfield, 1999; Campbell et al., 2000; Babcock et al., conifer seed-feeding species seem to be restricted to the 2001; Lopez-Vaamonde et al., 2001; Rokas et al., 2002). Holarctic region. Most species have been described from the West Palaearctic region and from North America, but the discovery of an increasing number of species from China Materials and methods is likely (Roques et al., 1995; A. Roques, pers. obs.) and cryptic species probably exist in Central Asia (Grissell, Insect collection 1999). Moreover, these species exhibit a large invasive poten- tial facilitated by the globalization of seed trade. Some of From 1994 to 2004, an extensive survey of seed chalcids their life cycle features tend to facilitate insect introduction was undertaken on different native and exotic species of (e.g. entire development concealed within the same seed) and conifers across the Northern Hemisphere (Table 1). The establishment in exotic countries (e.g. parthenogenesis and sampled seed lots were all radiographed using a Faxitron- prolonged diapause, allowing them to cope with the hetero- 43855Ò apparatus (15 kV, 3 mA, 30300 to 40300 depending geneity in space and time of host abundance; for reviews, see on seed species) and X-ray-sensitive films (KodakÒ Turgeon et al., 1994; Roques et al., 2003). Here again, as ‘Industrex M’). The insect-infested seeds were placed in many morphological characters can be misleading in chalci- individual rearing boxes stored in an outdoor insectary doid taxonomy, the possibility remains that an invasive located at INRA, Orle´ans, France [107 m above sea-level Megastigmus species actually is a cryptic native species that (a.s.l.)]. Adult emergence was recorded over the 3 years would have been misidentified. following seed maturation because of a possible prolonged Despite their taxonomic, morphological and ecological diapause (Roques & Skrzypczynska, 2003). After emer- diversity, our knowledge of the phylogenetic relationships gence and identification, wasps were preserved in 100% within Megastigminae remains limited, and the patterns of alcohol at À20 C. For one species (M. strobilobius host-associated radiations have been largely unexplored. Ratzeburg), we failed to collect infested seeds or emerging The evolutionary relationships amongst Megastigmus spe- adults; consequently, dry museum specimens were used. All cies have been questioned previously with allozyme mar- individuals (both native and introduced) sampled from the kers (Roux & Roques, 1996), but using a limited data set Western Palaearctic region were identified following and with low phylogenetic resolution. A reconstructed evo- Roques & Skrzypczynska (2003). The Chinese species lutionary history would provide a crucial framework for (M. cryptomeriae Yano, M. likiangensis Roques & Sun understanding the origins and evolution of the highly spe- and M. pingii Roques & Sun) were identified by cialized association between conifers and seed chalcids. A. Roques, and Nearctic species (M. hoffmeyeri Walley, Specifically, it could test if Megastigmus species occurring M. thyoides Kamijo, M. tsugae Crosby) by J. Turgeon. on the same host genus or family share a recent common The descriptions of two new species are included in this ancestor; moreover, it could estimate the degree of biologi- paper (Appendix: M. thuriferana Roques and El Alaoui on cal constraint due to host use and, furthermore, help test Juniperus thurifera and M. formosana Roques and Pan on hypotheses for the geographical distribution and radiation J. formosana). In addition to the Megastigmus species of the genus Megastigmus worldwide. Moreover, molecular reared from conifers, we also included a seed feeder from data would assist in investigating cryptic species, both in Rosaceae (M. rosae Boucˇek) and two European endopar- the case of apparent host shifts and supposed invasive asitoids of cynipid gall wasps (M. dorsalis Fabricius and species. M. stigmatizans Fabricius). Three species of Torymus Here, we present the first phylogenetic reconstruction of (Torymidae: Toryminae) were used as outgroup (Grissell, Megastigmus associated with conifers, based on DNA 1999). The species used in the study, their collecting locality sequencing of twenty-nine species, twenty-six of which are and distribution are summarized in Table 1. Voucher mate- conifer seed feeders. Partial sequences of the cytochrome b rial of specimen remnants and associated complete speci- gene (mitochondrial DNA, mtDNA) and of the D2 region mens from the same original series are kept in ethanol in of the 28S ribosomal subunit (rDNA) were used to