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Diptera: Agromyzidae) Inferred from Sequence Data from Multiple Genes

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Diptera: Agromyzidae) Inferred from Sequence Data from Multiple Genes Molecular Phylogenetics and Evolution 42 (2007) 756–775 www.elsevier.com/locate/ympev Phylogenetic relationships within the leaf-mining Xies (Diptera: Agromyzidae) inferred from sequence data from multiple genes Sonja J. ScheVer a,¤, Isaac S. Winkler b, Brian M. Wiegmann c a Systematic Entomology Laboratory, USDA, Agricultural Research Service, Beltsville, MD 20705, USA b Department of Entomology, University of Maryland, College Park, MD 20740, USA c Department of Entomology, College of Agriculture and Life Sciences, North Carolina State University, Raleigh, NC 27695, USA Received 9 January 2006; revised 29 November 2006; accepted 18 December 2006 Available online 31 December 2006 Abstract The leaf-mining Xies (Diptera: Agromyzidae) are a diverse group whose larvae feed internally in leaves, stems, Xowers, seeds, and roots of a wide variety of plant hosts. The systematics of agromyzids has remained poorly known due to their small size and morphological homogeneity. We investigated the phylogenetic relationships among genera within the Agromyzidae using parsimony and Bayesian anal- yses of 2965 bp of DNA sequence data from the mitochondrial COI gene, the nuclear ribosomal 28S gene, and the single copy nuclear CAD gene. We included 86 species in 21 genera, including all but a few small genera, and spanning the diversity within the family. The results from parsimony and Bayesian analyses were largely similar, with major groupings of genera in common. SpeciWcally, both analy- ses recovered a monophyletic Phytomyzinae and a monophyletic Agromyzinae. Within the subfamilies, genera found to be monophyletic given our sampling include Agromyza, Amauromyza, Calycomyza, Cerodontha, Liriomyza, Melanagromyza, Metopomyza, Nemorimyza, Phytobia, and Pseudonapomyza. Several genera were found to be polyphyletic or paraphyletic including Aulagromyza, Chromatomyia, Phytoliriomyza, Phytomyza, and Ophiomyia. We evaluate our Wndings and discuss host-use evolution in light of current agromyzid taxon- omy and two recent hypotheses of relationships based on morphological data. Published by Elsevier Inc. Keywords: Phytophagy; Acalypterate; Opomyzoidea; Host-use evolution; Endophagy 1. Introduction one or a few closely related plant species (Spencer, 1990; ScheVer and Wiegmann, 2000). Host-use evolution within The leaf-mining Xies (Diptera: Agromyzidae) are small the Agromyzidae is a subject of great interest because Xies having phytophagous larvae that feed within leaves, diversiWcation in this group appears to be largely associated stems, roots, Xowers, or seeds. Agromyzids attack a broad with host shifts and dietary specialization (Spencer, 1990; diversity of plant hosts, including more than 140 plant fam- Kulp, 1968; ScheVer and Wiegmann, 2000). However, mod- ilies representing all major terrestrial plant groups, with the ern phylogenetic analyses necessary for elaborating the his- exception of mosses and most gymnosperms (Spencer, tory of agromyzid/host associations have only recently 1990; Benavent-Corai et al., 2005). These Xies are distrib- been applied to studies of these Xies (ScheVer and Wieg- uted worldwide with their greatest diversity in northern mann, 2000; Dempewolf, 2001). temperate regions (Spencer, 1977). Despite the broad diet Despite their near ubiquity and interesting larval habits, breadth exhibited by agromyzids as a group, most agro- the systematics of agromyzids has remained rather poorly myzid species are remarkably specialized, feeding on only understood due to their small size and morphological homogeneity. Species identiWcation generally requires dis- section of the male genitalia, and it is diYcult to identify * Corresponding author. Fax: +1 301 504 6482. some female specimens even to genus using only morpho- E-mail address: [email protected] (S.J. ScheVer). logical characters. Currently, the Agromyzidae contains 1055-7903/$ - see front matter Published by Elsevier Inc. doi:10.1016/j.ympev.2006.12.018 S.J. ScheVer et al. / Molecular Phylogenetics and Evolution 42 (2007) 756–775 757 two subfamilies, the Agromyzinae and the Phytomyzinae, Here, we present the Wrst comprehensive molecular phy- based on one larval and one adult character (Spencer and logenetic analysis of the entire family Agromyzidae. A Steyskal, 1986) although these characters are not always major goal is to provide new evidence from nuclear and consistent (von Tschirnhaus, 1971). Twenty-eight genera mitochondrial genes on higher-level relationships within are recognized containing approximately 2860 described the family. With these new phylogenetic results, we investi- species (Table 1), although it is clear from the number of gate patterns of diversiWcation within leafminers, evaluate new species found during regional surveys and detailed relative support from genes and morphology for currently study of species groups (e.g., ScheVer and Wiegmann, 2000; recognised genera as well as for key areas of agromyzid Zlobin, 1994a, 2002) that this represents only a fraction of classiWcation, and establish an initial framework for future agromyzid diversity (see also Spencer, 1977; Spencer and investigations of agromyzid relationships and host-use evo- Steyskal, 1986). Nearly a third of the known genera have lution. fewer than 10 species (Table 1), while many of the other genera are large, containing many groups of morphologi- 2. Materials and methods cally similar species that often feed on closely related host plants (Spencer, 1990; also e.g., GriYths, 1974, 1976, 1977; Agromyzid specimens representing 86 species in 21 ScheVer and Wiegmann, 2000; Zlobin, 2000). genera were obtained from a variety of locations around Modern hypotheses of relationships among agromyzid the world (Appendix A). We attempted to include conge- genera come primarily from two sources: a verbal “phy- ners from diVerent subgenera or diVerent species groups letic lines” scheme by Spencer (1990) in his consummate whenever possible, particularly for the larger genera. treatise on agromyzids and their host plants (Table 2), For outgroups, we chose two Fergusonina species (Fer- and a quantitative morphological phylogeny based on 83 gusoninidae). Several authors have suggested that the larval and adult characters (Fig. 1) in a dissertation by Agromyzidae and the Fergusoninidae are closely related, Dempewolf (2001). Spencer envisioned four phyletic lines and at one time fergusoninids were even placed within the within the family with the “Penetagromyza group” corre- Agromyzidae (Tonnoir, 1937; Colless and McAlpine, sponding to the Agromyzinae, and the traditional Phy- 1970). Several morphological characters suggest that the tomyzinae broken into the “Phytobia group,” the Fergusoninidae may be the sister group to the Agromyzi- “Phytoliriomyza group,” and the “Napomyza group.” dae (McAlpine, 1989), although recent molecular work Relationships among the latter three groups are unspeci- does not corroborate this (Rung, Winkler, and ScheVer, Wed. Most important in Spencer’s scheme is the assertion, unpublished data). The Odiniidae has also been suggested Wrst suggested by Nowakowski (1962), that Phytobia, a to be the sister group to the Agromyzidae (Hennig, 1958 widespread genus of large, cambium-mining species, is of as reported by McAlpine, 1989; Spencer, 1969; Dempe- ancient origin and represents the “primitive” condition wolf, 2005). We included a species of Odinia as an addi- within the family. This continues a long-held belief among tional outgroup in our analyses. agromyzid workers that groups of small leaf-mining spe- Specimens were preserved for study in 95% ethanol and cies are derived from larger stem-feeding species (Nowa- stored at ¡80 °C prior to DNA extraction. For most spe- kowski, 1962; Spencer, 1990; von Tschirnhaus, 1991). In cies, a male specimen was chosen for DNA extraction fact, within each of Spencer’s four phyletic lines the gen- because of the importance of male genitalia for species era are arranged from a “primitive” stem-mining genus to identiWcation. Preliminary identiWcation of specimens “more advanced” leaf-mining groups. based on external morphology was performed by SJS and Dempewolf’s (2001, 2005) phylogenetic analysis of 83 ISW using keys by Spencer (1969, 1972, 1976, 1977), Spen- larval and adult characters resulted in 90 most parsimoni- cer and Stegmaier (1973), and Spencer and Steyskal ous trees obtained by successive weighting using the consis- (1986). Each male specimen was dissected by removing tency index. The strict consensus of these trees is shown in the posterior half of the abdomen and clearing it by sub- Fig. 1 (redrawn from Dempewolf, 2005). In this analysis, merging it in a hot 10% KOH solution for 5 min. Cleared the two subfamilies are found to be monophyletic, although genitalia were then used for Wnal identiWcations and support values for these and all other relationships are not retained as voucher specimens. These genitalia and, in available. Relationships diVer from those suggested by some cases, additional intact specimens have been depos- Spencer in several ways, most notably in Wnding ited as vouchers in the National Museum of Natural His- Aulagromyza and Gymnophytomyza to be associated with tory in Washington, DC. the Napomyza group of Spencer. Additionally, Ama- Total nucleic acids were extracted from single dis- uromyza is found to be sister to Cerodontha and well inside sected specimens by grinding the specimen in PBS solu- a clade also including Liriomyza, Galiomyza, Phy- tion and following the insect protocol B of the DNeasy
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