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Suprageneric Systematics of Flea Beetles (Chrysomelidae: Alticinae)

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Suprageneric Systematics of Flea Beetles (Chrysomelidae: Alticinae) Molecular Phylogenetics and Evolution 62 (2012) 793–805 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Suprageneric systematics of flea beetles (Chrysomelidae: Alticinae) inferred from multilocus sequence data ⇑ ⇑ Deyan Ge a,c,e, Jesús Gómez-Zurita b, Douglas Chesters a,c,d, Xingke Yang a, , Alfried P. Vogler c,d, a Key Laboratory of the Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road, Chaoyang, Beijing 100101, China b Institut de Biologia Evolutiva (CSIC-UPF), 08003 Barcelona, Spain c Department of Entomology, Natural History Museum, Cromwell Road, London SW7 5BD, UK d Imperial College London, Department of Life Sciences, Silwood Park Campus, Ascot SL5 7PY, UK e Graduate School of Chinese Academy of Sciences, Beijing 100039, China article info abstract Article history: Recent phylogenetic studies of flea beetles (Alticinae) based on morphological or molecular data have Received 15 October 2010 focused on the relationship and possible paraphyly with respect to the closely related Galerucinae, while Revised 13 November 2011 the supra-generic classification mainly dates back to the 19th century. Here, phylogenetic analysis was Accepted 21 November 2011 performed on DNA sequences for two mitochondrial (rrnL and cox1) and two nuclear (SSU and LSU rRNA) Available online 14 December 2011 genes from 158 genera and 165 species that cover most suprageneric groups of flea beetles proposed in the older literature. Various alignment strategies and tree search methods were used to test the stability Keywords: of major clades. Besides confirmation of the placement of several alticine lineages within Galerucinae, a Taxonomic classification preliminary framework for classification of the main alticine clades was obtained. It is proposed to rec- Bayesian analysis Data partitioning ognize 18 groups of genera based on well-supported nodes. These include the Altica, Amphimela, Aphth- Metafemoral spring ona, Blepharida, Chabria, Chaetocnema, Dibolia, Disonycha, Griva, Lactica, Longitarsus, Manobia, Monoplatus, Galerucinae Nisotra, Oedionychis, Pentamesa, Phygasia and Pseudodera groups. These groups provide a novel perspec- tive to the existing classification. The analysis of 14 morphological characters used in the traditional clas- sification of Alticinae and Galerucinae revealed high levels of homoplasy with respect to the DNA-based tree, but significant hierarchical structure in most of them. Even if not unique to any particular group of genera, these traits largely corroborate the groupings established with DNA sequences. Ó 2011 Published by Elsevier Inc. 1. Introduction used as biological control agents for invasive weeds (e.g., Tansey et al., 2005; Roehrdanz et al., 2006). Furthermore, they also are Flea beetles have been treated as a subfamily (Alticinae) of the widely used as experimental models for evolutionary and ecologi- leaf beetles (Chrysomelidae) (Maulik, 1929; Heikertinger and Csiki, cal research (Vencl and Morton, 1998; Xue et al., 2007). A striking 1939–1940; Seeno and Wilcox, 1982; Konstantinov and Vanden- feature of these beetles is their ability to perform huge jumps to es- berg, 1996). They are closely related to the subfamily Galerucinae cape from predators, enabled by an enlarged endosclerite of the and sometimes have been considered a tribe (Alticini) within this hind femur, the ‘metafemoral spring’ (Maulik, 1929; Furth, 1980). group (Chapuis, 1875; Reid, 1995; Lingafelter and Konstantinov, The presence of this structure and the thickened hind femurs in 1999). The Alticinae comprise nearly 570 genera and more than which it is contained are widely used to separate this group from 10,000 species (Seeno and Wilcox, 1982), and together with an other chrysomelids (Chen, 1985; Arnett et al., 2002). additional 6000 species of Galerucinae, they represent nearly half The prevailing view of a sister relationship of Galerucinae and of all described species of Chrysomelidae. Flea beetles are well Alticinae is now being replaced by morphological and molecular known for their economical and ecological importance. For exam- evidence that Alticinae are nested within Galerucinae. Initially, ple, they include species like Phyllotreta cruciferae and Phyllotreta studies of Farrell (1998) using the nuclear SSU rRNA gene com- striolata which are the most important pests of crucifer field crops bined with morphological data (Reid, 1995) established the reci- in North America (Capinera, 2008), while other species have been procal monophyly of Alticinae and Galerucinae which was also maintained under increased taxon sampling and an expanded gene set (Gómez-Zurita et al., 2008). However, the paraphyly of Gale- ⇑ Corresponding authors. Address: Department of Entomology, Natural History rucinae emerged from a matrix of 50 morphological characters Museum, Cromwell Road, London SW7 5BD, UK (A.P. Vogler). (Lingafelter and Konstantinov, 1999). This was corroborated in a E-mail addresses: [email protected] (X. Yang), [email protected] (A.P. Vogler). 1055-7903/$ - see front matter Ó 2011 Published by Elsevier Inc. doi:10.1016/j.ympev.2011.11.028 794 D. Ge et al. / Molecular Phylogenetics and Evolution 62 (2012) 793–805 recent paper accompanying the current study (Ge et al., 2011) therefore their phylogenetic placement is difficult. For example, showing that Galerucinae includes several small lineages hitherto several spring-bearing genera have hindwing venation, female classified as Alticinae. The latter therefore was found to be poly- spermatheca, male aedeagus, or ‘elytron-to-body meshing struc- phyletic. A key issue regarding the polyphyly of Alticinae is the po- tures’ typical of galerucines, or they have been considered to be sition of various groups considered to be ‘incertae sedis’ which had ‘Luperus like’ or ‘Pyrrhalta like’, referring to galerucine genera (Reid, not been included in earlier molecular studies (Farrell, 1998; Bun- 1992; Samuelson, 1994; Furth and Suzuki, 1998). nige et al., 2008; Gómez-Zurita et al., 2008; Gillespie et al., 2008). Besides the difficulties of establishing the limits of Alticinae rel- For these ‘problematical’ taxa (listed in SI Table 1), their association ative to Galerucinae, the internal relationships within Alticinae re- with either subfamily based on the presence or absence of the main poorly understood. As early as 1875, Chapuis established 19 metafemoral spring is not consistent with other characters and groups of genera based on the morphology of thorax, anterior coxal Table 1 Synopsis of existing suprageneric classifications in Alticinae and groups of genera proposed in this study. Chapuis (1875) Horn (1889) Takizawa (2005) This study Blepharidites: Notozona, Blepharidaa, Blepharidea: Blepharidaa Podontia group: Blepharidaa, Ophridaa, 4. Blepharida group: Blepharida, Ophrida, Podontia Ophridaa, Podontiaa Podontiaa Arsipodites: Arsipodaa, Nisotraa, Arsipodes: Mantura 14. Nisotra group: Euphitrea, Sinocrepis, Podagrica, Podagricaa, Balanomorpha Sphaeroderma, Nisotra Amphimelites: Amphimelaa Clitea group: Cliteaa, Crepidoderaa, 2. Amphimela group: Amphimela, Podagricomela, Hippuriphilaa, Lythrariaa Clitea 12. Manobia group: Manobia, Aphthonoides, Asiorestia, Lythraria Halticites: Halticaa, Pelonia, Halticae: Halticaa Altica group: Alticaa, Lysathiaa, 1. Altica group: Altica, Macrohaltica, Syphraea Phrynocepha, Plectrotetra, Cacoscelis, Macrohalticaa, Aphthonaa, Disonychaa, Caloscelis, Caeporis Neocrepidodera, Othocrepisa Aphthonites: Longitarsusa, Phyllotretaa, Aphthona: Aphthonaa, 3. Aphthona group: Aphthona, Aphthonomorpha, Glyptinaa, Botaphilaa, Aphthonaa Longitarsusa, Glyptinaa, Glyptina Phyllotretaa Lacticites: Lacticaa, Diphaulaca, Lactica: Lacticaa, 10. Lactica group: Hermaeophaga, Lactica, Hermaeophagaa, Psilapha, Myrcina, Diphaulaca, Trichaltica Orthocrepis Xuthea Disonychae: Disonychaa, 8. Disonycha group: Diphaltica, Agasicles, Disonycha Hemiphrynus Longitarsus group: Longitarsusa 11. Longitarsus group: Lanka, Longitarsus, Tegyrius Lanka group: Lankaa Crepidoderites: Pseudoderaa, Chaetocnemae: Chaetocnema group: Chaetocnemaa 6. Chaetocnema group: Psylliodes, Chaetocnema, Clamophora, Crepidoderaa, Systenaa, Chaetocnemaa Crepidodera Tenosis, Prasona, Iphitrea Crepidoderae: Hemiglyptus, Crepidoderaa, Orthaltica, Epitrixa, Leptotrix Psylliodites: Psylliodesa Psylliodes: Psylliodesa Liprus group: Liprus, Phygasiaa, 17. Pseudodera group: Pseudodera, Laboissierea Phyllotretaa, Pseudoderaa, Psylliodesa, Sangariolaa 18. Phygasis group: Phygasia, Trachyaphthona Diboliites: Diboliaa, Megistops Dibolia: Diboliaa Sphaeroderma group: Argopistesa, 7. Dibolia group: Argopistes, Dibolia, Jacobyana Argopusa, Diboliaa, Megistops, Schenklingiaa, Sphaerodermaa Mniophilites: Mniophila, Argopusa, Mniophilae: Argopistesa, Hypnophita, Sphaerodermaa, Sphaerodermaa Apteropeda, Argopistesa 16. Pentamesa group: Pentamesa, Bhamoina, Argopus 5. Chabria group: Chabria, Parathrylea, Sutrea, Chabrisoma Oedionychites: Omophoitaa, Oedionychis: Hamletia, Hemipyxis group: Alagoasaa, Kuschelina, 15. Oedionychis group: Hemipyxis, Hyphasis, Physodactyla, Oedionychisa, Oedionychisa Walterianellaa, Disonychaa, Hemipyxisa, Philopona, Physoma, Oedionychis, Alagoasa, Eutornus, Physonychis, Lithonoma, Omophoitaa, Philoponaa Omophoita, Asphaera, Wanderbiltiana, Aspicela Physomaa Aspicelites: Aspicelaa, Sebaethea, Aspicelea: Homophaeta, Sphaerometopa group: Sphaerometopa (to Asphaeraa, Sphaerometopaa, Phydanis Galerucinae)
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