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Molecular Phylogeny Reveals Independent Origins of Body Scales In Molecular Phylogenetics and Evolution 70 (2014) 231–239 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular phylogeny reveals independent origins of body scales in Entomobryidae (Hexapoda: Collembola) ⇑ Feng Zhang a,b,c, Zhen Chen b, Rui-Rui Dong b, Louis Deharveng d, Mark I. Stevens e,f, Ya-Hong Huang b, , ⇑ Chao-Dong Zhu a, a Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, PR China b School of Life Sciences, Nanjing University, Nanjing 210093, PR China c Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing, PR China d UMR 7205 CNRS, Origine, Structure et Evolution de la Biodiversité, Museum National d’Histoire Naturelle, Paris, France e South Australian Museum, GPO Box 234, Adelaide, Australia f School of Earth and Environmental Sciences, University of Adelaide, Australia article info abstract Article history: Entomobryidae is the largest family in Collembola but relationships within the family have never been Received 3 January 2013 subjected to rigorous phylogenetic analyses. Within the family, body scales are present in many species, Revised 6 September 2013 and are fundamental in the classification at the subfamilial and tribal levels. A molecular phylogeny was Accepted 26 September 2013 reconstructed using the nuclear 18SrRNA and partial 28SrRNA and the mitochondrial 16SrRNA to exam- Available online 4 October 2013 ine the evolution of scales across Entomobryidae subfamilies. These datasets were analyzed separately and combined, with parsimony, likelihood and Bayesian algorithms. Monophyly of Orchesellinae was Keywords: not recovered, and it was split into a scaled clade and an unscaled clade, contradicting to all recent tax- rRNA onomic conceptions. The monophyly of Entomobryinae, Seirinae and Lepidocyrtinae is well supported mtDNA Classification however within Entomobryinae, the polyphyly of Entomobryini and Willowsiini implies that classifica- Convergence tion using the presence/absence of scales is not valid. Analyses of ancestral character state reconstruction Ancestral state reconstruction in Entomobryidae indicate that the presence of body scales have evolved independently at least five times, with a loss of scales occurring independently at least twice. A revision of the family Entomobryidae on molecular and morphological basis is clearly needed. Ó 2013 Elsevier Inc. All rights reserved. 1. Introduction Several studies have made significant contributions to the clas- sification of the family Entomobryidae (Börner, 1906, 1913; Yosii, Springtails (Collembola) are widespread, small arthropods 1961; Szeptycki, 1979; Yoshii and Suhardjono, 1989); Soto- found in all kinds of terrestrial ecosystems, from polar regions to Adames et al., 2008). Five main groups are traditionally recog- tropical areas, from plains to plateau. Entomobryidae, having long nized: Orchesellinae, Entomobryini, Willowsiini, Seirinae, Lep- appendages (antennae, legs and furcula) and elongated fourth idocyrtinae (Szeptycki, 1979), with the latter two (Seirinae and abdominal segment, is the largest family of Collembola with more Lepidocyrtinae) often treated as tribes within Entomobryinae than 1500 species (Bellinger et al., 1996–2013). As soft bodied (Yoshii and Suhardjono, 1989; Soto-Adames et al., 2008). Entomo- arthropods, collembolans are rarely preserved as fossils. The earli- bryini and Willowsiini are united as Entomobryinae in Szeptycki’s est fossil Rhyniella praecursor Hirst and Maulik, 1926 from the Low- system (Szeptycki, 1979). Five additional mono- or oligospecific er Devinian predates other hexapods (Whalley and Jazembowski, suprageneric taxa have been recognized that are not included in 1981; Whalley, 1995); while, several entomobryid fossils (Entomo- the present analysis: Capbryinae, and the tribes Bessoniellini, brya, Lepidocyrtus, Seira) from Miocene amber have also been re- Corynotrichini, Mastigocerini, Nothobryini among Orchesellinae. corded and are similar to extant species (Christiansen, 1971; Compared to other scaled collembolan groups (Tomoceroidea, Par- Mari-Mutt, 1983). onellidae), scales and their morphology in the classification of Entomobryidae are quite important diagnostic characters at the generic and suprageneric levels. Willowsiini, Seirinae, Lepidocyrti- ⇑ Corresponding authors. Fax: +86 10 64807099 (C.-D. Zhu). nae and part of Orchesellinae are scaled, with Willowsiini and E-mail addresses: [email protected] (F. Zhang), [email protected] (L. Dehar- Dicranorchesella lacking scales on the ventral side of dens and other veng), [email protected] (M.I. Stevens), [email protected] (Y.-H. Huang), [email protected] (C.-D. Zhu). scaled genera having dental scales. Shape and surface sculpture of 1055-7903/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2013.09.024 232 F. Zhang et al. / Molecular Phylogenetics and Evolution 70 (2014) 231–239 scales are also various and have traditionally been used as an Entomobryomorpha, two Tomoceridae and two Isotomidae species important taxonomic character (Fig. 1). Scales are intuitively con- as outgroups. Thirty seven ingroup species were selected from sidered to have evolved from ordinary chaetae, but the shift from Entomobryidae, including 6, 4, 5, 6, 16 taxa respectively from chaeta to scale has never been examined in a phylogenetic context. Orchesellinae, Seirinae, Lepidocyrtinae, Willowsiini and Entomo- Molecular approaches have been applied to Collembola phyloge- bryini. Table 1 provides the information of taxa name, traditional nies for more than 15 years. Previous phylogenetic studies mainly taxonomical position prior to this study, collection locality and dealt with relationships of collembolan higher orders (Lee et al., Genbank accession numbers. All specimens were collected by aspi- 1995b; Frati et al., 1997; D’Haese, 2002; Park, 2002; Xiong et al., rator or Tullgren-Berlese funnels, stored in 99% ethanol at À20 °C, 2008; Porco and Deharveng, 2009), Entomobryomorpha (Park, and identified using Nikon SMZ1000 and Nikon E600 microscopes. 2009), Neelipleona (Schneider et al., 2011), Hypogastruridae (Lee Photos of scales were taken using a Hitachi scanning electron et al., 1995a; Greenslade et al., 2011), Neanuridae (Frati and microscope (SEM). Dell’Ampio, 2000; Dell’Ampio et al., 2002). However, none has examined the relationship between subfamilies and tribes within Entomobryidae. 2.2. DNA extraction and amplification To improve our current understanding of the relationships within the family, the present study reconstructs the phylogeny DNA was extracted using DNeasy Blood and Tissue Kit (Qiagen, of the main clades based on nuclear and mitochondrial genes. To Hilden, Germany) following the manufacturer’s standard protocols. explore the origin of body scales during evolution, we employed Primers, fragment length and references are shown in Table 2. ancestral character state reconstruction and mapped scale pres- Amplification of the four fragments (16SrRNA, 18SrRNA, 28SrRNA ence onto our molecular phylogeny. Implications of our results D1–3 and D7–10) were carried out using TC-5000 Thermal Cycler for the classification of Entomobryidae and for the taxonomic value (TECHNE) and performed in 50 ll volumes containing 2.5 units of of scales are discussed. Easy Taq polymerase, 5 lM of each dNTP, 3 mM MgCl2 (TransGen Biotech, Beijing, China), 2 ll of template DNA, 2 ll of each primer 2. Material and methods (10 mM) and 28.5 ll ddH2O. The PCR programs of 18SrRNA fol- lowed Giribet et al. (1996), 28SrRNA D1–3 followed D’Haese 2.1. Taxon sampling (2002) and Greenslade et al. (2011), 16SrRNA and 28SrRNA D7– 10 after Xiong et al. (2008). All PCR products were checked on a Taxa were chosen for this study with the aim of representing 1% agarose gel. Products were purified and sequenced by Majorbio the phylogenetic diversity of the whole family, following the clas- (Shanghai, China) on an ABI 3730XL DNA Analyser (Applied sification of Szeptycki (1979). We included members of Biosystems). Fig. 1. Body scales in Entomobryidae. (A) Heteromurus major; (B) Dicranocentrus wangi; (C) Lepidocyrtus fimetarius; (D) Willowsia japonica; (E) Sinhomidia bicolor; (F) Janetschekbrya himalica. Scale bar, 10 lm. F. Zhang et al. / Molecular Phylogenetics and Evolution 70 (2014) 231–239 233 Table 1 Sequenced terminals, collection locality, and Genbank accession numbers. Species with both terga and dens scaled are marked with two asterisks (ÃÃ). Scaled species but without dental scales are marked with an asterisk (Ã). Sinella longisensilla and Sinella triseta not formal published but the related manuscripts have been submitted or in press. Group Species name Locality 16S 18S 28S D1–3 28S D7–10 Tomoceridae Tomocerus ocreatusÃÃ China KC236221 KC236262 KC236303 KC236343 Tomocerus jilinensisÃÃ China – KC236261 KC236302 KC236342 Isotomidae Folsomia candida China KC236200 KC236239 KC236281 KC236320 Folsomia qudrioculata France KC236199 KC236240 KC236280 KC236320 Orchesellinae Ochesella cincta France KC236208 KC236250 KC236290 KC236331 Orchesellides sinensis China KC236209 KC236251 KC236293 KC236332 Orchesellides sp. China KC236217 KC236226 KC236267 KC236308 Heteromurus majorÃÃ France KC236201 KC236241 KC236282 KC236322 Heteromurus nitidusÃÃ France KC291493 KC236242 KC236283 KC236323 Dicranocentrus wangiÃÃ China KC236192 KC236232 KC236273 KC236313 Seirinae Seira delamareiÃÃ
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