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Dental Scales Could Occur in All Scaled Subfamilies of Entomobryidae

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Dental Scales Could Occur in All Scaled Subfamilies of Entomobryidae Dental scales could occur in all scaled subfamilies of Entomobryidae (Collembola): new definition of Entomobryinae with description of a new genus and three new species Author(s): Feng Zhang, Zhixiang Pan, Jun Wu, Yinhuan Ding, Daoyuan Yu and Beixin Wang Source: Invertebrate Systematics, 30(6):598-615. Published By: CSIRO Publishing URL: http://www.bioone.org/doi/full/10.1071/IS16005 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. CSIRO PUBLISHING Invertebrate Systematics, 2016, 30, 598–615 http://dx.doi.org/10.1071/IS16005 Dental scales could occur in all scaled subfamilies of Entomobryidae (Collembola): new definition of Entomobryinae with description of a new genus and three new species Feng Zhang A,E, Zhixiang Pan B, Jun Wu C, Yinhuan Ding A, Daoyuan Yu D and Beixin Wang A,F ADepartment of Entomology, College of Plant Protection, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, People’s Republic of China. BSchool of Life Sciences, Taizhou University, 1139 Shifu Road, Jiaojiang, Taizhou 318000, Zhejiang Province, People’s Republic of China. CNanjing Institute of Environmental Sciences under Ministry of Environmental Protection, 8 Jiangwangmiao Street, Nanjing 210042, People’s Republic of China. DSoil Ecology Lab, College of Resources and Environmental Sciences, Nanjing Agricultural University, 1 Weigang, Nanjing 210095, People’s Republic of China. EKey Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Beijing 100101, People’s Republic of China. FCorresponding author. Email: [email protected] and [email protected] Abstract. Body scales are fundamental in the classification of Entomobryidae at all taxonomical levels. Traditionally, scales on dens were considered to be absent in Entomobryinae, but present in other scaled subfamilies; however, this opinion was strongly challenged by recent morphological advances in tergal specialised chaetae (S-chaetae). A new genus, Lepidodens, is strikingly similar to the scaled Entomobryinae genus Willowsia in having pointed scales with relatively long ribs and 2, 2|1, 2, 2, 8, 3 tergal S-chaetae, but differs from it in having dental scales and a unique position of S-microchaetae on the first abdominal segment. Multilocus phylogeny and topology tests also support this view, the new genus clustering with Entomobryinae rather than Seirinae. Three new species, L. nigrofasciatus, L. similis and L. hainanicus, are described from South China. This study clearly undermines the traditional separation of Entomobryinae and Seirinae/Lepidocyrtinae, and demonstrates that dental scales could occur in all entomobryid subfamilies containing scaled taxa. In this new phylogenetic hypothesis, Entomobryinae has the greatest diversity in scale morphology and distribution among scaled collembolan groups, indicating multiple independent origins of scales. Additional keywords: Lepidodens, gen. nov., molecular phylogeny, Seirinae, South China, Willowsiini. Received 20 January 2016, accepted 27 April 2016, published online 13 December 2016 Introduction the family Entomobryidae has the largest diversity in both scaled Collembola (springtails), living in almost all kinds of terrestrial and unscaled groups. ecosystems, represents one of the largest radiations of soil Traditional classification of Entomobryidae was mainly organisms. Entomobryidae Tömösváry, 1882 with ~1800 contributed by Börner (1906, 1913), Yosii (1961), Szeptycki named living species accounts for ~20% of known collembolan (1979), Yoshii and Suhardjono (1989) and Soto-Adames et al. species (Bellinger et al. 1996–2016). Entomobryoidea distinctly (2008). The latter authors divided the family into Capbryinae, differs from other superfamilies and orders in a reduced prothorax, Orchesellinae and Entomobryinae (Entomobryini, Willowsiini, long appendages and elongated fourth abdominal segment. Seirini and Lepidocyrtini). Four taxa within Entomobryinae Relationships between Entomobryidae and other families sensu Soto-Adames et al. were often treated as subfamilies or within Entomobryoidea are still controversial. Closely related tribes by different authors. Zhang et al.(2014a) supported Paronellidae and Cyphoderidae are possibly ingroups of the monophyly of Entomobryinae sensu Szeptycki, Seirinae Entomobryidae based on molecular phylogeny and tergal and Lepidocyrtinae and the non-monophyly of Orchesellinae, specialised chaetae (S-chaetae) (Zhang et al. 2015). In any case, Entomobryini and Willowsiini based on ribosomal markers. Journal compilation Ó CSIRO 2016 www.publish.csiro.au/journals/is New definition of Entomobryinae and Lepidodens, gen. nov. Invertebrate Systematics 599 Integrating molecular and morphological evidence, Zhang and Materials and methods fi Deharveng (2015) revised the classi cation and erected the Taxa sampling framework of seven subfamilies. fi Distribution and morphology (shape and surface sculpture) of Following classi cation of Zhang and Deharveng (2015), 37 body scales are of great taxonomical values and are fundamental species were selected from Entomobryidae, representing the fi in the classification of Entomobryidae at all levels. Scales occur ve main subfamilies: Orchesellinae (3), Heteromurinae (4), in Heteromurinae, Entomobryinae, Seirinae and Lepidocyrtinae, Lepidocyrtinae (5), Seirinae (4) and Entomobryinae (21). among which only Entomobryinae includes both scaled and Tomocerus ocreatus (Tomoceridae), Folsomia candida and unscaled taxa. All traditional studies accepted the idea of the Folsomia quadriocula (Isotomidae) were chosen as outgroup absence of dental scales in Entomobryinae before molecular taxa. Species names, taxonomical positions, collection locality systematics were applied. Scaled taxa within Entomobryinae and GenBank accession numbers are provided in Appendix 1. All were grouped as Siraeformes by Denis (1941)andas materials were collected by aspirator or Tullgren-Berlese funnels, À Willowsiini by Yoshii and Suhardjono (1989). However, Zhang stored in 99% ethanol at 20 C and then morphologically and Deharveng (2015)nolongerseparatedEntomobryinaeinto examined using Nikon SMZ1000, Nikon 80i microscopes and unscaled Entomobryini and scaled Willowsiini in the light of a Hitachi scanning electron microscope. independent origins of body scales within the subfamily (Zhang et al. 2014a, 2014b, 2015), returning largely to Szeptycki’s(1979) DNA extraction and sequencing conception. They even transferred the Lepidosira-group sensu DNA was extracted using an Ezup Column Animal Genomic Yoshii & Suhardjono, 1989 with dental scales from Seirinae to DNA Purification Kit (Sangon Biotech, Shanghai, China) Entomobryinae based on the patterns of tergal bothriotricha following the manufacturer’s standard protocols. PCR and S-chaetae and the mucro structure. The absence/presence of amplification of the four fragments, mitochondrial COI and dental scales in Entomobryinae still appears disputable due to the 16SrRNA (16S) and nuclear 18SrRNA (18S) and 28SrRNA lack of comprehensive evidence from molecular phylogeny. D1–3 (28S), was carried out following Zhang et al.(2014a, Within Entomobryinae, scaled taxa except the Lepidosira- 2014d). All successful PCR products were purified and group, whose dental scales are absent (sensu Willowsiini), sequenced by GenScript (Nanjing, China) on an ABI 3730XL usually have scales mostly pointed with coarse ribs. The most DNA Analyzer (Applied Biosystems, Waltham, MA, USA). characteristic scale form is that of Willowsia, with long basal Sequences were assembled in Sequencher 4.5 (Gene Codes ribs on the surface (Fig. 1). A new genus and three new species Corporation, Ann Arbor, MI, USA), and were submitted to discovered in South China, which have pointed scales with GenBank (Appendix 1). Sequences were blasted in GenBank long basal ribs, remarkably resemble Willowsia species in and checked for possible errors. They were then preliminarily most features. However, the presence of scales on dens recalls aligned using MAFFT v7.149 by the Q-INS-I strategy (Katoh and rather Seirinae or Lepidocyrtinae, while other features point Standley 2013). Alignments were checked and corrected to Entomobryinae, to which we here assign the new genus. manually, with partially ambiguous sites of 16S excluded from To clarify the systematic position of the new genus and all analyses. In the final 4016-bp concatenated alignment, COI, improve the understanding of Entomobryinae, we conducted a 16S, 18S and 28S were 658 bp, 415 bp, 1681 bp and 1259 bp, molecular phylogeny and a detailed morphological comparison respectively. among the above taxa. As the second
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