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Molecular Phylogeny of the Higher Taxa of Odonata (Insecta) Inferred from COI, 16S Rrna, 28S Rrna, and EF1 Sequences

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Molecular Phylogeny of the Higher Taxa of Odonata (Insecta) Inferred from COI, 16S Rrna, 28S Rrna, and EF1 Sequences bs_bs_banner Entomological Research 44 (2014) 65–79 RESEARCH PAPER Molecular phylogeny of the higher taxa of Odonata (Insecta) inferred from COI, 16S rRNA, 28S rRNA, and EF1-α sequences Min Jee KIM1, Kwang Soo JUNG2, Nam Sook PARK3, Xinlong WAN1,4, Ki-Gyoung KIM5, Jumin JUN6, Tae Joong YOON7, Yeon Jae BAE7, Sang Mong LEE3 and Iksoo KIM1 1 Department of Applied Biology, College of Agriculture & Life Sciences, Chonnam National University, Gwangju, Korea 2 College of Natural Sciences, Andong National University, Andong, Korea 3 College of Natural Resources & Life Science, Pusan National University, Pusan, Korea 4 Institute of Health and Environmental Ecology, Wenzhou Medical College, Wenzhou City, Zhejiang, China 5 Biological Resources Research Department, National Institute of Biological Resources, Incheon, Korea 6 Wildlife Genetic Resources Center, National Institute of Biological Resources, Incheon, Korea 7 Environmental Science and Ecological Engineering, College of Life Sciences and Biotechnology, Korea University, Seoul, Korea Correspondence Abstract Iksoo Kim, Department of Applied Biology, College of Agriculture & Life Sciences, In this study, we sequenced both two mitochondrial genes (COI and 16S rRNA) Chonnam National University, Gwangju and nuclear genes (28S rRNA and elongation factor-1α) from 71 species of 500-757, Korea. Odonata that represent 7 superfamilies in 3 suborders. Phylogenetic testing for Email: [email protected] each two concatenated gene sequences based on function (ribosomal vs protein- coding genes) and origin (mitochondrial vs nuclear genes) proved limited resolu- Received 6 September 2013; tion. Thus, four concatenated sequences were utilized to test the previous accepted 6 March 2014. phylogenetic hypotheses of higher taxa of Odonata via Bayesian inference (BI) and doi: 10.1111/1748-5967.12051 maximum likelihood (ML) algorithms, along with the data partition by the BI method. As a result, three slightly different topologies were obtained, but the BI tree without partition was slightly better supported by the topological test. This topology supported the suborders Anisoptera and Zygoptera each being a monophyly, and the close relationship of Anisozygoptera to Anisoptera. All the families represented by multiple taxa in both Anisoptera and Zygoptera were consistently revealed to each be a monophyly with the highest nodal support. Unlike consistent and robust familial relationships in Zygoptera those of Anisoptera were partially unresolved, presenting the following relationships: ((((Libellulidae + Corduliidae) + Macromiidae) + Gomphidae + Aeshnidae) + Anisozygoptera) + (((Coenagrionidae + Platycnemdidae) + Calopterygidae) + Lestidae). The subfamily Sympetrinae, represented by three genera in the anisopteran family Libellulidae, was not monophyletic, dividing Crocothemis and Deielia in one group together with other subfamilies and Sympetrum in another independent group. Key word: COI, elongation factor-1α, Odonata phylogeny, 16S rRNA, 28S rRNA. is characterized by a broader hindwing, possession of the Introduction crossvein that divides the discoidal cell into a triangle and The insect order Odonata contains approximately 5500 super triangle in both wings, and outstretched wings when at species and is divided into three suborders: Anisoptera, rest, whereas Zygoptera is characterized by a hindwing Zygoptera, and Anisozygoptera (Tofilski 2004). Anisoptera essentially similar to the forewing, wings parallel to the © 2014 The Entomological Society of Korea and Wiley Publishing Asia Pty Ltd M. J. Kim et al. body when at rest, and widely separated eyes (Needham 16S and 28S rRNAs from 32 species belonging to 1903; Tillyard 1923, 1928). The third suborder Anisoptera, Anisozygoptera, and Zygoptera (Fig. 1H). Both Anisozygoptera is composed of two living species, found in of these studies, that included limited taxonomic diversity, Japan and in the Himalayas, respectively. Although the have shown paraphyly of Zygoptera, placing the damselfly Anisozygoptera is morphologically intermediate between family Lestidae, belonging to Lestoidea, as the sister to Anisoptera and Zygoptera in adult body and wings, this either the monophyletic Anisoptera (Fig. 1G) or the suborder is often grouped together with Anisoptera, under monophyletic Anisoptera + Anisozygoptera (Fig. 1H). Sub- the name Epiprocta (Bechly 1996; Lohmann 1996; Trueman sequent further extensive work was performed by Fleck 1996; Rehn 2003; Hasegawa & Kasuya 2006). et al. (2008) based on the 2026 aligned positions from 16S Along with the phylogenetic position of Anisozygoptera rRNA, tRNAVal, and 12S rRNA. With the inclusion of 121 there have been many studies that have attempted to resolve species in 12 families and five superfamilies for Anisoptera, the relationships within the Odonata, but conflicting rela- one species for Anisozygoptera, and 17 species in seven tionships still exist. One of the unresolved relationships families and four superfamilies for Zygoptera, this study includes each monophyly of Anisoptera and Zygoptera. The also supports paraphyly of Zygoptera, associating the dam- monophyly of Anisoptera has been proposed by wing vena- selfly family Lestidae to the monophyletic Anisoptera + tion (Fraser 1957; Fig. 1A), flight apparatus and copulatory Anisozygoptera (Fig. 1I). On the other hand, molecular data structures (Pfau 1991; Fig. 1B), and also from wing venation by Dumont et al. (2010) and combined data of morphologi- with the cladistic parsimony method (Trueman 1996; cal, molecular, and fossil record by Bybee et al. (2008) have Fig. 1C), whereas the non-monophyly of Zygoptera was shown monophyletic Zygoptera (Figs 1J–L). proposed in these studies (Figs 1A–C). On the other hand, Among the anisopteran families the Libellulidae is the the monophyly of both suborders have been supported by largest group that is distributed world-wide containing other several studies (Carle 1982; Bechly 1996; Rehn 2003; ∼1000 species in 11–13 subfamilies, with one of the sub- Figs 1D–F). families, Sympetrinae, containing ∼200 species in 22 genera Monophylies of several superfamilies have also been (Tillyard 1917; Fraser 1957; Bridges 1994; Steinmann 1997; ambiguous among morphological studies, providing conflict Pilgrim & Von Dohlen 2008). The monophyly of and unresolved relationships. For example, Fraser (1957) Sympetrinae has been supported by morphological studies. supported monophylies of superfamilies for a limited For example, Fraser (1957) classified this subfamily based group such as the Libelluloidea for Anisoptera and the on four synapomorphic characters such as non-extended last Coenagrionoidea and the Calopterygoidea for Zygoptera. antenodal crossvein (ACV) of the forewings beyond the Pfau (1991) supported monophylies for the Coenagrionoidea subcosta, placement of the arculus between the first and and Calopterygoidea, and Libelluloidea. Trueman (1996) second ACV, conspicuous radial and medial planates, and supported monophyly only for Libelluloidea, Carle (1982) broad hindwing base with a highly visible anal loop. for Coenagrionoidea and Libelluloidea, Bechly (1996) for However, these characters are shared with other subfamilies, Calopterygoidea, Coenagrionoidea, and Libelluloidea, and lacking synapomorphy for the subfamily Sympetrinae (Ware Rehn (2003) only for Libelluloidea. Due to the lack of et al. 2007; Pilgrim & Von Dohlen 2008). monophylies in most superfamilies, familial relationships In order to expand our understanding for odonate phylog- are also mostly unresolved and inconsistent among studies. eny and enrich molecular markers, in this study we sequenced Nevertheless, the sister relationship of Corduliidae and a total of ∼3.8 kb consisting of mitochondrial COI (1147 bp), Libellulidae within Libelluloidea was concordantly found mitochondrial 16S rRNAincluding tRNALeu (UUR) and tRNAVal in Trueman (1996), Bechly (1996), and Rehn (2003) (1368–1374 bp), nuclear 28S rRNA (830–842 bp), and (Figs 1C,E,F). Among superfamilial relationships in nuclear elongation factor-1α (EF-1α) (541 bp). These Anisoptera, eitherAeshnoidea (Figs 1A,B,E) or Gomphoidea sequences were utilized to infer evolutionary patterns of each (Figs 1C,F) has been placed as the most basal lineage. Other gene, and to test the previous phylogenetic hypotheses of superfamilial relationships are mostly obscured by non- Odonata. monophyletic superfamilies in Anisoptera. Molecular phylogenetic studies within Odonata provided Materials and methods somewhat more consistent relationships regarding higher taxonomic relationships among studies, but still relation- Taxon sampling ships within several taxonomic levels are neither well resolved nor consistent (Figs 1G–L). Saux et al. (2003) The 71 odonate species included in this study (Table S1) is sequenced a partial 12S ribosomal RNA (rRNA) from 26 composed of 3 of the 3 suborders, 7 of the 8 superfamilies, species belonging to Anisoptera and Zygoptera (Fig. 1G). and 10 of the 28 families in world-wide odonate diversity Also, Hasegawa and Kasuya (2006) sequenced both a partial (Bridges 1994; Rehn 2003). At least one family was 66 Entomological Research 44 (2014) 65–79 © 2014 The Entomological Society of Korea and Wiley Publishing Asia Pty Ltd © 2014 The Entomological SocietyEntomological of Research Korea and Wiley Publishing Asia Pty Ltd A Fraser (1957) B Pfau (1991) C Trueman (1996) Lestidae Lestoidea (Z) Coengrionidae Coengrionoidea (Z) Lestidae Lestoidea (Z) Calopterygidae Calopterygoidea (Z) Lestidae Lestoidea (Z) Coengrionidae
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