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(Moniligastridae, Clitellata) in the Russian Far East: Sequence Data of Two Mitochondrial Genes

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(Moniligastridae, Clitellata) in the Russian Far East: Sequence Data of Two Mitochondrial Genes European Journal of Soil Biology 86 (2018) 1–7 Contents lists available at ScienceDirect European Journal of Soil Biology journal homepage: www.elsevier.com/locate/ejsobi Molecular differentiation of epigeic and anceic forms of Drawida ghilarovi T Gates, 1969 (Moniligastridae, Clitellata) in the Russian Far East: Sequence data of two mitochondrial genes ∗ Gennady N. Ganina, Dmitry M. Atopkinb,c, a Institute Water and Ecology Problems, Far Eastern Branch of Russian Academy of Sciences, 680000, Khabarovsk, Russia b Department of Cell Biology and Genetics, Far Eastern Federal University, 690051, Vladivostok, Russia c Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of Russian Academy of Sciences, 690022, Vladivostok, Russia ARTICLE INFO ABSTRACT Handling editor: Thibaud Decaens Mitochondrial cytochrome oxidase subunit I (COI) and 16S rRNA gene sequence data were analysed for 43 – Keywords: specimens of Drawida ghilarovi earthworms of a tropical genus on the northern boundary of their natural Drawida habitat, including two ecological forms and three colour morphs collected from different regions of the southern Clitellata Russian Far East. Intraspecific genetic differentiation of these clitellata was analysed with different criteria that Mitochondrial DNA characterise different forms and morphs. A sample of anecic worms was shown to possess higher genetic var- Earthworm iation than a sample of epigeic worms. Haplotype network reconstructions showed that the meadow-swamp Russian Far East epigeic black-coloured D. ghilarovi is more highly diverged from the anecic forest grey- and brown-coloured worms than the grey and brown colour morphs are from each other. Genetic differentiation between three colour morphs ranged from 9.89 ± 0.58 to 11 ± 0.59% using COI and 16S data. An AMOVA test and an exact test showed a high probability of non-differentiation between grey and brown earthworms. A multimodal mismatch distribution was revealed for the whole D. ghilarovi sample and for each colour morph. The minimum spanning tree showed that the differentiation of specimens is associated with ecological and geographical criteria. Molecular data for Drawida showed high genetic differentiation between epigeic and anecic using COI and 16S gene sequence data as well as the various phylogenetic relationships among the studied forms. The anecic earthworms possibly represent different genetic lineages of the D. ghilarovi species complex. The epigeic Drawida, based on the complex data, can be considered a new species of this genus. 1. Introduction tertiary fauna where they did not experience effects of the last glacia- tion events. Tropical earthworms of the genus Drawida (Moniligas- Earthworms constitute up to 90% of the soil invertebrate biomass tridae) inhabit these territories on the northern boundary of their nat- and are important ecosystem engineers [1]. Earthworms comprise ap- ural habitat. This fact has attracted the attention of researchers. proximately 4000–6000 described species, but this number probably Studying of the Drawida earthworms with respect to possible factors of only represents half of the actual worldwide diversity of the group origin and coexistence of closely related species on their areal border, [2,3]. In many cases, morphological identification of earthworm species along with the phylogeography and the evolution, is very important. is impeded by the lack of stable and easily observable morphological Representatives of the Moniligastridae family presumably invaded characters and a high level of phenotypic variability. There are 60 Southeast Asia after the collision of the Indian and Asian geological earthworm species that nominally inhabit Russian territory. Most of plateau during the Tertiary period, i.e. about 70 million years ago [5,6]. them belong to the family Lumbricidae [4]. Only on the southern “Drawida areal is from Primorsky Krai of Russia, China, Korea, Japan boundary of the Russian Far East in the Primorsky and Priamursky across Malaysia and East Asia to the Hindustan southern tip (if not to Regions (42°30’–49°30′ of northern latitude and 130°37’–137°03′ of Ceylon) and is wider than that of any other genus of earthworm” [[7], eastern longitude) are there another three megadrilid families, one of p. 676]. In the Northeast China provinces, closest to Russia, Drawida are which are representatives of Moniligastridae, and are widely dis- represented by 6 species [8], with 22 total species in China, 21 species tributed in Southeastern Asia. These regions are refuge territories for on the Korean peninsula, and 8 species in Japan [9]. ∗ Corresponding author. Department of Cell Biology and Genetics, Far Eastern Federal University, 690051, Vladivostok, Russia. E-mail address: [email protected] (D.M. Atopkin). https://doi.org/10.1016/j.ejsobi.2018.02.004 Received 10 March 2017; Received in revised form 29 January 2018; Accepted 18 February 2018 1164-5563/ © 2018 Elsevier Masson SAS. All rights reserved. G.N. Ganin, D.M. Atopkin European Journal of Soil Biology 86 (2018) 1–7 Table 1 List of taxa Drawida ghilarovi species-complex, incorporated into analysis. № Species (morph/form) n Location (Abb.) Acc. Number COI 16S 1 D. ghilarovi (black/epigeic) 3 Wetland, Nanaian region, Khabarovsk Territory (Nch) HG970197–HG970199 HG970212–HG970214 49°27′N, 136°46′E 2 D. ghilarovi (black/epigeic) 1 Wetland, Anyui Park, Kahabarovsk Territory (Ach) HG970203 HG970218 49°20′N, 137°03′E 3 D. ghilarovi (black/epigeic) 3 Wetland, Bastak Researve, Jewish Autonomous Region (Bch) HG970191–HG970193 HG970206–HG970208 48°59′N, 135°03′E 4 D. ghilarovi (black/epigeic) 3 Wetland, Chirki River, Khabarovsk Territory (Chch) HG970194-HG970196 HG970209-HG970211 48°09′N, 135°08′E 5 D. ghilarovi (black/epigeic) 3 Wetland, Razdol'naja River, Primorye Territory (Pch) HG970200–HG970202 HG970215–HG970217 43°33′N, 131°54′E 6 D. ghilarovi (black/epigeic) 1 Wetland, Like Khanka Reserv. Primorye Territory (KhCh) KY711475 KY711474 44°38′N, 132°49′E 7 D. ghilarovi (black/epigeic) 2 Wetland, v. Stolbowoe, Jewish Autonomous Region (Sch) KY711476–KY711477 KY711446–KY711447 47°54′N, 131°06 ′E 8 D. ghilarovi (grey/anecic) 1 Forest cedar-broad-leaved, Ussurijskij Researve, Primorye Territory (Uz) HG970205 HG970220 43°33′N, 132°21′E 9 D. ghilarovi (grey/anecic) 3 Forest cedar-broad-leaved, Shivki Mountain, Kahabarovsk Territory, Southern KY711499–KY711501 KY711468–KY711468 Sikhote-Alin (ShS) 47°00′N, 134°22′E 10 D. ghilarovi (grey/anecic) 1 Forest dark coniferous, Sikhote-Alin Reserv. Primorye Territory (Ss) KY711493 KY711459 44°59′N, 136°31′E 11 D. ghilarovi (grey/anecic) 2 Forest cedar-broad-leaved, Sikhote-Alin Reserv. Primorye Territory (Ssk) KY711494–KY711495 KY711462–KY711463 45°13′N, 136°29′E 12 D. ghilarovi (grey/anecic) 3 Forest cedar-broad-leaved, Biological Station “Gornotayozhnaya”, Primorye KY711482–KY711484 KY711450–KY711452 Territory (Gs) 43°41′N, 132°09′E 13 D. ghilarovi (grey/anecic) 1 Forest fir-broad-leaved, Kedrovaja Pad’ Researve, Primorye Territory (Ps) HG970204 HG970219 42°26′N, 130°37′E 14 D. ghilarovi (brown/anecic) 3 Forest cedar-broad-leaved, Shivki Mountain, Southern Sikhote-Alin (ShK) KY711496–KY711498 KY711465–KY711465 47°00′N, 134°22′E 15 D. ghilarovi (brown/anecic) 2 Forest cedar-broad-leaved, Sikhote-Alin Reserve, Primorye Territory (Sk) KY711491–KY711492 KY711460–KY711461 45°13′N, 136°29′E 16 D. ghilarovi (brown/anecic) 3 Forest cedar-broad-leaved, Lazovsky Reserve, Primorye Territory (Lk) KY711485–KY711487 KY711453–KY711455 43°00′N, 133°44′E 17 D. ghilarovi (brown/anecic) 2 Forest cedar-broad-leaved, Biological Station “Gornotayozhnaya”, Primorye KY711479–KY711480 KY711448–KY711449 Territory (Gk) 43°41′N, 132°09′E 18 D. ghilarovi (brown short/anecic) 3 Forest cedar-broad-leaved, Marine Biological Station “Vostok”, Primorye Territory KY711512–KY711514 KY711439–KY711441 (Vkk) 42°56′N, 132°42′E 19 D. ghilarovi (brown elongate/ 1 Forest cedar-broad-leaved, Marine Biological Station “Vostok”, Primorye Territory KY711509 KY711438 anecic) (Vkd) 42°53′N, 132°44′E 20 D. ghilarovi (brown short/anecic) 1 Forest dark coniferous, Lazovsky Ridge, Primorye Territory (Lkk) KY711508 KY711442 43°30′N, 133°35′E 21 D. ghilarovi (brown elongate/ 1 Forest dark coniferous, Lazovsky Ridge, Primorye Territory (Lkd) KY711507 KY711443 anecic) 43°30′N, 133°35′E 22 D. bullata 1 Kumar et al., 2011 JN887894 No data 23 D. gracilis 2 Kumar et al., 2011 JN887887–JN887888 JN887899–JN887900 24 D. hattamimizu 2 Minamiya et al., 2010 AB543206, AB543227 No data 25 D. j. japonica 4 Chang et al., 2009 EF077597-EF077600 No data The possible presence of several species of this genus in the Russian endogeic, anecic and epigeic [15]. Anecic worms migrate vertically Primorje was mentioned in the mid-1970s [10], but only one species of from the capsule upwards towards the decomposed leaf litter. These this Indo-Malayan genus is still known from Russia [11]. Drawida ghi- worms are better adapted to the soil temperature extremes, but their larovi Gates, 1969 is an endemic species of the south of the Russian Far natural habitat is limited by soil drainage [16]. Epigeic worms live on East that is included in the Red Book of Russia and the Khabarovsk the soil surface or under leaf litter and selectively feed on fallen phy- Territory [12]. The earthworm specimens were first found in the Ke- tomass or rootlets within the humus. Epigeic species are hydrophilic drovaja Pad’ and Ussurijskiy forest reserves in the Primorje Territory, and better adapted to flooding [16]. Anecic and epigeic species are and were later described by Gates (1969) as a new species [7]. Later considered as earthworms that are ecologically replacing each other several colour morphs were found among different specimens of D. because of the great differences in extreme dampness conditions [15]. ghilarovi, which were dependent on their environments. Our research Anecic species are able to inhabit the subtropical climatic environments has registered three colour morphs (black, brown, grey) but only two (in our case, up to 47°northern latitude (NL)), and the epigeic species ecological forms (epigeic and anecic) of Drawida ghilarovi [13,14].
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