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Ground Beetles (Coleoptera, Carabidae) of the World Inferred from a Phylogenetic Tree of Mitochondrial ND5 Gene Sequences

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Ground Beetles (Coleoptera, Carabidae) of the World Inferred from a Phylogenetic Tree of Mitochondrial ND5 Gene Sequences Genes Genet. Syst. (2003) 78, p. 53–70 Mode of morphological differentiation in the Latitarsi- ground beetles (Coleoptera, Carabidae) of the world inferred from a phylogenetic tree of mitochondrial ND5 gene sequences Zhi-Hui Su1*, Yûki Imura2, Hong-Zhang Zhou3, Munehiro Okamoto4 and Syozo Osawa1,† 1JT Biohistory Research Hall, 1-1 Murasaki-cho, Takatsuki, Osaka 569-1125, Japan 2Shinohara-cho 1249-8, Kohoku-ku, Yokohama 222-0026, Japan 3Institute of Zoology, Chinese Academy of Sciences, Haidian, Beijing 100080, China 4Department of Laboratory Animal Science, School of Veterinary Medicine, Faculty of Agriculture, Tottori University, Tottori 680-8553, Japan (Received 19 August 2002, accepted 22 January 2003) The Latitarsi is one large division of the subtribe Carabina (subfamily Carabi- nae, family Carabidae), and has been considered as a discrete morphological group consisting of 17 genera. The phylogenetic relationships and evolutionary pattern of the Latitarsi ground beetles have been investigated by analyzing mitochondrial NADH dehydrogenase subunit 5 (ND5) gene sequences. The phylogenetic tree suggests that the Latitarsi members do not form a single cluster, i.e., not mono- phyletic and at least 16 lineages belonging to the so-called Latitarsi emerged at about the same time of the Carabina radiation together with the members of other divisions. This suggests that these lineages (A, B, C, H, L, N, O, P, Q, R, S, T, U, V, W and X in Fig. 2a) may be treated each as a phylogenetically distinct division equivalent to other divisions. The group with bootstrap value of more than 80 percent has been considered as a single lineage (division) with two exceptions, V and X. The independency of each lineage has been assumed by the traditional morphology as well as a single clustering on the trees constructed by independent methods, unchanged topology by replacement of outgroups, etc. Generally speak- ing, the members in a single lineage are geographically linked. Many phyloge- netic lineages are composed of a single or only a few species without conspicuous morphological differentiation. In contrast to such a “silent morphological evolu- tion”, a remarkable morphological differentiation occasionally took place in several lineages. Key words: ground beetles, Latitarsi, mitochondrial ND5 gene, phylogeny, evo- lution, taxonomy include 168 species (Brˇezina, l999). The phylogenetic INTRODUCTION trees of the mitochondrial NADH dehydrogenase subunit The Latitarsi are one large taxonomic division of the 5 (ND5) gene sequences have been reported for some ground beetles in the subtribe Carabina, and are widely groups in this division, namely, the Oreocarabus complex distributed throughout the holarctic region and the north- (Imura et al., 1998a), Leptocarabus (Kim et al., 2000a, b) ern periphery of North Africa. Morphologically, they and Tomocarabus in the Japanese Islands (Su et al., have been classified into 17 genera (Imura, l996) which 2000). The representative genera in this division seem to have radiated within a relatively short time a little Edited by Naruya Saiou after or around the radiation of the Carabina 50–40 mil- * Corresponding author. E-mail: [email protected] lion years ago (MYA) as deduced from an ND5 phyloge- † Present address: 2-4-7-1003, Ushita-Asahi, Higashi-ku, netic tree. This division is most probably polyphyletic Hiroshima 732-0067, Japan. (Imura et al., 1998a; Su et al., 2001). This situation The nucleotide sequences data reported in this paper will appear in the DDBJ, EMBL, and GenBank nucleotide seems to make it difficult to estimate the meaningful phy- sequences databases with the accession numbers shown in logenetic positions of various Latitarsi groups. Table 1. In the present study, the NJ-, the UPGMA and the MP- 54 Z.-H. SU et al. phylogenetic trees of the ND5 gene have been constructed MATERIALS AND METHODS for 165 specimens consisting of 77 species of the Latitarsi including 38 species used in the previous papers (Imura The specimens analysed for the ND5 gene sequences in et al., 1998a, b; Su et al., 2001). The overall phylogeny this study are listed in Table l, and the localities where and evolutionary pattern of the Latitarsi ground beetles the samples were collected are shown in Fig. 1. The sci- have been discussed. entific names used by Imura & Mizusawa (1996) and Table 1. List of the specimens used in this study Specimen DDBJ/EMBL/GenBank No.* Scientific name Locality Accession no. Reference A- 1 Autocarabus auratus auratus France: Bourgogne D86204 Su et al. 1996b 2 Au. cancellatus graniger Romania: Judet Caras-Severin, Teregova env. AB092699 This paper 3 Au. cancellatus graniger Romania: Judet Caras-Severin, Baile Herculane, Topenia Val. AB092700 ” 4 Au. cancellatus tuberculatus Russia: Leningrad Distr., Liebiazhie AB092701 ” 5 Au. cancellatus emarginatus Italy: Piemonte, Vercelli, Crevacuore, near Guardabosone (600 m) AB092702 ” 6 Au. cancellatus carinatus France: Jura AB092703 ” 7 Au. cancellatus carinatus France: Jura AB092704 ” B- 1 Mesocarabus problematicus planiusculus France: Bourgogne D86210 Su et al. 1996b 2 Me. problematicus harcyniae Germany: Niedersachsen, Lamspringe, Hildesheim AB050680 Su et al. 2001 C- 1 Orinocarabus putzeysianus germanae Italy: Piemonte, Cuneo, V. Tanaro, Viozene, Mt. Saccarello (2200 AB017453 Imura et al. m) 1998a 2 Or. putzeysianus omensis Italy: Piemonte, Cuneo, Castelmagno, Col del Mulo (2300 m) AB017454 ” D- 1 Megodontus kolbei aino Japan: Hokkaido, Kamikawa D50365 Su et al. 1996a 2 Aristocarabus viridifossulatus rizeanus China: Sichuan, Jiuzhaigou Xian, Jiuzhaigou, Rizegou (3100 m) AB050677 Su et al. 2001 3 Shenocoptolabrus osawai micangshanus China: Sichuan, Nanjiang, Micang Shan Mts., Daba (1350 m) AB050681 ” E- 1 Gnathocarabus kuznetzovi kuznetzovi Iran: Mazandaran, Gombad-e Kavus, Karim Ishan AB047253 Imura et al. 2000a 2 Archicarabus monticola monticola Italy: Piemonte, Cúneo, Brondello AB047259 ” 3 Ar. nemoralis nemoralis USA: Washington Srat., Snohomish, W. Index AB047262 ” F- 1 Cyclocarabus karaterekensis hemicallis- Kirgiz: SE. of Tshandalash Mts., Tshakmak-Suu Riv. (3100–3400 AB053499 Su et al. 2002 thenes m) 2 Morphocarabus sibiricus haeres Russia: Belgorod, near Borisovka steppe AB053520 ” 3 Mo. venustus liaoningensis China: Liaoning, Dandong, Mt. Shifang Ding AB050678 Su et al. 2001 G- 1 Isiocarabus miaorum miaorum China: Guangxi, Xingían, Mt. Miaoíer Shan AB041053 Tominaga et al. 2000 2 Carabus (s. str.) vanvolxemi vanvolxemi Japan: Aomori, Mutsu, Mt. Osore-zan AB041062 ” H- 1 Cavazzutiocarabus latreilleanus latreil- Italy: V. díAosta, Champorcher (2400 m) AB017478 Imura et al. leanus 1998a I- 1 Limnocarabus clathratus clathratus Germany: W. Niedersachsen, Dalums Moor near Lingen AB031507 Kim et al. 1999a 2 Li. maacki aquatilis Japan: Aomori, Nakasato D50358 Su et al. 1996a 3 Euleptocarabus porrecticollis porrecticol- Japan: Gifu, Nakatsugawa AB022564 Kim et al. lis 1999b J- 1 Hemicarabus tuberculosus tuberculosus Japan: Fukushima, Shirasaka D50353 Su et al. 1996a 2 Homoeocarabus maeander paludis Japan: Hokkaido, Sarobetsu D50354 Su et al. 1996a K- 1 Apotomopterus sauteri yunkaicus China: Guangxi, Mt. Miao’er Shan AB031490 Kim et al. 1999a 2 Ap. tonkinensis tonkinensis Vietnam: Lao Cai Prov., Deo Tram Ton AB031494 ” 3 Ap. iris iris China: Sichuan, Daliang Shan Mts., Meigu~Leibo AB031504 ” L- 1 Autocarabus cristoforii cristoforii France: Vicdesos, Ariège prov. AB092705 This paper M- 1 Chaetocarabus intricatus intricatus France: Bourgogne D86208 Su et al. 1996b 2 Heterocarabus marietti ornatus Turkey: W. Giresun AB047196 Imura et al. 2000b 3 Platycarabus depressus depressus Italy: Piemonte, Varallo, Val Sesia AB047198 ” N- 1 Eurycarabus famini fezzanus Morocco: Michlifen (1800 m) AB092706 This paper Phylogeny of Latitarsi ground beetles 55 continued O- 1 Nesaeocarabus abbreviatus abbreviatus Spain: Is. Tenerife, El Bueno, Arico (900 m) AB092707 ” 2 Ne. abbreviatus abbreviatus Spain: Is. Tenerife, Siete Fuentes (1500 m) AB092708 ” P- 1 Cytilocarabus cribratus cribratus Turkey: Yusufeli, Artvin AB017460 Imura et al. 1998a 2 Cy. cribratus cribratus Turkey: Coruh, Karcal Dagi AB092709 This paper 3 Cy. cribratus ispirensis Turkey: Col d’Ovit, Dag (2500 m) AB092710 ” 4 Cy. porrectangulus porrectangulus Turkey: Yayladere, Kostandag, Yagmurdere (1900 m) AB017462 Imura et al. 1998a 5 Cy. cribratus pulumuricus Turkey: Mercon M.R.-S. Erzincan, Mt. Akbaba (2900 m) AB092711 This paper 6 Cy. porrectangulus porrectangulus Turkey: W. Giresun Mt. R. W. Erico Tepesi (1200 m) AB092712 ” 7 Cy. porrectangulus porrectangulus Turkey: Giresun Mt. R. Karagol Ridge (2500 m) AB092713 ” 8 Cy. cribratus cribratus Russia: Caucasus, Osetia, Mt. Khumaratkhok (2300 m) AB017461 Imura et al. 1998a 9 Cy. porrectangulus porrectangulus Turkey: W. Giresun Mts., Gonderic Tepesi (2000 m) AB092714 This paper 10 Cy. gemellatus gemellatus Iran: Tehrun, Gach-i-sar (2700 m) AB092715 ” Q- 1 Tomocarabus harmandi harmandi Japan: Tochigi, Nasu AB039810 Su et al. 2000 2 To. harmandi mizunumai Japan: Toyama, Arimine AB039813 ” R- 1 Pachycarabus koenigi koenigi Russia: Caucasus, Aibga Mts. (2400 m) AB092716 This paper 2 Pachyc. staehlini staehlini Russia: Caucasus, Osetia, Bokovoy Mts., AB092717 ” Sources of Riv. Liadon, Mt. Tepli (2700–3000 m) 3 & Pachyc. roseri ciftekopruleriensis Turkey: SE. slope of Mt. Karcal Dag (2500 m) AB092718 ” 4 S- 1 Euporocarabus hortensis hortensis Austria: Tirol, Innsbruck, Alpen Zoo AB017463 Imura et al. 1998a 2 Pachystus cavernosus variolatus Italy: Abruzzi, Gran
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