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Phylogeny of Cave-Dwelling Atyid Shrimp Troglocaris in the Dinaric Karst Based on Sequences of Three Mitochondrial Genes

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Phylogeny of Cave-Dwelling Atyid Shrimp Troglocaris in the Dinaric Karst Based on Sequences of Three Mitochondrial Genes PERIODICUM BIOLOGORUM UDC 57:61 VOL. 112, No 2, 159–166, 2010 CODEN PDBIAD ISSN 0031-5362 Original scientific paper Phylogeny of cave-dwelling atyid shrimp Troglocaris in the Dinaric Karst based on sequences of three mitochondrial genes Abstract DAMJAN FRANJEVI] MIRJANA KALAFATI] Background and Purpose: The main purposes of this study was to revise MLADEN KEROVEC the current taxonomy of the genus Troglocaris in the Dinarids in the light of SANJA GOTTSTEIN molecular phylogenetic results from three major areas of disjunct distribu- Division of Biology, Faculty of Science tion (Southern France, West Dinarids, and West Caucasus), and addition- University of Zagreb ally to test the subfamily relationships between Paratyinae and Typhlatyinae Rooseveltov trg 6, 10 000 Zagreb, Croatia in the Dinarids. Correspondence: Materials and Methods: This study was performed on populations of Sanja Gottstein the cave-dwelling shrimp Troglocarisfrom three disjunct areas of distribu- Faculty of Science tion: Southern France, Dinaric Karst and Western Caucasus using mito- Division of Biology chondrial genes for 16S rRNA, cytochrome oxidase I and cytochrome Rooseveltov trg 6 oxidase II subunits. Wecombined mitochondrial data from shrimp popula- 10 000 Zagreb, Croatia Email: [email protected] tions to clarify the evolutionary relationship inside (within) the genus Troglocaris. Key words: Typhlatyinae, Paratyinae, Results: Our results, based on phylogenetic analysis of three mitochon- Dinaric karst, speciation, mitochondrial genes, Paratethys, Miocene drial genes from 14 populations of the closely related atyid taxa, do not sup- port the monophyly of the genus Troglocaris. Moreover, new insights were introduced in the Atyidae subfamily status. At subfamily level, a difference in current taxonomy was observed which excluded the genus Spelaeocaris from Typhlatyinae and placed it inside Paratyinae. Additionally the closest relative to the French species Troglocaris inermis appears to be the sur- face-dwelling shrimp Atyaephyra desmaresti. Conclusions: The separation of the oldest Western Troglocaris lineage from the Dinaro-Caucasian lineages is estimated to have occurred in the Late Miocene. Also DNA sequence data suggest that Troglocaris herce- govinensis from South Herzegovina and Troglocaris kutaissiana complex from Western Caucasus are sister species. INTRODUCTION he genus Troglocaris is the most widespread cave-dwelling deca- Tpod in Europe with a disjunct range extended to West Caucasus. In the Dinaric Karst, its distribution encompasses a number of major drainage basins and biogeographical regions characterized by the pres- ence of Troglocaris main predator, the European cave salamander Pro- teus anguinus anguinus Laurenti, 1768 (1). Originally, four species were Received January 30, 2009. described (2, 3): Troglocaris anophthalmus (Kollar 1848), T. hercegovi- nensis (Babi} 1922), T. inermis Fage, 1937, and T. kutaissiana (Sadovsky D. Franjevi} et al. Phylogeny and evolution of Troglocaris 1930). The nominal species T. anophthalmus from the The main purpose of this study was to revise the cur- Dinaric Karst was later treated as three distinct subspe- rent taxonomy of the genus Troglocaris in the Dinarids in cies (T. anophthalmus anophthalmus (Kollar 1848), T. ano- the light of molecular phylogenetic results from three phthalmus intermedia Babi}, 1922, and T. anophthalmus major areas of disjunct distribution (Southern France, planinensis Birstein, 1948) while T. kutaissiana from the West Dinarids, and West Caucasus), and additionally to West Transcaucasus was listed as five distinct subspecies test the subfamily relationships between Paratyinae and (T. kutaissiana kutaissiana, T. kutaissiana ablaskiri Bir- Typhlatyinae in the Dinarids. To gain such results a stein, 1939, T. kutaissiana fagei Birstein, 1939, T. kutai- comprehensive molecular phylogenetic analysis, using ssiana jusbaschjani Birstein, 1948, T. kutaissiana osterloffi different methods of phylogenetic inference, was applied Jusbaschjan, 1940) (2). Mugue et al. (4) have added an on parts of three mitochondrial genes (16S rRNA, cyto- additional species for West Transcaucasus, Troglocaris chrome oxidase I and cytochrome oxidase II). birsteini. Their short summary contains no information of diagnostic value, and we thus consider the species as nomen nudum. T.hercegovinensis was originally described MATERIALS AND METHODS as Troglocaridella hercegovinensis by Babi} (5) who origi- Taxon sampling nally created that separate genus. Our sampling includes one or more individuals of The remarkable discovery of a cave dwelling atyid each of the nominate taxa [Troglocaris anophthalmus (Ko- shrimp was the monotypic Spelaeocaris pretneri Matja{i~ llar 1848), T. inermis Fage 1937, T. intermedia Babi}, 1956 from south-eastern Herzegovina, which was later 1922, T. kutaissiana (Sadovsky 1930), T. planinensis (Bir- transferred to the genus Typhlatya by Sanz and Platvoet {tejn 1950)], originating from different localities throu- (6). On the basis of all the data mentioned above it is ob- ghout their area of distribution (Figure 1). A total of 12 vious that the current status of species inside Troglocaris Troglocaris populations were analyzed from 11 localities genera is not satisfactorily resolved. (Table 1). We chose two additional sister taxa, a cave- Allozyme studies on the diversity of Troglocaris popu- -dwelling shrimp Spelaeocaris, currently member of Ty- lations from Italy suggest that allopatric speciation was phlatyinae (2, 3) and an epigean freshwater shrimp At- followed by secondary sympatric speciation which has yaephyra desmaresti (Millet 1848), currently a member of promoted the high genetic diversity of the nominal spe- Paratyinae (2, 3) to verify relationships between Para- cies in the Western Dinaric Karst (7). tyinae and Typhlatyinae. To root our phylogenetic trees two additional taxa were chosen as outgroups in analy- In a recent phylogenetic study Zak{ek et al. (8) sho- ses: epigean decapod Astacus astacus (Linnaeus 1758) wed that the currently recognized taxonomic diversity of and epigean amphipod Gammarus balcanicus (Schäferna Troglocaris, which was predicted by Sket (1) as the most 1922). species-rich cave-dwelling shrimp, is probably lower than the number of distinct lineages on the molecular The specimens were preserved in 96% ethanol and phylogenetic tree. After all previous studies the current stored at –20°C until extraction of DNA. From the ma- status and the patterns of speciation of the genus Tr o - jority of samples all three genes were analyzed. However, glocaris and Spelaeocaris remain to be completely eluci- some samples failed to amplify for all three genes, possi- dated. bly due to degraded genomic DNA. Sequences are stored Figure 1. Distribution of analyzed haplotypes. The numbers correspond to the haplotype names presented in Table 1. 160 Period biol, Vol 112, No 2, 2010. Period biol, Vol 112, No 2, 2010. TABLE 1 Phylogeny and evolution of List of taxa with indicated haplotype group, geographical origin and collection numbers (specimen tissue voucher abbreviations) of all taxa sequenced and analyzed in this study along with GenBank accession numbers of sequences used in phylogenetic inference. The numbers in parentheses represent collection localities referred according to the Fig. 1. Subfamily Lineages Taxon Geographical origin Haplotype Voucher Name of sequence GenBank (current (current taxonomy) abbreviation used in phylogenetic Accesion Number taxonomy) inference Paratyinae »Anophthalmus« T. anophthalmus Mandalina {pilja, anchihaline Troglocaris n. sp. 1 A1 A1 16S DQ320019 (Kollar, 1948) cave, [ibenik, HR (1) Troglocaris Paratyinae »Anophthalmus« T. anophthalmus Tunnel Plomin, T. anophthalmus A A2 A2 16S DQ320020 (Kollar, 1948) spring in tunnel, HR (2) A2 COI DQ320036 A2 COII DQ320052 Paratyinae »Anophthalmus« T. anophthalmus Jama pod Krogom, cave, T. anophthalmus AN AN1 AN1 16S DQ320021 (Kollar, 1948) Mlini, HR-Sl (3) AN1 COI DQ320037 AN1 COII DQ320053 Paratyinae »Dinaro-Caucasian« T. hercegovinensis Spring Rupe~ica, Ivanci, Troglocaris n. sp. 2 L1 L1 16S DQ320022 (Babi}, 1922) Ogulin, HR (4) L1 COI DQ320038 Paratyinae »Anophthalmus« T. anophthalmus Cave near Jurjevi}i, Troglocaris n. sp. 3 P1 P1 16S DQ320023 (Kollar, 1948) Pelje{ac peninsula, HR (5) P1 COI DQ320039 P1 COII DQ320054 Paratyinae »Anophthalmus« T. planinensis Planinska jama, cave, T. a. planinensis PL1 PL1 6S DQ320024 (Bir{tejn, 1948) Planina, Sl (6) PL1 COI DQ320040 PL1 COII DQ320055 Paratyinae »Anophthalmus« T. anophthalmus Vjetrenica, cave, Troglocaris n. sp. 4 T21 T21 16S DQ320025 (Kollar, 1948) Popovo polje, BA (7a) T21 COI DQ320041 T21 COII DQ320056 Paratyinae »Anophthalmus« T. intermedia Kukuruzovi}a {pilja, cave, T. a. intermedia T24 T24 16S DQ320026 (Babi}, 1922) Vaganac, Rakovica, HR (8) T24 COI DQ320042 T24 COII DQ320057 Paratyinae »Anophthalmus« T. anophthalmus Jama u Predolcu, cave, Troglocaris n. sp. 4 T26 T26 16S DQ320027 D. Franjevi} (Kollar, 1948) Metkovi}, HR (9) T26 COII DQ320058 Paratyinae »Dinaro-Caucasian« T. hercegovinensis Vjetrenica, cave, T. hercegovinensis TH1 TH1 16S DQ320028 (Babi}, 1922) Popovo polje, BA (7b) TH1 COI et al. 161 DQ320044 D. Franjevi} et al. Phylogeny and evolution of Troglocaris in GenBank under accession numbers from DQ320019 to DQ320061. DNA extraction, gene amplification, and DQ320030 DQ320046 DQ320059 DQ320032 DQ320048 DQ320033 DQ320061 DQ320029 DQ320045 DQ320031 DQ320047 sequencing DNA extraction – Total genomic DNA was extracted from alcohol
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