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Teleostei: Cyprinidae) from Cytochrome B Sequences

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Teleostei: Cyprinidae) from Cytochrome B Sequences Copeia, 2002(3), pp. 665±678 Evolutionary Relationships of the Plagopterins (Teleostei: Cyprinidae) from Cytochrome b Sequences THOMAS E. DOWLING,C.ALANA TIBBETS,W.L.MINCKLEY, AND GERALD R. SMITH Sequences of cytochrome b (cytb) were used to examine composition and phylo- genetic relationships of cyprinid ®shes of the tribe Plagopterini, endemic to the Great Basin and Lower Colorado River in southwestern North America. The pla- gopterin genera, Lepidomeda, Meda, Plagopterus, and Snyderichthys, were most closely af®liated with the chubs Couesius and Margariscus of northern and eastern North America. As indicated by previous morphologic, allozymic, and mtDNA studies, Sny- derichthys is intimately related to Lepidomeda. The relationship is paraphyletic, how- ever, according to our molecular data. Snyderichthys from the Snake and Bear River drainages are part of a clade that includes Lepidomeda mollispinis and Lepidomeda albivallis according to the cytb sequence, with Snyderichthys from the central and southern Bonneville basin more divergent. This paraphyly and the complex geo- graphic relationships of mtDNA sequences indicate a complex history of the group and cast doubt on the validity of morphologically diagnosed Snyderichthys. Estimates of divergence time, based on a combination of fossil and molecular data, indicate that the plagopterins are an ancient clade, at least 17 million years old. HE Cyprinidae or minnows are the most di- They hypothesized existence of three major T verse freshwater ®sh family in North Amer- groups: ``shiner,'' ``chub,'' and ``western'' ica, represented by more than 300 species in clades. Plagopterins fell within a Gila clade of approximately 50 genera (Burr and Mayden, western minnows, most closely related to a clade 1992). Although recent morphological studies containing Agosia, Moapa, and Rhinichthys.As provide hypotheses of relationships among gen- previously indicated by Uyeno (1960), Gila copei era, species groups, and species (Mayden, 1989; was considered distinct from the plagopterins. Cavender and Coburn, 1992; Coburn and Cav- Studies of molecular characters indicated dif- ender, 1992), analysis of molecular characters ferent plagopterin relationships. DeMarais sometimes produce con¯icting results (e.g., Si- (1992) provided allozymic evidence that G. copei mons and Mayden, 1997, et seq.; Broughton was closely af®liated with Lepidomeda, possibly and Gold, 2000) and a different perspective of rendering the plagopterins paraphyletic. Fur- evolutionary relationships. ther taxonomic studies were deemed necessary The plagopterins are a monophyletic group to ensure proper phylogenetic placement of G. of North American cyprinids diagnosed by copei; however, its close af®nities with Lepidomeda spinelike ossi®cation of the ®rst two rays of the led DeMarais (1992) to recommend resurrec- dorsal and pelvic ®ns. As de®ned by Miller and tion of Snyderichthys, a recommendation we fol- Hubbs (1960), the group consists of six species low. in three genera: Lepidomeda vittata, Lepidomeda Simons and Mayden (1997, et seq.) identi®ed mollispinis, Lepidomeda albivallis, and Lepidomeda four major lineages (with sequences from 12S altivelis; Meda fulgida; and Plagopterus argentissi- ribosomal DNA) that differed from those iden- mus. These are (or were) endemic to the middle ti®ed by Coburn and Cavender (1992). Both and lower Colorado River drainage. Relation- morphological and molecular data indicated a ships of this group to several other cyprinids of distinct western clade; however, there were ma- the region have been hypothesized, especially jor differences in composition and placement Snyderichthys copei (Miller, 1945) of the adjacent of taxa within the chubs and shiners. Creek Bonneville basin and upper Snake River drain- chubs and relatives (Couesius, Hemitremia, Mar- age. That species was placed in the monotypic gariscus, Semotilus) were identi®ed as a distinct genus Snyderichthys by Miller (1945) but consid- lineage (``creek chub clade'') instead of being ered a monotypic subgenus of the genus Gila by members of the chub clade as hypothesized by Uyeno (1960). Coburn and Cavender (1992). Plagopterins (in- Coburn and Cavender (1992) completed an cluding Snyderichthys) were more closely related extensive analysis of phylogenetic relationships to this clade than to members of the genus Gila. among North American cyprinids based on Simons and Mayden (1997) included only two morphological and osteological characters. plagopterins (L. vittata, M. fulgida); therefore, q 2002 by the American Society of Ichthyologists and Herpetologists 666 COPEIA, 2002, NO. 3 gopterus argentissimus are found only in single drainages. Previous studies of variation in L. vit- tata indicated limited divergence among locali- ties (Tibbets, 1998; Tibbets et al., 2001); there- fore, single individuals of Lepidomeda mollispinis mollispinis, L. vittata, and Plagopterus argentissi- mus were used to represent each. Previous stud- ies of Meda fulgida (Anderson and Hendrickson, 1994; Tibbets and Dowling, 1996) identi®ed di- vergent populations in the Gila and Verde Riv- ers; therefore each was represented. Because of the widespread distribution and potential para- phyly of Snyderichthys to the plagopterins, mul- tiple samples were also examined (Bonneville basin, Bear and Snake River drainages). Representatives of the three major clades (western, shiner, and chub) of Coburn and Cav- ender (1992) were also examined, with special emphasis on hypothesized sister taxa to plagop- terins. These names will be used throughout manuscript. Chubs were Campostoma anomalum, Couesius plumbeus, Hybognathus hankinsoni, Mar- Fig. 1. Approximate distribution of species and gariscus margarita, Nocomis micropogon, and Semo- samples (indicated by lines and shading). Snyderichthys tilus atromaculatus. Shiners included Cyprinella copei, Goose Creek (SCGC), Sulphur Creek (SCSC), spiloptera, Luxilus chrysocephalus, and Pimephales Spanish Fork River (SCSF), Sevier River (SCSR); Lep- notatus. Representatives of the western clade idomeda albivallis (LA), Lepidomeda mollispinus mollispi- were Acrocheilus alutaceus, Agosia chrysogaster, Gila nus (LMM), Lepidomeda mollispinus pratensis (LMP); cypha, Moapa coriacea, Orthodon microlepidotum, Lepidomeda vitatta (LV); Plagopterus argentissimus (PA); and Rhinichthys atratulus. Based on relationships Meda fulgida, Verde River (MFV), Aravaipa Creek inferred from morphological characters (Cav- (MFA). The southwest range limits of the sister ender and Coburn, 1992; Coburn and Caven- groups, Couesius plumbeus and Margariscus margarita, are shown in the upper right. der, 1992), sequences from the leuciscins Abram- is brama (Briolay et al., 1998; GenBank accession nunber Y10441) and Notemigonus crysoleucas relationships within the group and effects of (Schmidt and Gold, 1995; GenBank accession taxonomic sampling on placement of Snyderi- number U01318) were used as outgroups. chthys could not be examined. We use sequences from the cytochrome b Sequencing.ÐSequences were obtained from (cytb) gene from all extant plagopterins to ex- PCR products by either standard dideoxy se- amine relationships among members of this quencing or cycle-sequencing and deposited in group and to test the hypothesized placement GenBank (accession numbers in Material Ex- of these ®shes relative to other cyprinids [as amined). In the standard method, templates proposed by Coburn and Cavender (1992) and were obtained through two rounds of ampli®- Simons and Mayden (1997)]. Given the unique cation. In the ®rst, a double-stranded product morphology and geography of these ®shes, was generated as follows: 1±5 ml (approximately knowledge of their phylogenetic relationships 1±5 ng) of genomic DNA; 0.25 units of Taq DNA to other minnow lineages provides important polymerase [from Promega Corp. or puri®ed information for the evolution of morphological characters and the biogeography of several ma- from a clone as described by Pluthero (1993)]; jor drainages in western North America. 4 ml of dNTP mix (®nal concentration of 200 mM of each of the four dNTPs); 2.5 ml MgCl2 stock (®nal concentration of 2.5 mM); 2.5 mlof MATERIALS AND METHODS 103 buffer stock [provided by the enzyme sup- Samples.ÐMost plagopterin taxa now occupy plier or as described in Pluthero (1993)]; 1.25 limited ranges (Fig. 1) in the lower Colorado ml of each primer (®nal concentration of 0.5 River system. Lepidomeda albivallis and Lepidome- mM of each); sterile-distilled water to a ®nal vol- da mollispinis pratensis are restricted to single lo- ume of 25 ml. Ampli®cation was performed by calities and L. m. mollispinis, L. vittata, and Pla- 20 cycles of denaturation at 94 C for 1 min, an- DOWLING ET AL.ÐRELATIONSHIPS OF PLAGOPTERINS 667 TABLE 1. SEQUENCES OF PRIMERS USED FOR AMPLIFICATION AND SEQUENCING OF CYTb. Primera Positionb Sequence LA-a 15248 59 GTG ACT TGA AAA ACC ACC GTT G 39 LC-s 15536 59 ATA CAT GCC AAC GGA GCA TC 39 HD-a 15894 59 GGG TTG TTT GAT CCT GTT TCG T 39 LD-a 15848 59 CCA TTC GTC ATC GCC GGT GC 39 LDIB-a 15768 59 ACC CTT GTT CAA TGA ATC TG 39 LDLUX-a 15812 59 ACA TTA ACA CGA TTC TTC GC 39 LE-s 16084 59 CCC ACC ACA CAT TCA ACC 39 HA-a 16462 59 CAA CGA TCT CCG GTT TAC AAG AC 39 a Primers are designated by strand (L 5 light, H 5 heavy) and application (a 5 ampli®cation and sequencing, s 5 sequencing only). b Position is identi®ed relative to the published sequence for carp, Cyprinus carpio, (Chang et al., 1994). nealing at 48 C for 1 min, and extension at 72 Swofford, Sinauer Associates,
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