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Phylogenetic Relationships of the Western North American Phoxinins (Actinopterygii: Cyprinidae) As Inferred from Mitochondrial 1

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Phylogenetic Relationships of the Western North American Phoxinins (Actinopterygii: Cyprinidae) As Inferred from Mitochondrial 1 MOLECULAR PHYLOGENETICS AND EVOLUTION Vol. 9, No. 2, April, pp. 308–329, 1998 ARTICLE NO. FY970467 Phylogenetic Relationships of the Western North American Phoxinins (Actinopterygii: Cyprinidae) as Inferred from Mitochondrial 12S and 16S Ribosomal RNA Sequences Andrew M. Simons1 and Richard L. Mayden *Department of Biological Sciences, The University of Alabama, Box 870344, Tuscaloosa, Alabama 35487 Received June 6, 1997 able in appearance, biology, and distributions, ranging Parsimony analysis of the mitochondrial 12S and 16S from the small, herbivorous Eremichthys with a maxi- rRNA sequences of North American phoxinin taxa mum length of 65 mm to the large, piscivorous Ptycho- indicated the existence of three major clades, the cheilus that can reach lengths of up to 1.8 m. Members Western Clade, the Creek Chub Clade, and the Open of this fauna have previously been hypothesized to be Posterior Myodome Clade. The monophyletic Western related to both Asian (Howes, 1984; Miller, 1959, 1965) Clade identified in this paper contained fewer taxa and eastern North American taxa (Bailey, 1956; Uyeno, than that identified by previous authors. This clade 1961). However, few studies on relationships of the contained species restricted to drainages west of the Continental Divide, such as Gila, Acrocheilus, Relic- western fauna have included appropriate taxa neces- tus, Eremichthys, Siphateles, Ptychocheilus, Lavinia, sary to assess their interrelationships to other cy- and Orthodon, and the wide-ranging genus Phoxinus prinids. The traditional view of a uniquely derived found in eastern North America and Eurasia. Within this western fauna is complicated by the presence of wide- Western Clade Phoxinus was the basal sister group. Gila spread taxa such as Rhinichthys and the presumed was recognized as a monophyletic group exclusive of relationships between western genera, such as Richard- Siphateles and Snyderichthys, clades traditionally recog- sonius, and eastern genera, such as Clinostomus. The only nized as subgenera of Gila. The genus Gila was most explicitly phylogenetic study that clearly identified a clade closely related to the genus Acrocheilus and together of western cyprinids was that by Coburn and Cavender these formed the sister group to the genus Relictus. These (1992); however, based on their analysis, the western relationships were supported independent of weighting cyprinid fauna does not constitute a monophyletic group. schemes used in analyses. Identification of Phoxinus as Much of the western cyprinid fauna was described in the the basal sister taxon of the Western clade implies that late 1800s and early 1900s particularly by Baird, Girard, other major clades of North American Phoxinins likely Snyder, Jordan, and Evermann. Their work was an invalu- haveAsian or European relatives. ௠ 1998 Academic Press able first step in understanding this fauna. Unfortunately, in the process of describing this fauna they generated a confusing plethora of names, particularly with taxa related INTRODUCTION to Gila. Some taxa were even described a number of times, even within the same publication (Girard, 1856). In 1945, The cyprinids of western North America have long Miller revised the genera Gila, Siboma, Tigoma, Cheonda, presented an interesting taxonomic problem. The west- and Richardsonius. Of these genera, Miller recognized only ern cyprinid fauna has traditionally been identified Richardsonius and Gila. Cheonda, Siboma, and Tigoma largely on geographic criteria, containing taxa native to were subsumed under Gila. Within Gila, Miller recognized drainages west of the Continental Divide. The fauna is the subgenera Gila, Siboma, and Temeculina and erected viewed as distinctive due to the high number of en- the subgenus Klamathella to contain Gila bicolor (Girard). demic genera in the region, roughly 50% of which are The diagnoses of these subgenera were based on pharyn- monotypic (Miller, 1959). These taxa are highly vari- geal tooth counts, scale radii, and point of origin of the dorsal fin relative to that of the pelvic fins. Bailey (1956) 1 To whom correspondence and reprint requests should be ad- subsumed the genera Richardsonius and Clinostomus into dressed at current address: The University of Massachusetts, Depart- the genus Gila based on their general appearance, ecology, ment of Biology, Graduate Program in Organismic and Evolutionary and distribution. Bailey’s classification was not widely Biology, Morrill Science Center, Box 35810, Amherst, MA accepted, and Uyeno (1961), in his study of the osteology Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under Accession Nos. AF 023183, AF and phylogeny of Gila and relatives, resurrected Richard- 023186, AF 023188, AF 023192, AF 023194, AF 023195, AF 023197, sonius (including Clinostomus) from synonymy with Gila. AF 023198, AF 023201, AF038468–AF038498. Uyeno combined the genera Siphateles and Snyderichthys 308 1055-7903/98 $25.00 Copyright ௠ 1998 by Academic Press All rights of reproduction in any form reserved. PHYLOGENETIC RELATIONSHIPS OF PHOXININS 309 FIG. 2. Hypothesized phylogenetic relationships of the Western FIG. 1. Hypothesized relationships of the genera Gila, Richardso- Clade based on osteological and lepidological characters, from Co- nius, and Ptychocheilus from Uyeno (1961). burn and Cavender (1992). with Gila, an action that caused nomenclatural difficulties, large genetic difference between Notemigonus and the as the name bicolor was then used for the blue chub, Gila remainder of the included taxa, consistent with the bicolor, and the tui chub, Siphateles bicolor. Bailey and view that Notemigonus is a leuciscin, not closely related Uyeno (1964) resolved this by selecting Algansea bicolor as to the remainder of the North American fauna, which the name to retain in Gila for the tui chub and designating are phoxinins (Cavender and Coburn, 1992). Of the Gila coerulea as the oldest available name for the blue native California cyprinids included in Avise and Aya- chub. Uyeno (1961) recognized three subgenera within la’s (1976) analysis, two groups can be identified, one Gila, Gila, Siphateles, and Snyderichthys, and presented a containing Richardsonius and Pogonichthys and the other containing Ptychocheilus, Mylopharodon, Lavinia, phylogeny (Fig. 1) wherein Gila and Siphateles were 3 depicted as sister taxa, sister to Snyderichthys. The genus and Hesperoleucas. Within the second group, S. bicolor Gila was identified as the sister group to Richardsonius clusters with Orthodon. This cluster is sister to Hespero- (including Clinostomus), and this clade was sister to Ptycho- leucas plus Lavinia and Mylopharodon plus Ptychochei- cheilus. Although the subgenus Temeculina has been recog- lus. Indeed, the genetic distances between Mylophar- nized by some (Barbour and Miller, 1978) this taxonomy odon and Ptychocheilus and between Hesperoleucas and renders the subgenus Gila paraphyletic based on Uyeno’s Lavinia were so small that Avise and Ayala (1976) sug- (1961) tree. gested that they should be considered congeners. Avise and Ayala (1976) examined genetic variability Coburn and Cavender (1992) performed a phyloge- at 24 loci in eight species of California cyprinids and netic analysis on almost all North American cyprinid Notemigonus crysoleucas.2 Their analysis revealed a taxa using lepidological and osteological characters. They proposed a monophyletic western clade contain- ing Gila and relatives (Fig. 2). This clade was largely 2 They utilized three algorithms to determine relationships among composed of taxa restricted to the Colorado system, the these taxa: (1) UPGMA, (2) WPGMA, and (3) Modified Wagner. Of these methods, the modified Wagner analysis requires fewer assump- tions regarding evolutionary rates and therefore will be the only 3 We refer G. bicolor to the genus Siphateles as our results indicate analysis discussed herein. that this taxon is not closely related to Gila. 310 SIMONS AND MAYDEN Great Basin, and Pacific drainages. Their analysis Specimens Examined indicated that some taxa previously considered rela- The specimens examined included the following: tives of Gila, such as Clinostomus and Richardsonius Abramis bjoerkna (Brunnsviken Bay, Stockholm, Upp- (Bailey, 1956; Uyeno, 1961), were more closely related land, Sweden, UAIC 85533.03); Acrocheilus alutaceus to other major clades of North American cyprinids. (Kettle River, British Columbia, Canada, UAIC Coburn and Cavender were unable to resolve relation- 11365.01); Couesius plumbeus Mill Creek, 100 miles ships among many western taxa; only their Gila clade north of Ft. Nelson, British Columbia, Canada, UAIC is resolved (Fig. 2). Based on their analysis the genus 11366.01); Eremichthys acros (Soldier Meadows, Hum- Gila, as recognized by Uyeno (1961), is polyphyletic. Of boldt Co., NV); Gila atraria (Sevier River, Piute Co., the taxa that Coburn and Cavender included in the UT); Gila coerulea (Upper Klamath Lake, Klamath Co., western clade, we consider the following to be members OR, OS015083 (two specimens)); Gila conspersa (Rio of the open posterior myodome (OPM) clade: Mylocheilus, San Isabel at General Trias, Chihuahua, Mexico, UAIC Pogonichthys, Rhinichthys, Tiaroga, and Agosia (Simons, 7910.01); Gila cypha (Colorado River, Coconino Co., 1996). We refer to the Plagopterins plus the Creek Chubs AZ); Gila ditaenia (Sycamore Canyon, Santa Cruz Co., as the Creek Chub Clade (Simons and Mayden, 1997). AZ); Gila nigrescens (Mimbres River, NM); Gila orcutti In a study based on
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