Molecular Systematics of North American Phoxinin Genera (Actinopterygii: Cyprinidae) Inferred from Mitochondrial 12S and 16S Ribosomal RNA Sequences
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Blackwell Science, LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin- nean Society of London, 2003? 2003 1391 6380 Original Article A. M. SIMONS ET AL. NORTH AMERICAN PHOXININ SYSTEMATICS Zoological Journal of the Linnean Society, 2003, 139, 63–80. With 7 figures Molecular systematics of North American phoxinin genera (Actinopterygii: Cyprinidae) inferred from mitochondrial 12S and 16S ribosomal RNA sequences ANDREW M. SIMONS1*, PETER B. BERENDZEN1 and RICHARD L. MAYDEN2 1University of Minnesota, Department of Fisheries, Wildlife, and Conservation Biology & Bell Museum of Natural History 1980 Folwell Avenue, St Paul, MN 55108, USA 2Saint Louis University, Department of Biology, 3507 Laclede Avenue, St Louis, MO 63103, USA Received June 2002; accepted for publication December 2002 The cyprinid fish fauna of North America is relatively large, with approximately 300 species, and all but one of these are considered phoxinins. The phylogenetic relationships of the North American phoxinins continue to pose diffi- culties for systematists. Results of morphological analyses are not consistent owing to differences interpreting and coding characters. Herein, we present phylogenetic analyses of mitochondrial 12S and 16S ribosomal RNA sequence data for representatives of nearly all genera of North American phoxinins. The data were analysed using parsimony, weighted parsimony, maximum likelihood and bayesian analyses. Results from weighted parsimony, likelihood and the bayesian analysis are largely consistent as they all account for differing substitution rates between transitions and transversions. Several major clades within the fauna can be recognized and are strongly supported by all anal- yses. These include the western clade, creek chub–plagopterin clade and the open posterior myodome clade. The shiner clade is nested in the open posterior myodome clade and is the most species-rich clade of North American phoxinins. Relationships within this clade were not well resolved by our analyses. This may reflect the inability of the mitochondrial RNA genes to resolve recent speciation events or taxon sampling within the shiner clade. © 2003 The Linnean Society of London, Zoological Journal of the Linnean Society, 2003, 139, 63–80. ADDITIONAL KEYWORDS: bayesian estimation – evolution – maximum likelihood – parsimony. INTRODUCTION with all North American genera in the subfamily Leu- ciscinae. Leuciscinae was diagnosed by two charac- The family Cyprinidae is native to all continents ters: pharyngeal arch with one or two rows of teeth, except for Australia, Antarctica and South America and the loss of the suborbital–infraorbital connection. (Mayden, 1991). Over 2000 species have been Within Leuciscinae, two lineages of cyprinids were described (Nelson, 1994), 300 of which are from North recognized, both of which are present in North Amer- America (Mayden et al., 1992). Their high diversity ica, leuciscins and phoxinins. The leuciscins are pri- and widespread distribution have made cyprinids one marily Eurasian, with a single North American of the most difficult groups of fishes to understand tax- representative, the golden shiner (Notemigonus cryso- onomically and systematically (Mayden, 1989, 1991). leucas [Mitchill]). Phoxinins make up the remaining Various researchers have attempted to decipher the North American cyprinid diversity. There are several phylogenetic history and classify these fishes. One of Eurasian phoxinin genera known but their relation- the latest efforts employing phylogenetic systematics ship to the North American taxa is currently was by Cavender & Coburn (1992). Cavender & unresolved. Coburn recognized several subfamilies worldwide, The North American phoxinins are one of the most taxonomically difficult groups of fishes on the conti- nent. The large number of taxa, their diverse and com- *Corresponding author. E-mail: [email protected] plex morphological evolution, and their widespread © 2003 The Linnean Society of London, Zoological Journal of the Linnean Society, 2003, 139, 63–80 63 64 A. M. SIMONS ET AL. distribution has hampered an understanding of their Relationships and classification of North Ameri- phylogenetic relationships, essential for comprehend- can phoxinins have been chaotic since Rafinesque ing the evolution of biodiversity of these fishes. The (1818) described Notropis atherinoides (Fig. 2a). A tremendous breadth of trophic morphologies, breeding proliferation of generic and specific names has behaviours and habitat preferences (to name a few resulted in complex synonymies; some taxa have characteristics) is unmatched by any other group of been described a number of times, even within the North American fishes. Like cyprinid groups from same paper, e.g. Girard (1856). The confusion con- other continents, North American phoxinins contain tinued through the early part of the 20th century, algivores, herbivores (Fig. 1c,d), planktivores and pis- reflecting the absence of a coherent philosophy gov- civores (Fig. 1a,f), often with specialized oral morphol- erning classification and taxonomy. The cyprinid ogies for obtaining food. The most bizarre of these is fauna was considered to contain two distinct Exoglossum maxillinguae (Lesueur), a species that groups, a western fauna and an eastern fauna. The has been reported to use its modified lower jaw to western fauna contained taxa native to Pacific pluck eyes out of other fishes (Scott & Crossman, 1973; drainages whereas the eastern fauna contained Page & Burr, 1991). Breeding behaviours are very taxa native to the Mississippi, other Gulf of Mexico diverse; these include various courtship displays with drainages and Atlantic drainages. Although several spawning over unprepared substrate, in rock crevices, taxa obviously did not conform to this pattern, this cavities beneath rocks and on large, gravel nests. view has persisted. Members of the genus Nocomis (Fig. 2h) construct In the 1950s, Reeve Bailey dramatically revised the nests over 1 m in diameter and up to one-third of a taxonomic structure of several groups of North Amer- metre in height (Johnston & Page, 1992). Other spe- ican fishes. In an attempt to simplify the classification cies are known as nest associates and spawn over cyp- of minnows, Bailey (1951, 1956) synonymized several rinid or non-cyprinid fish species nests and leave genera based on a few morphological characters. parental care to the nest-constructing species. Pter- These characters include the presence and position of onotropis hubbsi (Bailey & Robison) and Notropis barbels, scalation and gut morphology. His simplifica- cummingsae Myers spawn over nests of sunfishes and tion of cyprinid classification was paralleled by basses (Centrarchidae) (Fletcher & Burr, 1992, 1993), similar changes in the classification of the North species that are normally considered predators, and American darters (Bailey, 1951; Bailey, Winn & initiate their spawning only after the presumed Smith, 1954; Bailey & Gosline, 1955). These taxo- release of pheromones contained in the milt of the cen- nomic changes were not proposed in papers on classi- trarchid species male (Hunter & Hasler, 1965). North fication but as footnotes in keys (Bailey, 1951, 1956) or American phoxinins are found in a wide range of hab- as commentaries in papers on distribution (Bailey itats, including high-velocity headwater streams, et al., 1954). Although there were some immediate large, silt-laden rivers, swamps and lakes and exhibit reactions to these taxonomic changes (Lachner & Jen- a wide range of morphologies allowing them to persist kins, 1967; McPhail & Lindsey, 1970; Jenkins & Lach- in these habitats (Figs 1, 2). ner, 1971), they strongly influenced work on North Many early classifications relied on morphological American fish systematics. Hubbs & Miller (1977: characters such as scalation, position of fin insertion, 275) effectively summarized the confusion: ‘It is abun- gut morphology and pharyngeal tooth counts to delin- dantly obvious that much of the generic placement in eate taxonomic boundaries. These classifications were American cyprinids is in a chaotic state, and that the not phylogenetic and were generally based on subjec- prime significance attributed to intestinal coiling vs. tive evaluations of the degree of taxonomic differenti- the single compressed-S configuration, and to the ation provided by various morphological features. presence vs. absence of a maxillary barbel, in the tax- Some characters were considered indicative of generic onomy of the group has been very considerably dis- differences, whereas others were indicative of specific credited.’ Hubbs focused on morphological differences or subspecific differentiation. This approach generated whereas Bailey focused on similarities. The differ- taxonomic instability and confusion. The emergence of ences between Hubbs’ and Bailey’s views perhaps phylogenetic systematics has altered the arguments reflects the tensions of systematic thought of the time, from the value of particular characters or character that classifications should reflect both history and systems to phylogeny reconstruction and appropriate adaptation. interpretation of characters. Although disagreements The introduction of a fundamentally phylogenetic still exist, recent phylogenetic studies are converging approach to classification marked the first real change on a consensus of North American phoxinin relation- in systematics of North American fishes (reviewed by ships. Herein, we review historical approaches and Mayden & Burr, 1992). Mayden (1989)