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Phylogenetic Relationships of the Western North American Cyprinid Genus Richardsonius, with an Overview of Phylogeographic Structure

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Phylogenetic Relationships of the Western North American Cyprinid Genus Richardsonius, with an Overview of Phylogeographic Structure Molecular Phylogenetics and Evolution 55 (2010) 259–273 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogenetic relationships of the western North American cyprinid genus Richardsonius, with an overview of phylogeographic structure Derek D. Houston a,*, Dennis K. Shiozawa b, Brett R. Riddle a a University of Nevada Las Vegas, School of Life Sciences, 4505 Maryland Parkway, Las Vegas, NV 89154-4004, USA b Brigham Young University, Department of Biology, 147-A WIDB, Provo, UT 84602, USA article info abstract Article history: Diversification of many North American taxa, including freshwater fishes, has been heavily influenced by Received 14 July 2009 the effects of complex geological and climatic events throughout the Cenozoic that have significantly Revised 9 October 2009 altered the landscape. Here, we employ an array of phylogenetic analyses using a multiple gene tree Accepted 13 October 2009 approach to address several questions regarding the phylogenetic relationships of the North American Available online 27 October 2009 cyprinid genus Richardsonius and two other closely related genera, Clinostomus and Iotichthys. We also use divergence time estimates generated using fossil calibrations to qualitatively assess the phylogeo- Keywords: graphic implications of evolution within the group. Mitochondrial and nuclear DNA sequences show a Biogeography sister relationship between Iotichthys and Richardsonius, with Clinostomus being sister to an Iotichthys– Clinostomus Cyprinidae Richardsonius clade, hence the currently recognized sister relationship between Clinostomus and Drainage history Richardsonius is not supported. These genera appear to be monophyletic lineages, and sister species Iotichthys within genera appear to be reciprocally monophyletic. The two species within the genus Richardsonius Lahontan redside shiner both exhibit phylogeographic structure that is worthy of further investigation. Divergence time estimates Redside shiner between genera and species are Miocene or Pliocene in age, and divergence between phylogroups within species occurred in the late Pliocene to Pleistocene. These splits coincide with documented geological and climatic events. Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction various freshwater fishes around the globe (e.g., Bermingham and Avise, 1986; McGuigan et al., 2000; Unmack, 2001; Smith The cumulative geological and climatic changes that molded and Bermingham, 2005; Swartz et al., 2007; Zemlak et al., 2008). the Cenozoic North American landscape have profoundly influ- The evolution of freshwater fishes in western North America has enced patterns of diversification across numerous taxa (e.g., been characterized by long term isolation of populations, punctu- Minckley et al., 1986; Riddle, 1995; Klicka and Zink, 1997; Soltis ated by sporadic dispersal amongst hydrological basins during ma- et al., 1997; Brunsfeld et al., 2001; Hershler and Sada, 2002; He- jor events such as floods or stream captures, some of which witt, 2004; Castoe et al., 2007; Liu and Hershler, 2007; Kohn and coincide with major climatic events (Smith, 1981; Minckley Fremd, 2008). If, as seems likely, the evolution of many North et al., 1986; Johnson, 2002; Smith et al., 2002; Mock et al., 2006). American taxa has been influenced both by recent changes in glo- Richardsonius is a genus of western North American freshwater bal climate as well as by temporally deeper geological changes to fish from the family Cyprinidae that contains two species: redside the landscape (Riddle, 1996), those taxa should exhibit shallow ge- shiner Richardsonius balteatus (Richardson) and Lahontan redside netic structure superimposed on deep divergences. Indeed, such shiner Richardonius egregius (Girard). However, the state of Oregon hierarchical structure has been demonstrated for a variety of taxa recognizes two additional species, coastal redside shiner R. siuslawi (e.g., Demboski and Cook, 2001; Wilke and Duncan, 2004; Alexan- and hotspring redside shiner R. thermophilus, claiming that they der and Riddle, 2005; Carstens et al., 2005a; Steele et al., 2005). were ‘‘lumped with R. balteatus without evidence” (ODFW, 2005). Perhaps due to their reduced vagility in comparison, aquatic For the purposes of this study, we use the conventional two species taxa tend to maintain a more intact signature of responses to geo- classification of R. balteatus and R. egregius (as recognized by the logical processes and climate change than do terrestrial organisms American Fisheries Society, the American Society of Ichthyologists (Bernatchez and Wilson, 1998), as has been demonstrated among and Herpetologists, and the Integrated Taxonomic Information System). Richardsonius is of biogeographic interest because of its wide distribution throughout several western North American * Corresponding author. Fax: +1 702 895 3956. E-mail addresses: [email protected] (D.D. Houston), shiozawa@byu. drainages (Fig. 1). Numerous ancient connections have existed be- edu (D.K. Shiozawa), [email protected] (B.R. Riddle). tween these drainage basins at different times throughout the 1055-7903/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2009.10.017 260 D.D. Houston et al. / Molecular Phylogenetics and Evolution 55 (2010) 259–273 Fig. 1. Map depicting the natural distributions of the seven species belonging to the Mylocheilus sub-clade of North American cyprinids. Two species, M. caurinus and R. balteatus overlap through much of their ranges, so that of M. caurinus is outlined with a dashed line to show the difference. Paleogene, suggesting a number of opportunities for isolation and Open Posterior Myodome (OPM) clade (Mayden, 1989; Simons dispersal as drainage systems evolved (Taylor, 1985; Minckley et al., 2003), which contains four genera: Clinostomus, Mylocheilus, et al., 1986; Smith et al., 2002; Spencer et al., 2008). Moreover, R. Pogonichthys and Richardsonius (Simons et al., 2003). Within the balteatus exhibits morphological (Hubbs and Miller, 1948; Lindsey, Mylocheilus sub-clade, Richardsonius and Clinostomus were most re- 1953; Smith, 1966; McPhail and Lindsey, 1986; Minckley et al., cently postulated to be sister genera (Simons et al., 2003), 1986; La Rivers, 1994; Smith et al., 2002) and ecological differences although, because one genus was not included in recent studies among populations (Houston and Belk, 2006) that may be due, in (see below), the extant sister genus to Richardsonius remains part, to a history of geographic isolation. Some of these morpholog- unclear. ical differences (primarily the number of anal fin rays), coupled Richardsonius is somewhat unique among western North Amer- with geographic distributions, are the basis for dividing R. balteatus ican cyprinids in that the hypothesized sister taxon, Clinostomus,is into two sub-species, R. b. balteatus and R. b. hydrophlox. a genus that occurs east of the Rocky Mountains. Like Richardso- Monophyly of Richardsonius has never been rigorously tested or nius, Clinostomus contains only two species: redside dace Clinosto- questioned. Given that recent studies have uncovered cryptic ge- mus elongatus (Kirtland), which occurs in the Great Lakes region, netic diversity within other North American cyprinid genera (John- and rosyside dace Clinostomus funduloides Girard, which occurs in son et al., 2004; Schönhuth et al., 2008; Houston et al., in press)we the southeastern United States (Fig. 1; Lee et al., 1980). The genera believe it is prudent to evaluate the monophyly of this genus prior Clinostomus and Richardsonius have long been considered to be clo- to engaging in detailed phylogeographic studies. Numerous studies sely related, and have even been grouped in the same genus at have provided what appear to be robust evolutionary hypotheses times (for review, see Simons and Mayden, 1998, 1999). The sister regarding the phylogenetic relationships of many North American relationship of these two genera appears to be supported both by cyprinid genera (e.g., Mayden, 1989, 1991; Cavender and Coburn, morphology (Coburn and Cavender, 1992) and by mitochondrial 1992; Coburn and Cavender, 1992; Dowling and Naylor, 1997; Si- DNA (mtDNA) sequence data (Simons and Mayden, 1999; Simons mons et al., 2003; Johnson et al., 2004; Blum et al., 2008). et al., 2003). However, recent evidence suggests that another Richardsonius belongs to the Mylocheilus sub-clade of Mayden’s genus, Iotichthys, may also be closely related to Richardsonius. D.D. Houston et al. / Molecular Phylogenetics and Evolution 55 (2010) 259–273 261 The least chub Iotichthys phlegethontis (Cope) is a monotypic spe- not likely to be any more closely related to Richardsonius than cies that occurs in the northern Bonneville Basin (Fig. 1; Lee other members of the shiner clade. et al., 1980; Mock and Miller, 2005). To our knowledge, there have We aligned GenBank sequences automatically using Sequen- been only a few phylogenetic studies to date that include Clinosto- cher v. 4.6 (Gene Codes Corp.) and corrected the alignment by mus, Iotichthys and Richardsonius. The first was based on morpho- eye, using the amino acid sequence for reference. We analyzed logical characters and showed sister relationships between the data using maximum parsimony (MP) and maximum likeli- Clinostomus and Richardsonius, and between Iotichthys and Utah hood (ML) optimality criteria, as well as Bayesian inference. For chub Gila atraria (Girard), another western
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