Taxonomy of Gila in the Lower Colorado River Basin of Arizona and New Mexico

Committee on Names of Fishes, a joint committee of the American Fisheries Society and the American Society of Ichthyologists and Herpetologists

By Lawrence M. Page, and Carole C. Baldwin, Héctor Espinosa-Pérez, Lloyd T. Findley,Carter R. Gilbert, Karsten E. Hartel, Robert N. Lea, Nicholas E. Mandrak, Juan J. Schmitter-Soto, H. J. Walker, Jr.

Species-level taxonomy is the scientific naming of natural populations of organisms for the purpose of communication about evolutionary relationships, geographic distributions, ecology, and other characteristics of importance to science and society. Unlike common names, scientific names are globally recognized, and those of fishes and other animals are subject to the rules of the International Code of Zoological Nomenclature (ICZN 1999). Since 1948, the Committee on Names of Fishes (CNF), a standing joint committee of the American Fisheries Society and the American Society of Ichthyologists and Herpetologists, has published lists of accepted names of fishes of the United States and Canada (Chute et al. 1948; Bailey et al. 1960; Bailey et al. 1970; Robins et al. 1980). Names of fishes for Mexico were added in the sixth edition and continued in the seventh (Nelson et al. 2004; Page et al. 2013).

As stated in the most recent edition (Page et al. 2013:15):

the objectives of the list are to recommend common names and to provide the generally accepted scientific names for all species occurring within the geographic boundaries used. Common names can be stabilized by general agreement. Scientific names, on the other hand, will inevitably shift with advancing knowledge of the phylogenetic relationships of species and in accordance with the views of taxonomists. The scientific nomenclature employed has been reviewed carefully with regard to spelling, authorities, and years of original description. We emphasize that there are many groups of fishes for which there is disagreement on classification or where the classification is poorly known. 

Each scientific name is a label referring to a population distinguished by a set of attributes and, as such, is a hypothesis subject to continuous testing as new information and analyses of data become available. For example, until recently, Lepomis megalotis (described by Rafinesque in 1820) referred to a widespread population of individuals sharing certain characteristics separating segment of the population was recognized by Bailey et al. (2004) as a separate species, Lepomis peltastes (described by Cope in 1870), the name L. megalotis then referred to a less widespread population of individuals with a modified set of characteristics. As changes such as these occur in populations of North American fishes, the CNF modifies the list of accepted names. The seventh edition of the list contained names for 3,875 species for which about 880 changes (Page et al. 2013; Appendix 1) had been made from the sixth edition, which had been published 9 years earlier.

Most species of fishes have been distinguished from other species solely on analyses of morphological data. The rapidly increasing availability of genetic data allows testing of the validity of morphologically defined species. This often results in the recognition of “new” or “cryptic” species, populations that appear to be reproductively isolated but that had not been recognized based on morphological data (Egge and Simons 2006; Wallace and Tringali 2016). Analyses of genetic data, or other new sources of data, also may lead to species names being recognized as junior synonyms of older species names. This happens when morphological data have been misinterpreted, or were geographically incomplete, and were not sufficient to specifically distinguish populations as originally proposed. The taxonomic literature contains many examples of putative species, populations that appeared to be distinguishable based on morphological data but were later rejected. An extreme example is the Longnose Gar Lepisosteus osseus, described by Linnaeus in 1758 and subsequently described as a “new” species 32 times, according to Eschmeyer et al. (2016). Thirty-two of those names are now considered to be junior synonyms of L. osseus.

Another example of morphological data having been misinterpreted and insufficient to distinguish populations as originally proposed is that from Gila in the lower Colorado River basin of Arizona and New Mexico. The taxonomy of Gila in the lower Colorado River basin was the subject of a recent review by the CNF. Because of the complex geological history of the region fishes in freshwaters of the western United States are particularly taxonomically challenging (Smith et al. 2010). Tectonic activity in the western United States over the past 15 million years has resulted in periods of geographic isolation of drainage basins (Flint 1971) and the fishes in those basins. Over long periods, these episodes of isolation have led to varying degrees of genetic differentiation in fishes through natural selection and genetic drift. Tectonic events that followed periods of isolation often led to reunification of basins and mixing and hybridization of previously isolated populations of fishes. This has often resulted in confusing morphological variation within and among populations and has confounded the taxonomy of several groups of fishes (Smith et al. 2010). The recent study of Unmack et al. (2014) on suckers (Catostomidae) clearly demonstrated through analysis of mitochondrial DNA data that many extant species in the western United States are the products of a history of isolation and differentiation followed by periods of hybridization and genetic mixing as drainage patterns have changed. The genetic variation and ensuing morphological complexity are difficult to interpret and express taxonomically. Two species of minnows (Cyprinidae) confined to western drainages that illustrate this phenomenon particularly well are Tui Chub Siphateles bicolor (described by Girard in 1856), which has been described as a separate species 13 times, and Speckled Dace Rhinichthys osculus (also described by Girard in 1856), which has been described as a separate species 18 times (Eschmeyer et al. 2016).

Another taxonomically confusing group of western minnows, sometimes referred to as the Gila robusta species complex, has been a focus of several studies (Rinne 1976; Minckley and DeMarais 2000; Gerber et al. 2001; Schwemm 2006; Dowling et al. 2015). Three nominal species of Gila, G. robusta Baird and Girard 1853, Tigoma intermedia Girard 1856, and G. nigra Cope 1875, were all described in the second half of the 19th century from the lower Colorado River basin of Arizona and New Mexico (which includes the Little Colorado, Bill Williams, Gila, Verde, and Salt River drainages). Tigoma intermedia and G. nigra have been treated as synonyms of G. robusta for much of their taxonomic history, including in early editions of the lists of accepted common and scientific names of fishes (Bailey et al. 1960; Bailey et al. 1970; Robins et al. 1980).

Morphological studies involving Gila in the lower Colorado River basin have varied greatly in their conclusions, with recognition of one to three species in the G. robusta complex (Carter et al. 2016). As noted previously in this article, earlier editions of the checklist included only a single species, G. robusta. Robins et al. (1991), in the fifth edition, recognized G. intermedia as a valid species distinct from G. robusta, based on morphological studies by Rinne (1976) and Minckley’s (1973) use of the name in his book on Arizona fishes. Minckley and DeMarais (2000) revisited the problem and concluded that a third species (G. nigra) also merited recognition, despite considerable overlap throughout the complex in all morphological characters analyzed. Their study led to recognition of all three species in the sixth and seventh editions of the checklist (Nelson et al. 2004; Page et al. 2013). This interpretation included the Gila Chub G. intermedia and Headwater Chub G. nigra, both confined to the Gila River drainage of the lower Colorado River basin in Arizona and New Mexico, and the Roundtail Chub G. robusta, a much more wide-ranging species occurring throughout most of the entire Colorado River basin. A fourth species of Gila also found in the lower Colorado River basin of Arizona, the Bonytail G. elegans, was not considered part of the G. robusta complex.

Based on this understanding of species, G. intermedia was listed as endangered under the U.S. Endangered Species Act and is the subject of a draft recovery plan (USFWS 2005, 2015a). G. nigra and the lower Colorado River distinct population segment of G. robusta were proposed for listing as threatened in 2015 (USFWS 2015b).

Minckley and DeMarais (2000) showed the distributions of the three species they recognized to be largely allopatric, or parapatric in many areas, which could be expected to facilitate identification. However, staff of the Arizona Game and Fish Department (personal communication) have been unable to distinguish morphologically the three putative species as recognized by Minckley and DeMarais. Carter et al. (2016) concluded that the characteristics used by Minckley and DeMarais are too variable and contradict one another in ways that make assignments of individuals to species impossible or, at best, arbitrary.

A contrasting view was presented by Brandenburg et al. (2015), who concluded from a discriminant function analysis of morphological data from individuals collected in the Gila River drainage of the lower Colorado River basin in New Mexico that individuals could be assigned to G. robusta, G. intermedia, or G. nigra. However, in contrast to the results of Minckley and De-Marais (2000), they found the three species to be sympatric in almost all localities sampled and noted that

there is overlap in several morphologic and meristic values used to distinguish species, and even those species-specific characters that do not overlap are separated by very small margins. The narrow delineation in morphologic and meristic characters currently used to distinguish these three taxa presumes little intraspecific variation in populations both within and between systems. The strong evidence of hybridization in this suite of fishes further complicates species-specific determination. (Brandenburg et al. 2015:iv)

No river basin in North America is known to contain a monophyletic group of species that cannot be distinguished from one another morphologically. If populations of Gila in the lower Colorado River basin are an exception, this should be evident in the analysis of genetic data showing lineage sorting. However, the genetic data do not support recognition of more than one species. Genetic analyses of Gila from the lower Colorado River basin have been completed using mitochrondrial DNA (Gerber et al. 2001; Schwemm 2006; Schönhuth et al. 2012; Schönhuth et al. 2014), nuclear DNA (Schwemm 2006; Schönhuth et al. 2012; Schönhuth et al. 2014), and microsatellites (Dowling et al. 2015). As noted by Dowling et al. (2015), none of these studies found genetic markers that distinguish the three nominal species in the complex. Studies have sometimes concluded otherwise—that populations represent more than one species, but always with caveats on taxonomic conclusions and invoking scenarios of hybridization—including hybrid origin of species.

In our opinion, no morphological or genetic data define populations that have been referred to as the G. robusta complex in the lower Colorado River basin as members of more than one species (i.e., as populations on separate evolutionary trajectories; Simpson 1961; Wiley 1981). Differences that have been described among localities, and that led to the three-species hypothesis of Minckley and DeMarais (2000), are almost certainly the result of past periods of geographic isolation and differentiation, followed by more recent lineage mixing and hybridization. Alternatively, morphological variation may be due to phenotypic plasticity related to variation in stream size, flow, and substrate. Phenotypic plasticity has long been known to occur in fishes (Hubbs 1940), and populations of Gila may represent extreme examples (Schönhuth et al. 2014).

ACKNOWLEDGMENTS
We appreciate comments and suggestions for improving the manuscript from Luke Tornabene, Tyler Chafin, and anonymous reviewers.

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Brandenburg, W. D., J. L. Kennedy, and M. A. Farrington. 2015. Determining the historical distribution of the Gila robusta complex (Gila Chub, Gila intermedia, Headwater Chub, Gila nigra, and Roundtail Chub, Gila robusta) in the Gila River Basin, New Mexico, using morphological analysis. Final report to the New Mexico Department of Game and Fish, Santa Fe.

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Comment to “Taxonomy of Gila in the Lower Colorado River Basin of Arizona and New Mexico”

A publication by Moran et al. (2017) on species of Gila in the Gila River basin appeared after our paper was in press. The goal of their study was to test whether previously used morphological characters could differentiate G. robusta, G. intermedia, and G. nigra from one another, and if not, to discover methods that are better suited for identifying these species based on morphology. The study found that the variables proposed by Rinne (1976) and Minckley and DeMarais (2000) could not be used to identify
individuals to species but that geometric morphometrics could be used to differentiate the species. The study used canonical variate analysis, which requires a priori designation of groups and maximizes differences among these groups. Because of this, and noting the clear effect of geographic location on morphological variation in Gila, the authors concluded that “it is difficult to decide if the three species should be retained as valid, recognized as a single species, or considered as subspecies.” We view this study, while interesting and well conceived, as another that failed to recognize populations of G. robusta as belonging to more than one species.

REFERENCE
Moran, C. J., M. W. O’Neill, J. W. Armbruster, and A. C. Gibb. 2017. Can members of the south-western Gila robusta species complex be distinguished by morphological features? Journal of Fish Biology. 91:302–316.

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