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Analysis of the Ictalurus pricei complex (Teleostei: Ictaluridae) in Northwest Mexico based on mitochondrial DNA.

Ictalurid catfishes in the highlands of northwestern Mexico (states of Sonora, Chihuahua, and Durango) form a taxonomically problematic group (Hendrickson, 1983; Minckley et al., 1986; Minckley and Marsh, 2009). The Yaqui catfish (Ictalurus pricei) once occurred in the Sonora, Yaqui, Mayo, and Fuerte rivers on the Pacific slope and the endorheic Casas Grandes River in Chihuahua (Hendrickson et al., 1981; Miller et al., 2005). However, it apparently persists only in the Yaqui and Fuerte river basins (Varela-Romero et al., 2011) and is considered threatened by the Mexican government (SEMARNAT, 2010). Populations south of the Fuerte River on the Pacific Coast of northwestern Mexico represent an undescribed species (herein called Sinaloa catfish) that differs from I. pricei in cephalic morphology and lower anal-fin ray counts (Varela-Romero et al., 2011). A 2004-2006 survey of historical localities for native catfishes in the Pacific drainages of northwestern Mexico (Varela-Romero et al., 2011) found the Yaqui catfish at only one Yaqui River locality (Tutuaca River) and one Fuerte River location (Batopilas River). The survey team found the Sinaloa catfish only in the Sinaloa, Culiacan, and San Lorenzo river basins. In this paper, we use fish specimens from that survey in order to test the hypothesis from morphological appearance (Varela-Romero et al., 2011) that the Sinaloa catfish can be treated as a member of the I. pricei complex.

We examined mitochondrial cytochrome oxidase subunit I (COI) in Yaqui catfish from the Yaqui River (n = 1) and the Fuerte River (n = 1) and the Sinaloa catfish from the Culiacan (n = 2) and San Lorenzo (n = 1) basins (Fig. 1; Table 1). The tissues that we used were fin clips preserved in [greater than or equal to] 95% ethanol at the time of capture. We fixed the remainder of each specimen in 10% formalin and later transferred it to 70% ethanol for deposition as vouchers in the Native Fish Collection of the Departamento de Investigaciones Cientificas y Tecnologicas de la Universidad de Sonora.

We extracted genomic DNA with the QIAamp DNA Mini Kit from QIAGEN (Venlo, Netherlands). We amplified the COI gene by using polymerase chain reaction (PCR) primers tRNATyrF and tRNASerR (Waldbieser et al., 2003). We performed the amplification with 10 pmol of each primer and approximately 200 ng of genomic DNA in a total volume of 12.5 [micro]l using PuReTaq Ready-to-Go PCR beads (GE Healthcare, Little Chalfont, United Kingdom). The PCR beads contain 2.25 units of puReTaq DNA polymerase, 100 [micro]M of each dNTP in 10 mM Tris-HCl (pH 9.0), 50 mM KCl, and 1.5 mM Mg[Cl.sub.2] when used in a total volume of 25 pl. Amplification employed the following conditions: 94[degrees]C for 5 min followed by 34 cycles of 94[degrees]C for 50 s, 55[degrees]C for 50 s, and 72[degrees]C for 3 min, and finally one cycle of 7 min at 72[degrees]C. The PCR products were sent to Macrogen, Inc. (Seoul, Korea) for purification and bidirectional sequencing with the primers used in the PCR reactions.

We edited the COI sequences to a size of 651 bp and deposited them in GenBank. For the phylogenetic analysis, the ingroup included one haplotype from the mitochondrially rather homogeneous species (McClure-Baker et al., 2010) wolf catfish (Ictalurus lupus; GenBank accession number JN026911), and three from channel catfish (Ictalurus punctatus; NC003489, JF292358, JF292388). We used two haplotypes from blue catfish (Ictalurus furcatus; EU752098, JF292374) as the outgroup (Lundberg, 1992). We translated the sequences using the online software Expasy Translate (http://web.expasy.org/translate/); alignment with BLASTP (Altschul et al., 1990) conformed to a fish mitochondrial COI gene frame.

We assessed phylogenetic relationships with neighborjoining, maximum parsimony, and maximum likelihood (ML). We set neighbor-joining analyses using Kimura's twoparameter model. For maximum parsimony we used PAUP* (Swofford, 2002) in a heuristic search with tree bisection reconnection branch swapping. We estimated nodal support by nonparametric bootstrapping with 1,000 pseudoreplicates and 10 random addition sequences. We used ModelTest 3.6 to choose the most appropriate substitution model (Posada and Crandall, 1998) and incorporated this model (Generalised time-reversible[GTR] + G + I) in the maximum likelihood heuristic search provided by PAUP*. We input the resulting maximum likelihood tree and the initial tree search settings into PHYML (Guindon and Gascuel, 2003) for a bootstrap analysis (1,000 pseudoreplicates) of nodal support.

Sequence divergence among the three Sinaloa catfish haplotypes ranged from 0.1% to 0.9% (mean = 0.6%) and that between the two Yaqui catfish haplotypes was 0.9%. Mean divergence between the two groups of haplotypes was 1.3%. In contrast, these five sequences averaged 2.8% divergent from I. lupus (range = 2.6-3.1%) and 6.3% from I. punctatus (range = 6.6-7.7%).

The maximum parsimony analysis produced three equally parsimonious trees (not shown) that were consistent with the maximum likelihood tree (Fig. 2). With both approaches, I. lupus was resolved as sister to a clade comprising the Sinaloa and Yaqui catfishes. We found no consistent support for reciprocal monophyly between the Yaqui and Sinaloa catfishes, but this possibility was not rejected by the analysis. With maximum likelihood, the two forms appeared reciprocally monophyletic in the optimal tree and the monophyly of the Sinaloa catfish received bootstrap support (81%); there was also bootstrap support (77%) for the monophyly of I. pricei. In contrast, maximum parsimony supported monophyly for the Yaqui catfish (98% bootstrap support), but did not resolve relationships of the three Sinaloa catfish haplotypes. This lack of consistency likely is a result of the short (651-bp) sequence examined. A full understanding of the I. pricei complex will require additional sequence information, including nuclear genes, and more thorough sampling of Ictalurus from Mexico. Nonetheless, this analysis provides the first phylogenetic support for recognition of the I. pricei complex and the first evidence of a possible sister relationship with I. lupus, a species endemic to the Rio Grande and drainages of northeastern Mexico.

We thank S. Sanchez-Gonzales, J. E. Brooks, and N. Smith for field assistance. Comments of J. Lundberg and one anonymous reviewer improved the manuscript. M. Castarieda-Rivera was supported by a fellowship from Consejo Nacional de Ciencia y Tecnologia. This work was funded by Consejo Nacional de Ciencia y Tecnologia. Permit for collection issued by Secretaria de Agricultura, Ganaderia, Desarrollo Rural, Pesca y Alimentacion, Permiso de Pesca de Fomento DGO-PA.03947.250406.1606.

LITERATURE CITED

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Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52:696-704.

Hendrickson, D. A. 1983. Distribution records of native and exotic fishes in the Pacific drainages of northern Mexico. Journal of the Arizona-Nevada Academy of Science 18:33-38.

Hendrickson, D. A., W. L. Minckley, R. R. Miller, D. J. Siebert, and P. H. Minckley. 1981. Fishes of the Rio Yaqui Basin, Mexico and United States. Journal of the Arizona-Nevada Academy of Science 15:65-106.

Lundberg, J. G. 1992. The phylogeny of ictalurid catfishes: a synthesis of recent work. Pages 392-420 in Systematics, historical ecology and North American freshwater fishes (R. L. Mayden, editor). Stanford University Press, Redwood City, California.

McClure-Baker, S. A., A. A. Echelle, R. A. Van Den Bussche, A. F. Echelle, D. A. Hendrickson, and G. P. Garrett. 2010. Genetic status of headwater catfish in Texas and New Mexico: a perspective from mtDNA and morphology. Transactions of the American Fisheries Society 139:1780-1791.

Miller. R. R., W. L. Minckley, and S. Norris. 2005. Freshwater fishes of Mexico. University of Chicago Press, Chicago, illinois.

Minckley, W. L., and P. C. Marsh. 2009. Inland fishes of the greater Southwest: chronicle of a vanishing biota. University of Arizona Press, Tucson.

Minckley, W. L., D. A. Hendrickson, and C. E. Bond. 1986. Geography of western North American freshwater fishes; description and relations to intracontinental tectonism. Pages 519-613 in The zoogeography of North American freshwater fishes (C. H. Hocutt and E. O. Wiley, editors). John Wiley and Sons, New York.

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[SEMARNAT] Secretaria de Medio Ambiente y Recursos Naturales. 2010. Norma Oficial Mexicana NOM-059-2010. Proteccion ambiental-Especies nativas de Mexico de flora y fauna silvestres-Categorias de riesgo y especificaciones para su inclusion, exclusion o cambio-Lista de especies en riesgo. Diario Oficial, 30 de diciembre del 2010:1-78.

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Varela-Romero. A., D. A. Hendrickson, G. Yepiz-Plascencia, J. E. Brooks, and D. A. Neely. 2011. Status of the Yaqui catfish (Ictalurus pricei) in the United States and northwestern Mexico. Southwestern Naturalist 56:278-286.

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Submitted 13 January 2014.

Acceptance recommended by Associate Editor, Robert J. Edwards, 27 July 2014.

Melissa Castaneda-Rivera, Jose M. Grijalva-Chon, Luis E. Gutierrez-Millan, Gorgonio ruiz-campos, and Alejandro Varela- Romero *

Departamento de Investigaciones Cientificas y Tecnologicas de la Universidad de Sonora, P.O. Box 1819, Hermosillo, Sonora 83000, Mexico (MCR, JMGC, LEGM, AVR)

Universidad Autonoma de Baja California, Facultad de Ciencias, Ensenada, Baja California 22860, Mexico (GRC)

* Correspondent: avarela@guayacan.uson.mx

Table 1--Collection localities, GenBank accession numbers for the
cytochrome oxidase subunit 1 sequences, and catalog numbers for
voucher specimens of Ictalurus from northwestern Mexico. Locality
numbers as in Fig. 1.

Species              Locality         Haplotype/     Catalog
                                       accession    number (a)
                                        number

Ictalurus sp.   1. El Rodeo Creek     Haplotype 1   USON 01115
                upstream of           KJ019216
                El Rodeo              Haplotype 2
                                      KJ019217
Ictalurus sp.   2. San Lorenzo        Haplotype 3   USON 01120
                River N of El         KJ019218
                Igualamo

Ictalurus       3. Batopilas River,   KF536995      USON 01050
pricei          15 km E of
                Batopilas

Ictalurus       4. Tutuaca River,     KF536996      USON 01183
pricei          5 km downstream
                of El Nogal Ranch

Species               Lat/long

Ictalurus sp.   24[degrees]54.677'N,
                106[degrees]46.941'W

Ictalurus sp.   24[degrees]41.983'N,
                106[degrees]33.233'W

Ictalurus       27[degrees]05.923'N,
pricei          107[degrees]40.773'W

Ictalurus       28[degrees]34.733'N,
pricei          108[degrees]23.140'W

(a) USON = Native Fish Collection of the Departamento de
Investigaciones Cientificas y Tecnologicas de la Universidad de
Sonora.
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Author:Castaneda-Rivera, Melissa; Grijalva-Chon, Jose M.; Gutierrez-Millan, Luis E.; Ruiz-Campos, Gorgonio;
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1MEX
Date:Sep 1, 2014
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