Phylogenetics of Scaphirhynchus Based on Mitochondrial DNA Sequences

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Transactions of the American Fisheries Society 130:359–366, 2001 q Copyright by the American Fisheries Society 2001

Phylogenetics of Scaphirhynchus Based on Mitochondrial DNA Sequences ANDREW M. SIMONS* Department of Fisheries and Wildlife and James Ford Bell Museum of Natural History, University of Minnesota, 1980 Folwell Avenue, St. Paul, Minnesota 55108, USA

ROBERT M. WOOD Department of Biology, Saint Louis University, 3507 Laclede, St. Louis, Missouri 63103, USA

LUCIE S. HEATH, BERNARD R. KUHAJDA,

AND

RICHARD L. MAYDEN

Department of Biological Sciences, University of Alabama, Box 870345, Tuscaloosa, Alabama 34587, USA Abstract.—Species delineation and taxonomy within the sturgeon genus Scaphirhynchus is controversial. This issue is made more complex by political issues regarding the Alabama sturgeon S. suttkusi and potential hybridization between sympatric shovelnose sturgeon S. platorynchus and pallid sturgeon S. albus. We investigated phylogenetic relationships among species of Scaphirhynchus based on nucleotide sequences for two mitochondrial loci, cytochrome b and the control region (D-loop). White sturgeon Acipenser transmontanus and green sturgeon A. medirostris were used as outgroups. Phylogenetic analyses did not recover monophyletic shovelnose or pallid sturgeon; however, some populations of pallid sturgeon were resolved as sister to the Alabama sturgeon, and one specimen of shovelnose sturgeon was consistently resolved as the sister to all other ingroup taxa. The hierarchical pattern of relationships produced by analysis of mitochondrial DNA is not consistent with that produced by morphological data. It is consistent with the hypothesis of a low rate of evolution of these genes in Scaphirhynchus and reflects recent hybridization between shovelnose and pallid sturgeon, probably due to habitat degradation.

The genus Scaphirhynchus (Acipenseridae) contains three species: pallid sturgeon Scaphirhynchus albus, shovelnose sturgeon Scaphirhynchus platorynchus, and Alabama sturgeon Scaphirhynchus suttkusi (Williams and Clemmer, 1991). These species are endemic to free-flowing rivers of central and eastern North America. Historically common, all three have declined in abundance as these rivers have been impounded or otherwise modified. Pallid sturgeon occur in main channels of the middle and lower Mississippi River downstream of St. Louis and throughout the Missouri River, including the Yellowstone River (Lee 1980a). Shovelnose sturgeon have been recorded throughout much of the Mississippi River basin and the Rio Grande River (Lee 1980b). Alabama sturgeon are endemic to portions of the Mobile River basin (Burke and Ramsey 1995). The Alabama sturgeon is allopatric to the shovelnose and pallid sturgeon, whereas the pallid and shovelnose sturgeon are sympatric over a large portion of their ranges (Lee

* Corresponding author: [email protected] Received September 13, 2000; accepted October 13, 2000

1980a; b; Carlson et al. 1985). The range and abundance of the shovelnose sturgeon has decreased substantially (Keenlyne 1997), although they may be locally common. The pallid and Alabama sturgeon are in danger of extinction (Burke and Ramsey 1995; Mayden and Kuhajda 1997a; 1997b), and both are listed as endangered by the U.S. Fish and Wildlife Service (Federal Register 55 [September 6, 1990]: 36641–36647, Federal Register 65 [May 5, 2000]: 26439–26461). Decreases in abundances and ranges of these species are attributed to their riverine habitats being modified, including dams for power generation, flood control, and navigation (Carlson et al. 1985; Keenlyne et al. 1994; Burke and Ramsey 1995). Members of Scaphirhynchus form a monophyletic group, and together with species of the Central Asian genus Pseudoscaphirhynchus, form a monophyletic subfamily Scaphirhynchinae (Mayden and Kuhajda 1996; Findeis 1997). The taxonomy of Scaphirhynchus was reviewed by Bailey and Cross (1954), Williams and Clemmer (1991), and Mayden and Kuhajda (1996). Taxonomy and species delineation within Scaphirhynchus, particularly with respect to the Alabama sturgeon, has

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become controversial, prompting an interest in systematics by politicians and professional lobbyists. Although morphologically distinct, no differences between pallid and shovelnose sturgeon were found in an analysis of allozyme data (Phelps and Allendorf 1983). Furthermore, shovelnose and Alabama sturgeon are superficially very similar and were long considered to be conspecific. Recent work (Williams and Clemmer 1991; Mayden and Kuhajda 1996) provided ample morphological evidence for recognition of three extant species within Scaphirhynchus. Phylogenetic analysis of morphological characters indicated that the pallid sturgeon is sister to the Alabama sturgeon and shovelnose sturgeon (Mayden and Kuhajda 1996). Identification of sturgeons may be challenging. Small specimens (,300 mm standard length) of pallid sturgeon and shovelnose sturgeon can be difficult to identify (Bailey and Cross 1954; Williams and Clemmer 1991; Mayden and Kuhajda 1996). These apparently share a primitive (plesiomorphic) morphology; diagnosable morphological characteristics may only appear late in ontogeny because of allometric growth (see Figure 2 in Bemis et al. 1997). Paedomorphosis appears to be an important factor in the evolution of Acipenseriformes, in general, delayed ossification of endochondral elements being reported in several taxa (Grande and Bemis 1991; Bemis et al. 1997). Potential hybridization in habitats where pallid and shovelnose sturgeon are sympatric may also hinder identification (Carlson et al. 1985; Keenlyne et al. 1994). Putative hybrids have been reported relatively recently. Hybridization is thought to be a result of development of flood control and navigational modifications to the Missouri and lower Mississippi rivers, as well as construction of reservoirs in these systems (Carlson et al. 1985; Keenlyne et al. 1994). These modifications changed flow characteristics of these rivers so that natural spawning habitats for sturgeon are limited, resulting in depressed recruitment for both species. River modifications may also have led to a breakdown in reproductive isolating mechanisms between pallid and shovelnose sturgeon. An examination of allozyme variation at 37 loci in pallid and shovelnose sturgeon demonstrated little or no genetic divergence (Phelps and Allendorf 1983). That study raised the possibility that lack of genetic divergence may be due to recent speciation rather than hybridization. If this hypothesis is correct, then rapid morphological divergence has occurred unaccompanied by genetic divergence at the loci examined.

Carlson et al. (1985) used the criteria of Bailey and Cross (1954) to identify sturgeon at 12 stations in the Mississippi and Missouri rivers in Missouri. Putative hybrids were identified based on intermediacy of characters or inconsistency of character suites. Hybrids were identified from four sites. At all sites where hybrids were identified they were as common as pallid sturgeons. Keenlyne et al. (1994) presented morphometric comparisons between shovelnose sturgeon and pallid sturgeon at three areas in the upper Missouri River in Montana and South Dakota. They examined more specimens than previous authors and found overlap in supposedly diagnostic measures between species in each area. Most specimens could be identified as either pallid sturgeon or shovelnose sturgeon but putative hybrids were identified from Lake Sharpe, South Dakota (Keenlyne et al. 1994). Even when these individuals were excluded from analyses, diagnostic measures proposed by Bailey and Cross (1954) did not hold (Keenlyne et al. 1994). These findings cast doubt on identification of hybrids by Carlson et al. (1985). Controversy continues over identification of hybrid sturgeon based on morphological criteria. There are no indexes that allow unambiguous identification of hybrids between shovelnose sturgeon and pallid sturgeon (B. R. Kuhajda, unpublished data). This controversy led us to examine these taxa using molecular rather than morphological data. We had three objectives for this study: (1) document intra and interspecific variation in mitochondrial DNA (mtDNA), (2) evaluate sister-group relationships within the genus, and (3) determine whether the lack of allozyme variation between pallid and shovelnose sturgeon was due to recent divergence or recent hybridization. Methods Thirteen specimens of Scaphirhynchus and Acipenser were analyzed for mitochondrial DNA sequence variation at both the cytochrome-b gene and the control region (D-loop). These included one green sturgeon A. medirostris, one white sturgeon A. transmontanus, three Alabama sturgeon, four pallid sturgeon, and four shovelnose sturgeon; white sturgeon and green sturgeon were used as outgroups. Shovelnose sturgeon were from the Missouri River in Missouri and South Dakota (see Appendix). Pallid sturgeon were from North Dakota and South Dakota. Field identifications of nonvouchered specimens were made by U.S. Fish and Wildlife Service personnel.

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TABLE 1.—Primer sequences used for amplification and sequencing of control region and cytochrome b for the three species of Scaphirhynchus. Primer

Sequence Control Region

Amplification Primers L16615 H1144 Sequencing Primers L156 H866 L195 H905

59 cac cct taa ctc cca aag cta aga ttc 39 59 cct cac agg aat gcg gag act tgc 39 59 59 59 59

ctc tat gtg aac taa cac ga 39 ata taa gac cgt cag cgt aa 39 tgt agt aag agc cga aca t 39 tcg atg aca agt cag tcc tg 39 Cytochrome b

Amplification Primers L14724 H15915-stur Sequencing Primers L330 L646 L796 H820 a b

59 gtg act tga aaa acc acc gtt g 39a 59 cct tcg atc ttc ggt tta caa gac 39b 59 59 59 59

aga aac ctg aaa cat cgg agt 39 gac aaa gta aca ttc cac cca ta 39 cca cac atc aaa ccc gaa tg 39 agt atc att cgg gtt tga tgt g 39

Schmidt and Gold (1993). Modified from Schmidt and Gold (1993).

We used QIAGEN QIamp tissue kit (catalog number 29304) to extract genomic DNA. From these genomic extractions, the control region and cytochrome b were amplified with Tfl DNA polymerase (Epicentre Products, catalog number F10250) under conditions recommended by the manufacturer. Single-stranded DNA amplification (Gyllensten and Erlich 1988) followed the initial amplifications. Single-stranded amplification products were purified in Millipore filter units (Millipore Ultrafree MC polysulfone 30,000 NMWL, catalog number UFC3TTK00). Sequenase 2.0 (U.S. Biochemical, catalog number UF3TTK00) was used in sequencing reactions following manufacturer’s instructions. Amplification and sequencing primers are listed in Table 1. Resulting termination products were electrophoresed on 8% Long Ranger acrylamide gels (AT Biochem, catalog number 210) and visualized on Kodak BioMax film (catalog number 871 5187). Sequences have been deposited in the GenBank database under accession numbers U43697, U43740U43744, U43897, U55994, U56983-U56988, AF184105-AF184108. A total of 1,137 bases of cytochrome b and 829 bases of the control region were sequenced for each included specimen. Cytochrome-b sequences were aligned by eye. Control-region sequences, which are highly variable and often exhibit intraspecific variation, were machine-aligned using CLUSTAL W (Thompson et al. 1994). The machine alignment was subsequently adjusted by eye

(aligned sequences are available from the senior author). Saturation, loss of phylogenetic information due to repeated changes at a particular nucleotide position, was assessed graphically. All pairwise comparisons of transitions and transversions versus percent divergence were plotted for cytochrome b and the control region. Nonlinear change of either transitions or transversions versus divergence indicates saturation (Lydeard and Roe 1997). Phylogenetic analyses were performed on cytochrome b and the control region separately and together (entire data set). The control region is noncoding and presumably subject to different evolutionary constraints than the cytochrome-b gene. Thus, combined analyses may produce misleading results, particularly in a maximum likelihood analysis. Therefore, three data partitions were examined in each analysis: (1) control region only, (2) cytochrome b only, and (3) the entire data set. Phylogenetic trees were generated using PAUP 4.0b4a (Swofford 1998). Analyses were performed under three different optimality criteria: parsimony, distance, and likelihood. Parsimony analyses were performed using branch-and-bound searches on the control region, cytochrome b, and the entire data set. Distance analyses were performed with heuristic searches on the control region, cytochrome b, and the entire data set using the criterion of minimum evolution with LogDet/paralinear pairwise distances (Lockhart et al. 1994). Searches used tree

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TABLE 2.—Matrix of comparisons of the three species of Scaphirhynchus for absolute base-pair variation observed in cytochrome-b (upper) and control-region genes (lower). S. suttkusi

S. platorynchus

S. albus

Fish number

A1

A2

A3

SD1

SD2

H1

H2

P1

P2

P3

P4

A1 A2 A3 SD1 SD2 H1 H2 P1 P2 P3 P4

— 0 0 1 4 9 3 10 10 1 1

0 — 0 1 4 9 3 10 10 1 1

0 0 — 1 4 9 3 10 10 1 1

0 0 0 — 3 8 2 9 9 0 0

1 1 1 1 — 11 5 12 12 3 3

2 2 2 2 3 — 10 17 17 8 8

1 1 1 1 2 3 — 11 11 2 2

4 4 4 4 5 6 3 — 0 9 9

4 4 4 4 5 6 3 0 — 9 9

0 0 0 0 1 2 1 4 4 — 0

0 0 0 0 1 2 1 4 4 0 —

bisection and reconnection (TBR) branch swapping. Starting trees were obtained by stepwise addition with 100 random addition sequence replicates. Likelihood analyses require specification of a particular model of sequence evolution. For each data-set partition we tested 40 models with Modeltest (Posada and Crandall 1998). Models were chosen based on nested likelihood ratio tests (Huelsenbeck and Crandall 1997) using the standard Bonferroni correction (Rice 1989) at a 5 0.01. Models chosen were HKY 1 G for the control region, HKY 1 G for cytochrome b, and TrN 1 G for the entire data set. Heuristic searches were performed on each data partition under the appropriate model. Variables such as rate matrices, transition/transversion (TI/TV) ratio, and shape parameter of gamma distributions were estimated from the data. Nonparametric bootstrap analyses were performed under parsimony, distance, and likelihood criteria (Felsenstein 1985). For parsimony and distance 1,000 pseudoreplicates were performed with options maxtrees 5 500 and TBR branch swapping. Likelihood analyses are computationally intensive; to complete bootstrap analysis in a reasonable amount of time, 100 pseudoreplicates were performed with options of maxtrees 5 500, starting trees obtained with fast stepwise addition, and no branch swapping. Results Variation was limited among included specimens (Table 2). The following individuals were found to have identical haplotypes: A1 5 A2 5 A3, P3 5 P4 5 SD1, and P1 5 P2. The existence of identical haplotypes among individuals P3, P4, and SD1 was a surprise because this group in-

cludes both shovelnose and pallid sturgeon. In general, more inter and intraspecific variation was observed in the control region than in cytochrome b. This pattern was expected because the control region is noncoding and therefore not subject to the same functional constraints as the cytochromeb gene. Cytochrome-b sequences were identical for all Alabama sturgeon, shovelnose sturgeon SD1, and pallid sturgeon P3 and P4. However, 1–10 base pairs differed in control-region sequences and distinguished the Alabama sturgeon from shovelnose and pallid sturgeon. For cytochrome b, shovelnose sturgeon differed from one another by one to three base pairs; no differential variation was observed between Missouri and South Dakota specimens. The same pattern of variation also occurred within shovelnose sturgeon for control-region sequences, but the number of base-pair differences observed between individuals was greater, ranging from 2 to 11. Within pallid sturgeon, specimens P1 and P2 were identical, as were P3 and P4, for both cytochrome-b and control-region sequences. Four base pairs for cytochrome b and nine base pairs for the control region differed between P1 or P2 and P3 or P4. Pallid sturgeon P3 and P4 possess a shovelnose sturgeon haplotype identical to that found in SD1 (Table 2). Pallid sturgeon P1 and P2 are identical but possess more divergent sequences from shovelnose and Alabama sturgeon for both the control region and cytochrome b. Phylogenetic Analyses Pairwise comparisons for the entire data set revealed sequence divergence of 0–18% between all taxa. For control region, sequence divergence ranged from 0% to 30%. For cytochrome b, sequence divergence ranged from 0% to 11%. For the entire Scaphirhynchus data set, sequence di-

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FIGURE 1.—Phylogenetic analysis of five sturgeon species: (A) strict consensus tree of 541 equally parsimonious trees resulting from phylogenetic analysis of the entire data set; (B) strict consensus of 18 trees resulting from distance analysis of entire data set using criterion of minimum evolution with LogDet/paralinear distances; and (C) likelihood tree resulting from analysis of entire data set under TrN 1 G. In all three panels, the numbers above nodes indicated bootstrap support.

vergence ranged from 0% to 1.2% and absolute distance was 0–23 nucleotide changes. We found no evidence of sequence saturation of the mitochondrial genes examined within Scaphirhynchus. The three methods of phylogenetic analysis, parsimony, distance, and maximum likelihood produced largely consistent results across all data partitions. In general, most resolution was produced by the entire data set and cytochrome b provided the least amount of phylogenetic resolution. Parsimony analysis of the entire data set, re-

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sulted in 541 equally parsimonious trees (length[L] 5 403; Figure 1A). Within the ingroup, shovelnose specimen H1 is sister to all other Scaphirhynchus. Remaining taxa were contained in a polytomy consisting of a clade of the three specimens of Alabama sturgeon (A1–A3), a clade of shovelnose specimen H2 sister to two pallid specimens P1 and P2, and remaining pallid sturgeon (P3, P4) and shovelnose sturgeon (SD1, SD2). Branch and bound analysis of cytochrome-b sequences, resulted in a single most parsimonious topology (L 5 140). Within the ingroup, shovelnose sturgeon H1 is sister to all other Scaphirhynchus. This resolution is consistent with analysis of the entire data set. All other Scaphirhynchus formed an unresolved polytomy, except for a clade consisting of a shovelnose sturgeon, H2, sister to pallid sturgeon P1 plus P2. This relationship is consistent with that found in analysis of the entire data set. Analysis of cytochrome b did not resolve the Alabama sturgeon as a monophyletic group because this species possessed no autapomorphic characters at this locus. Branch and bound analysis of control-region sequences resulted in 4,683 equally parsimonious trees (L 5 263). Resolution of shovelnose sturgeon H1 as the sister to all other Scaphirhynchus is consistent with analyses of the entire data set and cytochrome b. Control-region sequences do not resolve shovelnose sturgeon H2 as sister to pallid sturgeon P1 plus P2 as found in the entire data set and cytochrome-b analyses; H2 was resolved in a basal polytomy with other shovelnose and pallid sturgeon and independent clades for the Alabama and pallid sturgeon. The Alabama sturgeon is always resolved as a divergent and monophyletic group in analyses of control-region sequences. Character weighting had no effect on the results of parsimony analyses, suggesting little or no saturation of the data. Distance analysis of the entire data set resulted in 18 trees with a score of 0.23167 (Figure 1B). Results were largely consistent with the parsimony analysis, except for placement of shovelnose sturgeon H2 and SD2. The Alabama sturgeon was resolved as monophyletic as were pallid sturgeon P1 and P2. Distance analysis of cytochrome b resulted in 5,130 trees. The strict consensus of these trees is consistent with parsimony analysis of cytochrome b. Distance analysis of the control-region sequence resulted in 18 trees. Results were the same as distance analysis of the entire data set, except for placement of shovelnose sturgeon H2 as sister to Alabama sturgeon.

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Likelihood analysis of the entire data set under TrN 1 G resulted in an ingroup topology identical to parsimony analysis (Figure 1C). Analysis of cytochrome b under HKY 1 G produced a similar result, except that Alabama sturgeon were not resolved as monophyletic. Analysis of control region under HKY 1 G produced a topology similar to likelihood analysis of the entire data set, except that shovelnose sturgeon H2 was not resolved as sister to pallid sturgeon P1 and P2 but instead is in a polytomy with pallid sturgeon P3 and P4 and shovelnose sturgeon SD1 and SD2. Discussion Analyses of sequence variation in cytochrome b and the control region for the three species of Scaphirhynchus revealed low levels of sequence divergence among these species. This is consistent with the negligible amount of allozyme variation between shovelnose sturgeon and pallid sturgeon (Phelps and Allendorf 1983). We interpret the overall similarity of haplotypes of Scaphirhynchus to be the result of a low rate of evolution at these loci. Low rates of molecular evolution in Acipenseridae were reported by Birstein et al. (1997), although extensive variation has been reported for white sturgeon (Brown et al. 1993). The isolation of the Alabama sturgeon in the Mobile basin from the shovelnose sturgeon is consistent with biogeographical patterns observed in many other groups of North American fishes (Wiley and Mayden 1985; Mayden 1988). The isolation of the Mobile basin from other drainage systems is an old event (1–5 million years ago) yet sequence divergence between Alabama sturgeon and shovelnose sturgeon is low. These low evolutionary rates result in conserved mitochondrial haplotypes that are difficult to use in species delineation. Phelps and Allendorf (1983) raised the possibility that the lack of genetic divergence they observed between shovelnose and pallid sturgeon may be due to recent speciation accompanied by rapid morphological change. This contrasts with the alternative and more commonly accepted hypothesis that the lack of genetic differences are due to hybridization induced by habitat change (Carlson et al. 1985; Keenlyne et al. 1994). The data presented by Phelps and Allendorf (1983) did not allow them to distinguish between these alternatives. Mitochondrial loci, unlike the nuclear loci studied by Phelps and Allendorf (1983) are maternally inherited and haploid. Therefore, the effective population size of mitochondrial loci is one-fourth that of nuclear genes (Moore 1995). The combination of low effective

population size and the relatively higher rate of evolution at mitochondrial loci suggests that coalescence of mitochondrial lineages should occur much more rapidly than with nuclear loci (Moore 1995). As a result, a mitochondrial gene tree should track a species tree better than a nuclear gene tree. If pallid sturgeon and shovelnose sturgeon have recently diverged, mitochondrial loci should produce a topology congruent with morphological characteristics, and any recoverable hierarchical structure should resolve shovelnose sturgeon and pallid sturgeon as sister taxa with respect to the Alabama sturgeon. If pallid sturgeon and shovelnose sturgeon have recently hybridized, then mitochondrial loci would not be expected to produce a hierarchy congruent with morphology because mitochondrial genotypes would have been exchanged between the two morphotypes. Resolved mitochondrial gene trees would be expected to be inconsistent with trees based on morphology. The presence of a hierarchical pattern in our analyses is consistent with the hybridization hypothesis. Although we can reconstruct a hierarchical pattern, it is not consistent with that supported by morphological data of Mayden and Kuhajda (1996). They identified a monophyletic pallid sturgeon sister to a clade containing the shovelnose sturgeon and Alabama sturgeon. In addition, the phylogenetic pattern is not consistent with the recent speciation hypothesis because the Alabama sturgeon is derived within Scaphirhynchus. We conclude that the lack of genetic diversity among the three species of Scaphirhynchus is due to a slow rate of molecular evolution and recent hybridization between shovelnose and pallid sturgeons. We predict that if hybridization continues, haplotype diversity among these taxa will be lost. Despite genetic similarities shown here, given the morphological differences among these taxa, we should continue to recognize and manage them as distinct evolutionary species. Acknowledgments We thank S. Cook, F. Harders, P. Kilpatrick, N. Nichols, W. Reeves, (Alabama Department of Conservation and Natural Resources), M. Dryer, S. Krentz, J. Lundin, F. Parauka, J. Stewart (U.S. Fish and Wildlife Service), and K. Graham (Missouri Department of Conservation) for assisting us in obtaining specimens and tissues of Scaphirhynchus. B. Parker and C. Foster provided tissues of both green and white sturgeon caught by Oregon fishermen. USFWS provided the necessary permits for possession of tissues and specimens of pallid sturgeon. Partial funding for this study was pro-

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freshwater fishes. North Carolina State Museum of Natural History, Raleigh, North Carolina. Lee, D. S. 1980b. Scaphirhynchus platorynchus (Rafinesque) shovelnose sturgeon. Page 44 in D. S. Lee, C. R. Gilbert, C. H. Hocutt, R. E. Jenkins, D. E. McAllister, and J. R. Stauffer, editors. Atlas of North American freshwater fishes. North Carolina State Museum of Natural History, Raleigh, North Carolina. Lockhart, P. J., M. A. Steel, M. D. Hendy, and D. Penny. 1994. Recovering evolutionary trees under a more realistic model of sequence evolution. Molecular Biology and Evolution 11:605–612. Lydeard, C., and K. J. Roe. 1997. The phylogenetic utility of the mitochondrial cytochrome b gene for inferring relationships among actinopterygian fishes. Pages 285–303 in T. D. Kocher and C. A. Stepien, editors. Molecular Systematics of Fishes. Academic Press, San Diego, California. Mayden, R. L. 1988. Vicariance biogeography, parsimony, and evolution in North American freshwater fishes. Systematic Zoology 37:329–355. Mayden, R. L., and B. R. Kuhajda. 1996. Systematics, taxonomy, and conservation status of the endangered Alabama sturgeon, Scaphirhynchus suttkusi Williams and Clemmer (Actinopterygii, Acipenseridae). Copeia 1996:241–273. Mayden, R. L., and B. R. Kuhajda. 1997a. Threatened fishes of the world: Scaphirhynchus suttkusi Williams and Clemmer, 1991 (Acipenseridae). Environmental Biology of Fishes 48:418–419. Mayden, R. L., and B. R. Kuhajda. 1997. b. Threatened fishes of the world: Scaphirhynchus albus (Forbes and Richardson, 1905) (Acipenseridae). Environmental Biology of Fishes 48:420–421. Moore, W. S. 1995. Inferring phylogenies from mtDNA variation: Mitochondrial-gene trees versus nucleargene trees. Evolution 49:718–726. Phelps, S. R., and F. W. Allendorf. 1983. Genetic identity of pallid and shovelnose sturgeon (Scaphirhynchus albus and S. platorynchus). Copeia 1983:696–700. Posada, D., and K. A. Crandall. 1998. MODELTEST: Testing the model of DNA substitution. Bioinformatics 14:817–818. Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43:223–225. Schmidt, T. R., and J. R. Gold. 1993. Complete sequence of the mitochondrial cytochrome b gene in the cherryfin shiner, Lythrurus roseipinnis (Teleostei: Cyprinidae). Copeia 1993:880–883. Swofford, D. L. 1998. ‘‘PAUP’’: Phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer Associates, Sutherland, Massachusetts. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22:4673–4680. Wiley, E. O., and R. L. Mayden. 1985. Species and speciation in phylogenetic systematics, with examples from the North American fish fauna. Annals of the Missouri Botanical Garden 72:596–635. Williams, J. D., and G. H. Clemmer. 1991. Scaphirhynchus suttkusi, a new sturgeon from the Mobile Basin of Alabama and Mississippi. Bulletin of the Alabama Museum of Natural History 10:17–31.

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Appendix: Specimens Examined TABLE A.1.—Species, specimen, and collection information (locality, state, date, and passive integrated transponder [PIT; applied by U.S. Fish and Wildlife Service] tag numbers) for sturgeon examined in this study; rkm 5 river kilometer (from the river’s mouth). Species and (specimen number) Acipenser medirostris (G-5); A. transmontanus (W-2): Scaphirhynchus albus (P-1) S. albus (P-2) S. albus (P-3) S. albus (P-4) S. platorynchus (H-1 and H-2)

S. platorynchus (SD-1) S. platorynchus (SD-2) S. suttkusi (A-1)

S. suttkusi (A-2)

S. suttkusi (A-3)

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Collection information Lower Columbia River and estuaries between Becon Rock and Columbia River, Astoria County, Oregon Lake Sharpe (Missouri River), Huges County, South Dakota (tube 58-2A, PIT tag 7F7D43582A) Missouri River, Williams County, North Dakota; 11 September 1993 (tube 39-80, PIT tag 7F7D43086C) Missouri River, Williams County, North Dakota; 10 July 1992 (tube3C-61, PIT tag 7F7D373C61) Missouri River, Williams County, North Dakota; 9 September 1993 (tube 37-11, PIT tag 7FTE6B3711) Missouri River (rkm 249.4) near Hartsburg, Boone County, Missouri; 14 December 1994; 11UAIC 11343.01 Missouri River, Hughes County, South Dakota; 16 March 1995 Missouri River, Hughes County, South Dakota; 16 March 1995 Alabama River at rkm 94.6 slightly upstream of Cedar Creek (in Clarke County), Monroe County, Alabama; 2 December 1993; UAIC 10885.01 Alabama River at rkm 92.4–94.3, just below eddy in current, Monroe County, Alabama; 19 May 1995; UAIC 11158.01 Alabama River near Claiborne Lock and Dam, Monroe County, Alabama; 18 April 1995.

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