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Based on Mitochondrial DNA Sequences Jeannette Krieger, Paul A

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Based on Mitochondrial DNA Sequences Jeannette Krieger, Paul A Molecular Phylogenetics and Evolution Vol. 16, No. 1, July, pp. 64–72, 2000 doi:10.1006/mpev.1999.0743, available online at http://www.idealibrary.com on Phylogenetic Relationships of the North American Sturgeons (Order Acipenseriformes) Based on Mitochondrial DNA Sequences Jeannette Krieger, Paul A. Fuerst, and Ted M. Cavender* Department of Molecular Genetics and *Department of Evolution, Ecology and Organismal Biology, The Ohio State University, Columbus, Ohio 43210 Received July 16, 1999; revised October 18, 1999 grouped within one family (Birstein, 1993). These fish The evolutionary relationships of the extant species are anadromous, diadromous, or potamodromous, with within the order Acipenseriformes are not well under- a North American and Eurasian distribution (Bemis stood. Nucleotide sequences of four mitochondrial and Kynard, 1997). In addition, sturgeon and paddle- genes (12S rRNA, COII, tRNAPhe, and tRNAAsp genes) in fish have long life spans, the potential to grow very North American sturgeon and paddlefish were exam- large in size, and slow maturation, as females often ined to reconstruct a phylogeny. Analysis of the com- require 10 to 20 years before reproduction in nature. bined gene sequences suggests a basal placement of Widely exploited for caviar and meat, their popularity the paddlefish with regard to the sturgeons. Nucleo- as a food source in a number of countries has resulted tide sequences of all four genes for the three Scaphi- in frequent overfishing. Recently, the population sizes rhynchus species were identical. The position of of many acipenseriform species have decreased to the Scaphirhynchus based on our data was uncertain. Within the genus Acipenser, the two Acipenser oxyrin- point at which they are threatened or endangered. The chus subspecies were very similar in sequence and decrease can be traced to three major factors: (1) cer- found to be basal to the remaining Acipenser species tain life history characteristics of these fish (slow examined. Based on our data, Acipenser transmonta- sexual maturation, females often reproduce only once nus and Acipenser medirostris were sister taxa, as every few years, and migratory nature); (2) the de- were Acipenser fulvescens and Acipenser brevirostrum. struction of spawning habitat by pollution, dams, or Comparison of our results with hypotheses of stur- other human intervention; and (3) overfishing. geon relationships proposed by previous authors is Sturgeons are of interest evolutionarily for a variety presented. The sequence data presented here are of reasons. The “living fossil” status of the group makes phylogenetically useful and provide a solid founda- them important for understanding vertebrate evolu- tion of genetic information for the North American tion in general (Gardiner, 1984), and the threatened or Acipenseriformes that can be expanded to include endangered status of many of these species indicates Eurasian species to provide a global picture of stur- that there may be a limited time left to study these geon evolution. © 2000 Academic Press organisms. For example, of the 10 species of Acipenseri- Key Words: Acipenseriformes; evolution; mitochon- formes in North America, the IUCN Red List catego- drial DNA; molecular phylogenetics; paddlefish; stur- rizes 6 species as vulnerable, 1 as threatened, and 1 as geon. critically endangered (Birstein et al., 1997a; 1996 IUCN Red List of Threatened Species at the World Conservation Monitoring Centre website: http://www. INTRODUCTION wcmc.org.uk/species/animals/animal_redlist.html). In The order Acipenseriformes is an ancient group of addition, information about the relationships of the fish identifiable from the Jurassic (Grande and Bemis, extant species of sturgeon and paddlefish may be use- 1991), which possess a highly cartilaginous skeleton, a ful in directing conservation efforts toward protecting spiral valve in the gut, a heterocercal tail, and a well maximum genetic diversity of sturgeon species (Moritz, developed rostrum with mouth inferior (Sokolov and 1995). However, the evolutionary relationships are still Berdichevskii, 1989). The group is characterized as not clearly understood (Birstein, 1993), and there is monophyletic based on eight osteological characters limited and sometimes confusing information available described in detail by Bemis et al. (1997). At present, it from morphological characters for elucidating species- consists of approximately 25 extant species of sturgeon level relationships. The need for additional investiga- divided into two subfamilies and four genera and 2 tion of this group by morphological, molecular, and extant species of paddlefish in different genera but other methods has been recently expressed (Bemis et 64 1055-7903/00 $35.00 Copyright © 2000 by Academic Press All rights of reproduction in any form reserved. ACIPENSERIFORM mtDNA PHYLOGENY 65 al., 1997; Findeis, 1997). In particular, regarding the for analysis because they have been shown to be useful North American species, more information about ge- in phylogenetic studies of other groups (Janecek et al., netic differences between the two Acipenser oxyrinchus 1996; Lavergne et al., 1996; Richards and Moore, subspecies and especially among the three species of 1996), and much information is known about the struc- Scaphirhynchus is needed. Evidence of genetic differ- tures and functions of the genes and their products entiation is necessary to firmly establish subspecific or (Brimacombe and Stiege, 1985; Capaldi, 1990; Gutell, specific status for these taxa to ensure protection of 1994). In addition, two transfer RNA gene sequences, maximum acipenseriform diversity within North the tRNA for phenylalanine (tRNAPhe) and the tRNA America. Another idea that has been in question is the for aspartic acid (tRNAAsp), were examined. They were existence of a sister species relationship between the included in the amplified products which contained the North American species Acipenser brevirostrum and mitochondrial 12S rRNA and COII gene sequences. Acipenser fulvescens. Researchers have provided evi- This study examines the relationships among the 10 dence both supporting (Artyukhin, 1995) and refuting extant North American sturgeon and paddlefish spe- (Birstein and Desalle, 1998) a sister species relation- cies by comparing the nucleotide sequences of the 12S ship between them, and Choudhury and Dick (1998) rRNA gene, the COII gene, tRNAPhe gene, and the have proposed a hypothetical scenario explaining the tRNAAsp gene from each species. historical biogeography for these two species that sup- ports a sister species relationship. To try to help resolve these relevant questions in- MATERIALS AND METHODS volving North American species and to add to the in- formation already obtained for these important and Specimens. Tissue samples from each of the North vulnerable fish (Bemis et al., 1997; Wirgin et al., 1997; American acipenseriform species (Mayden et al., 1992) Birstein and DeSalle, 1998), we conducted an exami- were provided by various researchers and fishery nation of the phylogenetic relationships among North workers from throughout the United States. Table 1 American acipenseriform species using molecular data, lists information on the tissue samples. The taxa in- specifically mitochondrial DNA gene sequences. The cluded were Polyodon spathula (North American study has focused on the North American species, not paddlefish), Acipenser fulvescens (lake sturgeon), A. because of an assumption that these species represent brevirostrum (shortnose sturgeon), A. transmontanus a monophyletic group within the Acipenseriformes but (white sturgeon), A. medirostris (green sturgeon), A. rather because our study will shed light on questions oxyrinchus oxyrinchus (Atlantic sturgeon) (Gilbert, which have a predominant or sole emphasis on the 1992), A. oxyrinchus desotoi (Gulf sturgeon), Scaphi- North American sturgeon fauna. rhynchus platorynchus (shovelnose sturgeon), S. albus The 12S ribosomal RNA (rRNA) gene and the cyto- (pallid sturgeon), and S. suttkusi (Alabama sturgeon). chrome c oxidase subunit II (COII) gene were chosen Blood samples were stored in Queen’s lysis buffer TABLE 1 Species Included in This Study Tissue Species name sample Origin of specimen Provider of sample Polyodon spathula Fin snip Hatchery fish—parents from Osage Blind Pony Lake Conservation Area, River Basin Missouri Scaphirhynchus albus Fin snip Hatchery fish—parents from National Biological Services Midwest Mississippi and Missouri Riversa Science Center, Missouri Scaphirhynchus platorynchus Fin snip Missouri River National Biological Services Midwest Science Center, Missouri Scaphirhynchus suttkusi Muscle Alabama River (UAIC 1885.01) University of Alabama at Tuscaloosa Acipenser brevirostrum Barbel Hatchery fish—parents from Bears Bluff National Fish Hatchery, Savannah River South Carolina Acipenser fulvescens Fin snip Wolf River Wisconsin Department of Natural Resources Acipenser medirostris Muscle Klamath River Humboldt State University, California Acipenser oxyrinchus oxyrinchus Fin snip Hudson River Northeast Fishery Center, U.S.F.W.S., Pennsylvania Acipenser oxyrinchus desotoi Blood Hatchery fish—parents from University of Florida Suwannee River Acipenser transmontanus Fin snip Snake River College of Southern Idaho a Male parents were from the Missouri River and female parents were from the Mississippi River. 66 KRIEGER, FUERST, AND CAVENDER (Seutin et al., 1991), whereas the other types of tissue cycles of 1 min at 93°C, 1.5 min at 50°C, and 2.5 min at
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