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Age and Biogeography of Major Clades in Sturgeons and Paddlefishes

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Age and Biogeography of Major Clades in Sturgeons and Paddlefishes Molecular Phylogenetics and Evolution 42 (2007) 854–862 www.elsevier.com/locate/ympev Short communication Age and biogeography of major clades in sturgeons and paddleWshes (Pisces: Acipenseriformes) Zuogang Peng a,1, Arne Ludwig b,1, Dengqiang Wang c, Rui Diogo d, Qiwei Wei c, Shunping He a,¤ a Laboratory of Fish Phylogenetics and Biogeography, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China b Department of Evolutionary Genetics, Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany c Key Laboratory of Freshwater Fish Germplasm Resources and Biotechnology, Ministry of Agriculture of China, Yangtze River Fisheries Research Institute, Chinese Academy of Fisheries Science, Jingzhou 434000, China d Laboratory of Functional and Evolutionary Morphology, University of Liege, B-4000 Liege, Belgium Received 22 January 2006; revised 11 September 2006; accepted 18 September 2006 Available online 27 September 2006 1. Introduction albus, Scaphirhynchus platorynchus, Scaphirhynchus sut- tkusi, Psephurus gladius, and Polyodon spathula) and tet- The order Acipenseriformes includes 25 extant sturgeon raploidy (species with »250 chromosomes including all species and two extant paddleWsh species (e.g., Birstein, taxa with between 220 and 276 chromosomes, e.g., Aci- 1993; Birstein and Bemis, 1997). Sturgeons and paddleWshes penser baerii, Acipenser fulvescens, Acipenser gue- are considered “living fossils”; in fact, although acipenseri- ldenstaedtii, Acipenser medirostris, Acipenser persicus, form Wshes Wrst appeared in the fossil record approximately Acipenser schrenckii, and Acipenser transmontanus) as well 200 Mya, they have seemingly not undergone much mor- as evolutionary octaploidy (species with »500 chromo- phological change since that time (Gardiner, 1984). These somes, e.g., Acipenser mikadoi) (reviewed in Birstein et al., “evolutionary relicts” display markedly disjunction distri- 1997). These Wshes represent an interesting model for butions with a wide distribution in the northern hemisphere studying lineage speciWc genome duplication events. Fur- (e.g., Gardiner, 1984; Bemis et al., 1997). Their unique ben- thermore, polyploidization is believed to be an important thic specializations and conserved morphology, their evolu- evolutionary aspect in animals, as it is in plants (e.g., Sol- tionary age, the variation in their basic diadromous life tis and Soltis, 1999; Le Comber and Smith, 2004; Crow history, and the large public interest due to their near et al., 2006). However, the timing of the polyploid events extinction or critically endangered status, make sturgeons in these acipenseriform Wshes remains uncertain. and paddleWshes interesting groups for molecular evolu- The phylogenetic relationships among extant acipens- tionary studies (e.g., Birstein, 1993; Choudhury and Dick, eriform groups has been the subject of numerous, 1998). detailed works (e.g., Grande and Bemis, 1991; Birstein Moreover, acipenseriform Wshes provide an ideal case and DeSalle, 1998; Ludwig et al., 2001; Robles et al., study for examination of genome duplication events. Mul- 2004). With a robust hypothesis on the relationships tiple levels of ploidy exist among these Wshes since they among these groups being available, it is of much interest include, for instance, diploidy (species with »120 chromo- to date the origin of these groups since this is crucial, in somes including all taxa with between 110 and 130 chro- fact, for clarifying acipenseriform evolution and histori- mosomes, e.g., Acipenser nudiventris, Acipenser cal biogeography. As stated above, sturgeons and padd- oxyrinchus, Acipenser ruthenus, Acipenser stellatus, Aci- leWshes are an interesting group for biogeographical penser sturio, Huso dauricus, Huso huso, Scaphirhynchus analysis: their wide distribution across North America and Eurasia, for example, raises the question on where * Corresponding author. Fax: +86 27 68780071. the centre of origin is, as well as on whether such wide E-mail addresses: [email protected] (Q. Wei), [email protected] (S. He). distribution was mainly due to dispersal, to vicariance, or 1 These authors contributed equally to this work. to a combination of both. 1055-7903/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2006.09.008 Z. Peng et al. / Molecular Phylogenetics and Evolution 42 (2007) 854–862 855 Therefore, the main aim of the present work is precisely PCR products were diluted in sterilized distilled water for to date the origin of the major groups of the order Acipens- subsequent use. eriformes, in order to discuss these and other questions Long PCR products were puriWed with a Cycle-Pure Kit related with the genome duplication events and the biogeo- (Omega) and subsequently used for direct cycle sequencing graphic distribution of these Wshes. with dye-labelled terminators (ABI). Methods of sequenc- ing were the same as above. Initial sequencing primers were 2. Materials and methods the same as those for long PCR, and subsequent sequencing was performed using primers designed with reference to 2.1. Taxon sampling, DNA extraction, long PCR, and previously-determined sequences (primer-walking). We sequencing by primer walking designed 64 sequencing primers (except for long PCR prim- ers; available from ZP upon request) for determining the The Yangtze sturgeon (Acipenser dabryanus), Chinese complete mtDNA sequences of the three acipenseriforms. swordWsh (P. gladius) and Mississippi paddleWsh (P. spath- ula) samples were conservation genetic analysis collections 2.2. Sequence analysis and molecular dating deposited in Yangtze River Institute of Fisheries, Chinese Academy of Fisheries Science. The other samples were DNA sequences were analyzed using the software Laser- retrieved from GenBank (Table 1). Total genomic DNA gene version 5.0 (DNASTAR). Contig assembly was per- was extracted from the muscle tissue using a QIAamp tis- formed with the program Seqman. Multiple alignments sue kit (Qiagen) following the manufacturer’s protocol. The were prepared for two rRNAs and eight protein-coding mitochondrial genome DNAs of the three acipenseriforms genes by using CLUSTAL X version 1.83 (Thompson et al., were ampliWed in its entirety using a long PCR technique 1997) at default settings, excluding 22 tRNAs, ND3, ND4L, (Cheng et al., 1994; Miya and Nishida, 1999). The primers and ATP8, due to their small size (e.g., Peng et al., 2006). designed to amplify the total mitochondrial genome are The CO2 gene was also excluded in our analyses due to its given in Appendix Table S1. Long PCR was done in a PTC- unavailable in alligator gar (Lepisosteus spatula). The 100 programmable thermal controller (MJ Research, nucleotide alignment for ND6 was unreliable due to an USA); reactions were carried out in 25 ul reaction volume unusual substitution pattern (e.g., Yoder and Yang, 2000), containing 2.5 ul 10 X LA PCR buVer II (Takara), 0.8 mM and was thus also removed from the analysis. To avoid bias W dNTPs, 2.5 mM MgCl2, 0.5 um each primer, 0.625 units LA in re ning alignments, ambiguous alignment positions Taq polymerase (Takara) and approximately 20 ng tem- (including beginnings and ends of many protein-coding plate DNA. The thermal cycle proWle was: pre-denatur- genes and rRNA highly variable regions) were excluded by ation at 96 °C for 1 min, and 30 cycles of denaturation at using the GBLOCKS 0.91b (Castresana, 2000) at default 95 °C for 30 s, annealing at 60 °C for 50 s, extension at 72 °C settings. for 3 min, Wnal extension at 72°C for 15 min, and were elec- We have applied two steps for dating the divergence trophoresed on a 0.8% agarose gel (Promega). The long time of sturgeons and paddleWshes. First, we reconstructed Table 1 Seven complete mitochondrial genome sequences of sturgeons and paddleWshes and related taxa plus one shark as outgroup retrieved from GenBank for the Wrst dating analysis Family Species Common name GenBank Accession No. References Heterodontidae H. francisci Horn shark AJ310141 Arnason et al. (2001) Lepidosirenidae Lepidosiren paradoxa South American lungWsh AF302934 Brinkmann et al. (2004) Pelomedusidae Pelomedusa subrufa African side-necked turtle AF039066 Zardoya and Meyer (1998) Bovidae Bos taurus Cow V00654 Anderson et al. (1982) Cercopithecidae Macaca mulatta Rhesus monkey AY612638 Gokey et al. (2004) Hominidae Pan troglodytes Chimpanzee D38113 Hixson and Brown (1986) Hominidae Homo sapiens Human V00662 Anderson et al. (1981) Amiidae A. calva BowWn AB042952 Inoue et al. (2003) Lepisosteidae L. spatula Alligator gar AP004355 Inoue et al. (2003) Lepisosteidae Lepisosteus oculatus Spotted gar AB042861 Inoue et al. (2003) Acipenseridae A. dabryanus Yangtze sturgeon AY510085 This study Acipenseridae Acipenser stellatus Stellate sturgeon AJ585050 Arnason et al. (2004) Acipenseridae Acipenser transmontanus White sturgeon AB042837 Inoue et al. (2003) Acipenseridae H. huso Beluga AY442351 Dunn et al. unpublished Acipenseridae Scaphirhynchus cf. albus Pallid sturgeon AP004354 Inoue et al. (2003) Polyodontidae P. spathula Mississippi paddleWsh AY510086 This study Polyodontidae P. gladius Chinese swordWsh AY571339 This study Osteoglossidae Osteoglossum bicirrhosum Silver arawana AB043025 Inoue et al. (2001) Pantodontidae Pantodon buchholzi Freshwater butterXyWsh AB043068 Inoue et al. (2001) Catostomidae Carpiodes River carpsucker AY366087 Broughton et al. unpublished Catostomidae Myxocyprinus Chinese sucker AY986503 Peng et al. (2006) 856 Z. Peng et al. / Molecular
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