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Downloaded Ses Were Performed, but Only Mt-Cytb (Gene Encoding from Genbank (Benson Et Al Biologia 64/4: 811—818, 2009 Section Cellular and Molecular Biology DOI: 10.2478/s11756-009-0121-8 Bayesian inference of cetacean phylogeny based on mitochondrial genomes Xiao-Guang Yang1,2 1Department of Physics and Astronomy, McMaster University, Hamilton, Ontario, Canada, L8S 4M1 2Current address: Department of Biological Engineering, University of Missouri, Columbia, MO 65211 USA, e-mail: [email protected] Abstract: The phylogeny of Cetacea (whales, dolphins, porpoises) has long attracted the interests of biologists and has been investigated by many researchers based on different datasets. However, some phylogenetic relationships within Cetacea still remain controversial. In this study, Bayesian analyses were performed to infer the phylogeny of 25 representative species within Cetacea based on their mitochondrial genomes for the first time. The analyses recovered the clades resolved by the previous studies and strongly supported most of the current cetacean classifications, such as the monophyly of Odontoceti (toothed whales) and Mysticeti (baleen whales). The analyses provided a reliable and comprehensive phylogeny of Cetacea which can provide a foundation for further exploration of cetacean ecology, conservation and biology. The results also showed that: (i) the mitochondrial genomes were very informative for inferring phylogeny of Cetacea; and (ii) the Bayesian analyses outperformed other phylogenetic methods on inferring mitochondrial genome-based phylogeny of Cetacea. Key words: Cetacea; Odontoceti; Mysticeti; cetacean phylogeny; Bayesian analysis; mitochondrial genomes. Abbreviations: mt, mitochondrial; aa, amino acid; nt, nucleotide; NJ, neighbor-joining; MP, maximum parsimony; ML, maximum likelihood; BP, bootstrap percentage; PP, Bayesian posterior probabilities; MCMC, Markov chain Monte Carlo; GTR4, general time-reversible four-state model; GTR2, general time-reversible two-state model; PHASE, Phylogenetics And Sequence Evolution. Introduction al. 2005; Nishida et al. 2007; Caballero et al. 2008). Some of the issues have been resolved: there is a general Cetaceans (whales, dolphins, porpoises) are large mam- agreement that Cetacea, the sister group of Hippop- mals that are widely distributed on Earth. They are im- tamidae, is within Artiodactyla (Hasegawa & Adachi portant species in the ecosystem. Many of them were 1996; Montgelard et al. 1997; Nikaido et al. 1999; Lum commercially harvested for long time, making the clas- et al. 2000; Thewissen et al. 2001); the monophyly and sification of cetaceans based on their morphology char- sister relationship of Odontoceti and Mysticeti were acteristics possible. Some of them, such as Yangtze supported by morphological, nuclear and mitochondrial River dolphin, are endangered species. The cetacean data (Messenger & McGuire 1998; O’Leary & Geisler phylogeny is important for understanding the cetacean 1999; Nikaido et al. 2001; Rychel et al. 2004; Yan et ecology and protecting endangered species. The or- al. 2005; May-Collado & Agnarsson 2006; Nishida et der Cetacea includes two extant suborders: Odontoceti al. 2007). It has been widely accepted that Balaenidae (toothed whales) and Mysticeti (baleen whales). Odon- is the basal group of Mysticeti (Arnason et al. 1992; toceti is composed of four major groups: Physeteroidea Milinkovitch et al. 1994; Arnason & Gullberg 1996; (sperm whales), Ziphiidae (beaked whales), Delphi- Rychel et al. 2004; Sasaki et al. 2005; May-Collado & noidea and polyphyletic river dolphins, while Mysticeti Agnarsson 2006; Nishida et al. 2007). However, some is- divides into four groups: Eschrichtiidae (gray whales), sues remain controversial: the relationships among the Neobalaenidae (pygmy right whales), Balaenidae (right groups within Odontoceti and Mysticeti (Adegoke et al. whales) and Balaenopteridae (rorquals and humpback 1993; Milinkovitch et al. 1993; Rosel et al. 1995; Arna- whales). The phylogeny of cetaceans has long attracted son & Gullberg 1996; Waddell et al. 2000; Hamilton et the interests of evolutionary biologists and has been al. 2001; Nikaido et al. 2001; Pichler et al. 2001), and investigated by many researchers based on different the relationships among several subgroups within Bal- datasets (e.g. morphology, nuclear and mitochondrial aenopteridae (Arnason et al. 1992; Adegoke et al. 1993; DNA, RNA and protein sequences) (Milinkovitch et al. Arnason & Gullberg 1994, 1996; Messenger & McGuire 1993; Rosel et al. 1995; Montgelard et al. 1997; Mes- 1998). senger & McGuire 1998; Rychel et al. 2004; Yan et Mitochondrial (mt) genomes have become popu- c 2009 Institute of Molecular Biology, Slovak Academy of Sciences 812 X.-G. Yang Table 1. Cetacean species list. Suborder/family Scientific name English name Mitochondrion Acc. No. Mysticeti Balaenidae Balaena mysticetus bowhead whale NC 005268 Eubalaena australis Southern right whale NC 006930 Eubalaena japonica Northern right whale NC 006931 Balaenopteridae Balaenoptera acutorostrata North Atlantic minke whale NC 005271 Balaenoptera bonaerensis Antarctic minke whale NC 006926 Balaenoptera borealis sei whale NC 006929 Balaenoptera brydei Bryde’s whale NC 006928 Balaenoptera edeni pygmy Bryde’s whale NC 007938 Balaenoptera musculus blue whale NC 001601 Balaenoptera omurai Omura’s baleen whale NC 007937 Balaenoptera physalus fin whale NC 001321 Megaptera novaeangliae humpback whale NC 006927 Eschrichtiidae Eschrichtius robustus Gray whale NC 005270 Neobalaenidae Caperea marginata pygmy right whale NC 005269 Odontoceti Delphinidae Lagenorhynchus albirostris white-beaked dolphin NC 005278 Iniidae Inia geoffrensis Boutu (Amazon River dolphin) NC 005276 Kogiidae Kogia breviceps pygmy sperm whale NC 005272 Lipotidae Lipotes vexillifer Yangtze River dolphin NC 007629 Monodontidae Monodon monoceros narwhal NC 005279 Phocoenidae Phocoena phocoena harbor porpoise NC 005280 Physeteridae Physeter catodon sperm whale NC 002503 Platanistidae Platanista minor Indus River dolphin NC 005275 Pontoporiidae Pontoporia blainvillei Franciscana dophin NC 005277 Ziphiidae Berardius bairdii Baird’s beaked whale NC 005274 Hyperoodon ampullatus Northern bottlenose whale NC 005273 lar in phylogenetic analysis since the mid 1990s for ity of the phylogeny was judged based on the recovery several reasons. The animal mt-genomes are relatively of the previously resolved and less controversial clades short and simple compared to the nuclear genomes, and (Gatesy et al. 1996; Gatesy 1997; Ursing & Arnason they are easy to amplify and sequence; the animal mt- 1998; Nikaido et al. 1999; Cassens et al. 2000; Nikaido DNA has relatively fast evolutionary rate (Brown et al. et al. 2001; Rychel et al. 2004; Sasaki et al. 2005). It 1979) and is free of recombination (Olivo et al. 1983). was also judged by the bootstrap percentage (BP) for In some previous studies, only 12 mt-genomes were in- NJ and MP methods and the Bayesian posterior prob- cluded in the phylogenetic analysis of Mysticeti (Sasaki abilities (PP) for Bayesian analyses (Suzuki et al. 2002; et al. 2005), or 16 mt-genomes in the order Cetacea (Ar- Erixon et al. 2003; Simmons et al. 2004). nason et al. 2004). The methods used in these studies were all standard statistical methods, such as neighbor- Material and methods joining (NJ), maximum parsimony (MP) and maxi- mum likelihood (ML). In other previous studies, a large Dataset number of species were included and Bayesian analy- The mt-genomes of 25 cetacean species were downloaded ses were performed, but only mt-Cytb (gene encoding from GenBank (Benson et al. 2008) at the Genomes web- mt-cytochrome b) or several other genes were employed site: http://www.ncbi.nlm.nih.gov/genomes/static/euk o. (Rychel et al. 2004; May-Collado & Agnarsson 2006). html. These species with completed mt-genomes are good In this study, Bayesian analyses were performed to representatives of the extant families within Cetacea. The recover the phylogenetic relationship of 25 representa- mt-genomes of 7 non-cetacean species, including the hip- tive species within Cetacea based on their mt-genomes popotamus, were employed as outgroups. Names and acces- for the first time. Bayesian analysis has been widely sion numbers of cetacean and non-cetacean species are listed in Table 1 and Table 2, respectively. used by researchers for inferring phylogeny (Huelsen- beck et al. 2001; Holder & Lewis 2003). The method Phylogenetic analyses has clear computational advantages over standard sta- The phylogenetic analyses were performed at both nu- tistical methods and can be used to explore a com- cleotide (nt) and amino acid (aa) levels. The 12 protein- plex model space in reasonable time (Huelsenbeck et coding genes on the same strand of mt-DNA were used. The al. 2001; Holder & Lewis 2003). The clades recovered NADH6 gene was excluded because the gene is on the oppo- in the previous studies, such as the monophyly and sis- site strand of mt-DNA and has different base composition than the other genes. The alignments of all these sequences ter relationship of Odontoceti and Mysticeti, were in- were obtained using Clustal X (Thompson et al. 1997) and vestigated. The controversial relationships among these modified carefully by eye using GeneDoc (Nicholas et al. suborders were also investigated and discussed. NJ and 1997). All the positions with ambiguous alignment were ex- MP analyses were performed in order to compare the cluded. The number of remaining codons of the 12 concate- results with those from Bayesian analyses. The reliabil- nated genes was 3589. Bayesian cetacean
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