Molecular systematics of Salmonidae: combined nuclear data yields a robust phylogeny

Abstract

The phylogeny of salmonid fishes has been the focus of intensive study for many years, but some of the most important relationships within this group remain unclear. We used 269 Genbank sequences of mitochondrial DNA (from 16 genes) and nuclear DNA (from nine genes) to infer phylogenies for 30 species of salmonids. We used maximum parsimony and maximum likelihood to analyze each gene separately, the mtDNA data combined, the nuclear data combined, and all of the data together. The phylogeny with the best overall resolution and support from bootstrapping and Bayesian analyses was inferred from the combined nuclear DNA data set, for which the different genes reinforced and complemented one another to a considerable degree. Addition of the mitochondrial DNA degraded the phylogenetic signal, apparently as a result of saturation, hybridization, selection, or some combination of these processes. By the nuclear-DNA phylogeny: (1) (Hucho hucho, Brachymystax lenok) form the sister group to (Salmo, Salvelinus, Oncorhynchus, H. perryi); (2) Salmo is the sister-group to (Oncorhynchus, Salvelinus); (3) Salvelinus is the sister-group to Oncorhynchus; and (4) Oncorhynchus masou forms a monophyletic group with O. mykiss and O. clarki, with these three taxa constituting the sister-group to the five other Oncorhynchus species. Species-level relationships within Oncorhynchus and Salvelinus were well supported by bootstrap levels and Bayesian analyses. These findings have important implications for understanding the evolution of behavior, ecology and life-history in Salmonidae.

Introduction

The family Salmonidae comprises three subfamilies, Coregoninae (whitefish and ciscoes), Thymallinae (grayling), and Salmoninae (char, trout, and salmon). The most speciose of these, Salmoninae, includes five genera distributed throughout the Northern Hemisphere, Brachymystax (lenok), Hucho (huchen and taimen), Oncorhynchus (Pacific trout and salmon), Salmo (Atlantic salmon and brown trout), and Salvelinus (char) (Hart, 1973; Hendry and Stearns, 2003; Scott and Crossman, 1973). Salmonid fishes have long been of great interest due to the commercial and recreational value of some species, and they are becoming increasingly important as model systems for addressing a wide range of evolutionary and ecological questions (Elliot, 1994; Groot and Margolis, 1991; Hendry and Stearns, 2003). Inference of a robust phylogeny for this group is important for comparative analyses of salmonid adaptations (e.g., Crespi and Teo, 2002; Fleming, 1998), comparative genomics (e.g., Woram et al., 2003), studies involving inference of ancestral states (e.g., McDowall, 1997; McLennan, 1994; Stearley, 1992), and evaluation of conservation priorities (Crandall et al., 2000).

Despite the importance of salmonids to humans, and to terrestrial and marine ecosystems, their evolutionary history has remained a matter of considerable dispute for many years (e.g., Domanico et al., 1997; McKay et al., 1996; McPhail, 1997; Norden, 1961; Oakley and Phillips, 1999; Phillips and Oakley, 1997; Phillips and Pleyte, 1991; Regan, 1914; Utter et al., 1973; Utter and Allendorf, 1994). Previous species-level and genus-level phylogenetic research on salmonid fishes have provided insights into some relationships, but numerous questions remain, most notably the among-genus divergences, and species-level relationships within Oncorhynchus and Salvelinus.

The lack of a comprehensive, well-resolved and well-supported phylogeny for Salmonidae can be largely attributed to previous studies using relatively small subsets of extant salmonid diversity, and only one or at most several genes or other character sets (e.g., morphology or karyology). To overcome these limitations, we have assembled and analyzed all available DNA-sequence data for the species in this family. The main goals of our study are twofold: (1) to use these data to infer the best tree for the family as a whole, and for particular lineages; and (2) to assess what additional data (i.e., sequence from which genes) are needed to achieve a species-level tree for the entire group.