Abstract

Considerable research efforts have focused on elucidating the systematic relationships among salmonid fishes; an understanding of these patterns of relatedness will inform conservation- and fisheries-related issues, as well as provide a framework for investigating evolutionary mechanisms in the group. However, uncertainties persist in current Salmonidae phylogenies due to biological and methodological factors, and a comprehensive phylogeny including most representatives of the family could provide insight into the causes of these difficulties. Here we increase taxon sampling by including nearly all described salmonid species (n = 63) to present a time-calibrated and more complete portrait of Salmonidae using a combination of molecular markers and analytical techniques. This strategy improved resolution by increasing the signal-to-noise ratio and helped discriminate methodological and systematic errors from sources of difficulty associated with biological processes. Our results highlight novel aspects of salmonid evolution. First, we call into question the widely-accepted evolutionary relationships among sub-families and suggest that Thymallinae, rather than Coregoninae, is the sister group to the remainder of Salmonidae. Second, we find that some groups in Salmonidae are older than previously thought and that the mitochondrial rate of molecular divergence varies markedly among genes and clades. We estimate the age of the family to be 59.1 MY (CI: 63.2-58.1 MY) old, which likely corresponds to the timing of whole genome duplication in salmonids. The average, albeit highly variable, mitochondrial rate of molecular divergence was estimated as ∼0.31%/MY (CI: 0.27–0.36%/MY). Finally, we suggest that some species require taxonomic revision, including two monotypic genera, Stenodus and Salvethymus. In addition, we resolve some relationships that have been notoriously difficult to discern and present a clearer picture of the evolution of the group. Our findings represent an important contribution to the systematics of Salmonidae, and provide a useful tool for addressing questions related to fundamental and applied evolutionary issues.

Highlights

  • The evolutionary relationships among salmonid fishes have been the focus of extensive systematic and phylogenetic research for many decades [1]–[5]

  • Unresolved issues in salmonid phylogenetics are often attributed to two causes: limitations imposed by biological factors and constraints imposed by methodological factors, including insufficient sampling of taxa or genes [5], [13], [14]

  • According to the groupings recommended by the Integrated Taxonomic Information System [64], our data set consisted of two Brachymystax species, 20 Coregonus species, two Hucho species, 11 Oncorhynchus species, six Prosopium species, six Salmo species, nine Salvelinus species, four Thymallus species and three species from monotypic genera: Parahucho perryi, Salvethymus svetovidovi and Stenodus leucichthys

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Summary

Introduction

The evolutionary relationships among salmonid fishes have been the focus of extensive systematic and phylogenetic research for many decades [1]–[5]. Salmonid fishes offer a unique opportunity to explore a number of evolutionary and ecological concepts, including mechanisms of speciation [6], the evolution of complex life-histories [8], [9], the role of hybridization in evolution [7], patterns of chromosomal evolution [10] and genome duplication [11]. Despite the large body of work dedicated to inferring phylogenetic relationships among salmonid species, some important questions regarding their evolutionary history remain unanswered These questions vary in their degree of resolution across different levels of biological organization, from the appropriate placement of the root of the Salmonidae tree to the role of introgression in species or subspecies designations. Unresolved issues in salmonid phylogenetics are often attributed to two causes: limitations imposed by biological factors (including parallel and convergent evolution due to similarity of ecological niches, rapid radiation, frequent hybridization, and local adaptation [4], [12]) and constraints imposed by methodological factors, including insufficient sampling of taxa or genes [5], [13], [14]

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