Pike and salmon as sister taxa: Detailed intraclade resolution and divergence time estimation of Esociformes + Salmoniformes based on whole mitochondrial genome sequences (original) (raw)

Highlights

Abstract

The increasing number of taxa and loci in molecular phylogenetic studies of basal euteleosts has brought stability in a controversial area. A key emerging aspect to these studies is a sister Esociformes (pike) and Salmoniformes (salmon) relationship. We evaluate mitochondrial genome support for a sister Esociformes and Salmoniformes hypothesis by surveying many potential outgroups for these taxa, employing multiple phylogenetic approaches, and utilizing a thorough sampling scheme. Secondly, we conduct a simultaneous divergence time estimation and phylogenetic inference in a Bayesian framework with fossil calibrations focusing on relationships within Esociformes

Salmoniformes. Our dataset supports a sister relationship between Esociformes and Salmoniformes; however the nearest relatives of Esociformes

Salmoniformes are inconsistent among analyses. Within the order Esociformes, we advocate for a single family, Esocidae. Subfamily relationships within Salmonidae are poorly supported as Salmoninae sister to Thymallinae

Coregoninae.

Introduction

A consensus on the evolutionary relationships among basal euteleost lineages is emerging as a result of increasing numbers of both taxa and loci represented in molecular datasets. Results from these studies are beginning to identify stable patterns of relationships between a set of lineages whose affinities have been controversial area since the inception of Euteleostei (Greenwood et al., 1966). Protacanthopterygian (Rosen, 1974) relationships have been examined in multiple phylogenetic studies relying on evidence from morphological and molecular traits (Begle, 1991, Begle, 1992, Diogo et al., 2008, Fink, 1984, Fink and Weitzman, 1982, Ishiguro et al., 2003, Johnson and Patterson, 1996, Lauder and Liem, 1983, López et al., 2004, Patterson, 1994, Rosen, 1982, Sanford, 1990, Williams, 1987). And, while a sister group relationship between Salmoniformes and Esociformes is broadly supported by analyses based on the suspensorium and associated musculature (Williams, 1987, Wilson and Williams, 2010), mitochondrial genome data (Ishiguro et al., 2003, Li et al., 2010), nuclear sequence data (López et al., 2004, Near et al., 2012, Santini et al., 2009), and combined nuclear and mitochondrial data (Burridge et al., 2012, López et al., 2004), the placement of the Esociformes

Salmoniformes clade among basal euteleost lineages remains problematic.

Mitochondrial genome (mitogenome) sequences from 33 teleost species provide evidence for a sister group relationship between esociforms and salmoniforms; however these two lineages were only represented with one species each in that analysis (Ishiguro et al., 2003). In this study, we expand the sampling of protacanthopterygians to 93 species with the addition of five newly determined mitogenome sequences and a targeted selection of previously published sequences designed to help test existing ideas on basal euteleost relationships. Specifically, we determined mitogenome sequences from two salmoniform and three esociform species. Increased taxon sampling is known to improve phylogenetic inference (Hedtke et al., 2006, Hillis, 1998, Hillis et al., 2003, Pollock et al., 2002), and to enhance the ability to infer macroevolutionary processes from a phylogenetic tree (Heath et al., 2008).

Our goals are to test possible placements of the Esociformes

Salmoniformes clade among basal euteleost lineages and to generate a hypothesis of intra-ordinal relationships within the Esociformes and Salmoniformes. Within esociforms we test whether the family Umbridae (Nelson, 2006) is a monophyletic group containing the genera Umbra, Novumbra, and Dallia; and within salmoniforms we examine alternative arrangements of the relationships between the three salmonid subfamilies and among the genera of Salmoninae. Finally, we also estimate the timing of major cladogenetic events in the history of the esociform

salmoniform group. We use a maximum likelihood (ML) framework to infer a mitochondrial genome phylogeny for the 93 taxa considered here and a Bayesian-based joint tree inference and divergence time estimation procedure on a 34 species taxonomic subset to focus on the intra-ordinal history of the esociform

salmoniform clade.

Section snippets

Taxonomic sampling

Sampling for novel mitogenome sequence determinations targeted unrepresented lineages within Salmoniformes and Esociformes (Table 1). Species were selected to divide long branches to reduce possible long branch generated artifacts in the phylogenetic inference (Hillis, 1998). We newly determined five mitogenomes for this study: Novumbra hubbsi, Umbra pygmaea, and Esox niger (Esociformes) and Prosopium cylindraceum and Parahucho perryi (Salmoniformes). The newly determined mitogenome sequences

Sequencing

We sequenced complete or nearly complete mitochondrial genomes of P. cylindraceum, P. perryi, N. hubbsi, Umbra krameri, and E. niger. The mitochondrial control regions contained repeating motifs and were not sequenced completely in some taxa. Gene content and order in the newly determined mitochondrial genomes follow the standard arrangement found in most vertebrates.

Esociform and salmoniform phylogenetic relationships

The Esociformes

Salmoniformes clade is supported in the ML topology using the 1n2nRnTn and 1n2n3RYRnTn codings with bootstrap

Phylogenetic placement of the Esociformes + Salmoniformes

Results of both full and reduced taxon set analyses reported here further strengthen the case for a sister group relationship between esociforms and salmoniforms (López et al., 2000, López et al., 2004) All our analyses invariably support a sister relationship of Esociformes and Salmoniformes. Among the euteleosts, the placement of Lepidogalaxias as the sister group of all other euteleost is in agreement with mitogenomic (Li et al., 2010), combined nuclear and mitochondrial data (Burridge et

Conclusion

Our results add to the emerging consensus on basal euteleost relationships in which Esociformes and Salmoniformes are sister lineages. Given the stability of this relationship, it may be appropriate at this time to identify an appropriate name for the Esociformes

Salmoniformes clade. A possible solution is to modify the limits of Salmoniformes to encompass both groups, abandon Esociformes and treat the two major lineages in the newly defined salmoniforms as the families Esocidae and Salmonidae.

Conflict of interest

None.

Acknowledgments

We would like to thank the following individuals in sample collections: Molly Hallock (Washington Department of Fish and Wildlife), Joseph Buckwalter (Alaska Department of Fish and Game), and Motohiro Kikuchi (Chitose Salmon Park). A gift of tissue was provided by the Academy of Natural Sciences of Philadelphia (ANSP 189305). Robert Marcotte provided helpful comments on a draft manuscript and Sébastien Lavoué provided the geologic time bar used in Fig. 2 and assistance with the BEAST analysis.

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