A Phylogenomic Perspective on the Radiation of Ray-Finned Fishes Based upon Targeted Sequencing of Ultraconserved Elements (UCEs)

Brant C Faircloth,Francesco Santini,Laurie Sorenson,Michael E Alfaro,Corrie S Moreau

doi:10.1371/journal.pone.0065923

Brant C Faircloth, Francesco Santini + Show 3 more

Open Access

https://doi.org/10.1371/journal.pone.0065923

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Journal: PLoS ONE	Publication Date: Jun 18, 2013
Citations: 252	License type: CC BY 4.0

Affiliation: University of California, Los Angeles

Abstract

Ray-finned fishes constitute the dominant radiation of vertebrates with over 32,000 species. Although molecular phylogenetics has begun to disentangle major evolutionary relationships within this vast section of the Tree of Life, there is no widely available approach for efficiently collecting phylogenomic data within fishes, leaving much of the enormous potential of massively parallel sequencing technologies for resolving major radiations in ray-finned fishes unrealized. Here, we provide a genomic perspective on longstanding questions regarding the diversification of major groups of ray-finned fishes through targeted enrichment of ultraconserved nuclear DNA elements (UCEs) and their flanking sequence. Our workflow efficiently and economically generates data sets that are orders of magnitude larger than those produced by traditional approaches and is well-suited to working with museum specimens. Analysis of the UCE data set recovers a well-supported phylogeny at both shallow and deep time-scales that supports a monophyletic relationship between Amia and Lepisosteus (Holostei) and reveals elopomorphs and then osteoglossomorphs to be the earliest diverging teleost lineages. Our approach additionally reveals that sequence capture of UCE regions and their flanking sequence offers enormous potential for resolving phylogenetic relationships within ray-finned fishes.

Highlights

The ray-finned fishes (Actinopterygii) constitute the dominant radiation of vertebrates on the planet including more than 32,000 species and equaling or exceeding richness estimates for the combined total of birds, mammals, and reptiles
The variance in the proportion of reads and contigs on-target suggests that input DNA quality, insert length of DNA libraries, and taxonomic distance between the taxon used to design probes and taxa from which we enriched ultraconserved elements (UCEs) may play a role in enrichment efficiency
The lowest enrichment efficiencies we observed resulted from our removal of duplicated ultraconserved elements that may result from lineage-specific duplication events

Summary

Introduction

The ray-finned fishes (Actinopterygii) constitute the dominant radiation of vertebrates on the planet including more than 32,000 species and equaling or exceeding richness estimates for the combined total of birds, mammals, and reptiles. The earliest morphological studies of ray-finned fishes unite gar (Lepisosteus) with the bowfin (Amia) in the clade Holostei [1] though this clade is not recovered in some later analyses [2,3]. Morphological analyses alternatively place the osteoglossomorphs [6] or the elopomorphs [7,8,9,10] as the sister group to all other teleosts and the remaining lineages sister to the ostarioclupeomorph/euteleost clade. Some molecular analyses place elopomorphs and osteoglossomorphs as the sister group to remaining teleosts [11,12] while others recover a basal divergence between osteoglossomorphs and other teleosts [5,13]

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