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Open Access Highly Accessed Research article

The dynamic proliferation of CanSINEs mirrors the complex evolution of Feliforms

Kathryn B Walters-Conte1*, Diana LE Johnson2, Warren E Johnson3, Stephen J O’Brien4 and Jill Pecon-Slattery3

Author Affiliations

1 Department of Biology, American University, 101 Hurst Hall 4440 Massachusetts Ave, Washington, DC 20016, USA

2 Department of Biological Sciences, The George Washington University, 2036 G St, Washington, DC 20009, USA

3 Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, VA 22630, USA

4 Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, 41 A, Sredniy Avenue St., Petersburg 199034, Russia

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BMC Evolutionary Biology 2014, 14:137  doi:10.1186/1471-2148-14-137

Published: 20 June 2014

Abstract

Background

Repetitive short interspersed elements (SINEs) are retrotransposons ubiquitous in mammalian genomes and are highly informative markers to identify species and phylogenetic associations. Of these, SINEs unique to the order Carnivora (CanSINEs) yield novel insights on genome evolution in domestic dogs and cats, but less is known about their role in related carnivores. In particular, genome-wide assessment of CanSINE evolution has yet to be completed across the Feliformia (cat-like) suborder of Carnivora. Within Feliformia, the cat family Felidae is composed of 37 species and numerous subspecies organized into eight monophyletic lineages that likely arose 10 million years ago. Using the Felidae family as a reference phylogeny, along with representative taxa from other families of Feliformia, the origin, proliferation and evolution of CanSINEs within the suborder were assessed.

Results

We identified 93 novel intergenic CanSINE loci in Feliformia. Sequence analyses separated Feliform CanSINEs into two subfamilies, each characterized by distinct RNA polymerase binding motifs and phylogenetic associations. Subfamily I CanSINEs arose early within Feliformia but are no longer under active proliferation. Subfamily II loci are more recent, exclusive to Felidae and show evidence for adaptation to extant RNA polymerase activity. Further, presence/absence distributions of CanSINE loci are largely congruent with taxonomic expectations within Feliformia and the less resolved nodes in the Felidae reference phylogeny present equally ambiguous CanSINE data. SINEs are thought to be nearly impervious to excision from the genome. However, we observed a nearly complete excision of a CanSINEs locus in puma (Puma concolor). In addition, we found that CanSINE proliferation in Felidae frequently targeted existing CanSINE loci for insertion sites, resulting in tandem arrays.

Conclusions

We demonstrate the existence of at least two SINE families within the Feliformia suborder, one of which is actively involved in insertional mutagenesis. We find SINEs are powerful markers of speciation and conclude that the few inconsistencies with expected patterns of speciation likely represent incomplete lineage sorting, species hybridization and SINE-mediated genome rearrangement.

Keywords:
Incomplete lineage sorting; SINEs; Carnivora; Speciation; transposable elements; Adaptation; Feliformia; Felidae