Article

Chromosome Research

, Volume 19, Issue 6, pp 685-708

Anchoring the dog to its relatives reveals new evolutionary breakpoints across 11 species of the Canidae and provides new clues for the role of B chromosomes

  • Shannon E. Duke BeckerAffiliated withDepartment of Molecular Biomedical Sciences, College of Veterinary Medicine, North Carolina State University
  • , Rachael ThomasAffiliated withDepartment of Molecular Biomedical Sciences, College of Veterinary Medicine, North Carolina State UniversityCenter for Comparative Medicine and Translational Research, North Carolina State University
  • , Vladimir A. TrifonovAffiliated withDepartment of Molecular and Cellular Biology, Institute of Chemical Biology and Fundamental Medicine
  • , Robert K. WayneAffiliated withDepartment of Ecology and Evolutionary Biology, University of California Los Angeles
  • , Alexander S. GraphodatskyAffiliated withDepartment of Molecular and Cellular Biology, Institute of Chemical Biology and Fundamental Medicine
  • , Matthew BreenAffiliated withDepartment of Molecular Biomedical Sciences, College of Veterinary Medicine, North Carolina State UniversityCenter for Comparative Medicine and Translational Research, North Carolina State UniversityCancer Genetics Program, UNC Lineberger Comprehensive Cancer Center Email author 

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Abstract

The emergence of genome-integrated molecular cytogenetic resources allows for comprehensive comparative analysis of gross karyotype architecture across related species. The identification of evolutionarily conserved chromosome segment (ECCS) boundaries provides deeper insight into the process of chromosome evolution associated with speciation. We evaluated the genome-wide distribution and relative orientation of ECCSs in three wild canid species with diverse karyotypes (red fox, Chinese raccoon dog, and gray fox). Chromosome-specific panels of dog genome-integrated bacterial artificial chromosome (BAC) clones spaced at ∼10-Mb intervals were used in fluorescence in situ hybridization analysis to construct integrated physical genome maps of these three species. Conserved evolutionary breakpoint regions (EBRs) shared between their karyotypes were refined across these and eight additional wild canid species using targeted BAC panels spaced at ∼1-Mb intervals. Our findings suggest that the EBRs associated with speciation in the Canidae are compatible with recent phylogenetic groupings and provide evidence that these breakpoints are also recurrently associated with spontaneous canine cancers. We identified several regions of domestic dog sequence that share homology with canid B chromosomes, including additional cancer-associated genes, suggesting that these supernumerary elements may represent more than inert passengers within the cell. We propose that the complex karyotype rearrangements associated with speciation of the Canidae reflect unstable chromosome regions described by the fragile breakage model.

Keywords

B chromosomes fragile breakage model breakpoint reuse theory fluorescence in situ hybridization phylogenetic Canidae