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 Becker; Rachael Thomas; Vladimir A. Trifonov; Robert K. Wayne; Alexander S. Graphodatsky; Matthew Breen

doi:10.1007/s10577-011-9233-4

Chromosome Research

August 2011, 19:685

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

Authors
Authors and affiliations

Shannon E. Duke Becker
Rachael Thomas
Vladimir A. Trifonov
Robert K. Wayne
Alexander S. Graphodatsky
Matthew BreenEmail author

Article

First Online:: 27 September 2011

Received:: 04 July 2011
Revised:: 15 August 2011
Accepted:: 16 August 2011

DOI: 10.1007/s10577-011-9233-4

Cite this article as:: Duke Becker, S.E., Thomas, R., Trifonov, V.A. et al. Chromosome Res (2011) 19: 685. doi:10.1007/s10577-011-9233-4

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

Abbreviations

BAC: Bacterial artificial chromosome
BLAST: Basic local alignment search tool
CBR: Chrysocyon brachyurus (maned wolf)
CFA: Canis familiaris (domestic dog)
CHORI: Children’s Hospital Oakland Research Institute
cKIT: Cellular homolog for feline sarcoma viral oncogene vKIT
CTH: Cerdocyon thous (crab-eating fox)
DNA: Deoxyribonucleic acid
DVE: Dusicyon vetulus (hoarey fox)
EBR: Evolutionary breakpoint region
ECCS: Evolutionarily conserved chromosomal segment
FBM: Fragile breakage model
FISH: Fluorescence in situ hybridization
FZE: Fennecus zerda (fennec fox)
LRIG1: Leucine-rich repeats and immunoglobulin-like domain protein 1
NPRp: Nyctereutes procynoides procynoides (Chinese raccoon dog)
NPRv: Nyctereutes procynoides viverrinus (Japanese raccoon dog)
OME: Otocyon megalotis (bat-eared fox)
RET: Rearranged during transfection
SA: South American
SVE: Speothus venaticus (bush dog)
UCI: Urocyon cinereogenteus (gray fox)
VMA: Vulpes macrotis (kit fox)
VVU: Vulpes vulpes (red fox)

Supplementary material

10577_2011_9233_Fig12_ESM.jpg (2 mb)

Supplemental Fig. 1

a Thirteen BAC probes spaced ∼10 Mb apart along the length of CFA1 were hybridized together onto CFA chromosome spreads. The location and orientation of the panel represents the CFA1 ECCS. b The CFA1 probe panel was hybridized to VVU5 and VVU1, revealing a breakpoint between probes representing CFA1;22.3 Mb (yellow) and CFA1;32. 3Mb (purple). Regions of CFA1 ECCSs on either side of the breakpoint are indicated with a suffix (i.e., CFA1a and CFA1b). Through application of the multicolor labeling strategy, the location and orientation of each CFA1 ECCS was evident (inset). Scale bar, 10 μm (JPEG 2026 kb)

10577_2011_9233_MOESM1_ESM.eps (6.2 mb)

High Resolution Image (EPS 6343 kb)

10577_2011_9233_MOESM2_ESM.xls (47 kb)

Supplemental Table 1–4CFA regions corresponding to ECCSs are listed with the corresponding regions of red fox (VVU), Chinese raccoon dog (NPRp), and gray fox (UCI) indicated. Table 1 is sorted by dog region, Table 2 by red fox chromosome locations, Table 3 by Chinese raccoon dog chromosome locations, and Table 4 by gray fox chromosome locations. Regions with additional hybridization to B chromosomes of red fox and Chinese raccoon dog are noted with asterisks. While we used the nomenclature of Wayne et al. (1987a) for gray fox chromosomes, the final column lists the nomenclature used in Graphodatsky et al. (2008). The gray fox cells described in Graphodatsky et al. (2008) contain a translocation relative to the cells described in this text. The regions involved (CFA7, 28, 37 ECCSs on UCI12, 15) are noted with double asterisks here, shown in Fig. 4 and discussed in the text (XLS 47 kb)

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Authors and Affiliations

Shannon E. Duke Becker
- 1
Rachael Thomas
- 1
- 2
Vladimir A. Trifonov
- 3
Robert K. Wayne
- 4
Alexander S. Graphodatsky
- 3
Matthew Breen
- 1
- 2
- 5
Email author

1.Department of Molecular Biomedical Sciences, College of Veterinary MedicineNorth Carolina State UniversityRaleighUSA
2.Center for Comparative Medicine and Translational ResearchNorth Carolina State UniversityRaleighUSA
3.Department of Molecular and Cellular BiologyInstitute of Chemical Biology and Fundamental MedicineNovosibirskRussia
4.Department of Ecology and Evolutionary BiologyUniversity of California Los AngelesLos AngelesUSA
5.Cancer Genetics Program, UNC Lineberger Comprehensive Cancer CenterChapel HillUSA

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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

Abstract

Keywords

Abbreviations

Supplementary material

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