Chromosome Research

, 19:685 | Cite as

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
Article
First Online:
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Revised:
Accepted:

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)

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Notes

Acknowledgments

This study was supported by a grant from the Morris Animal Foundation awarded to MB (D08ZO-022). SEDB was funded in part by the Comparative Biomedical Sciences Graduate Program at NCSU. RW was supported by funds from the National Science Foundation (DEB0614585), and ASG and VAT were supported by funds from the Program on Molecular and Cellular Biology (MCB) and Russian Foundation of Basic Research (RFBR).

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 1–4 CFA 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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Copyright information

© Springer Science+Business Media B.V. 2011

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

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