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Testing chromosomal phylogenies and inversion breakpoint reuse in Drosophila. The martensis cluster revisited

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Abstract

The chromosomal relationships of the four martensis cluster species are among the most complex and intricate within the entire Drosophila repleta group, due to the so-called sharing of inversions. Here, we have revised these relationships using comparative mapping of bacterial artificial chromosome (BAC) clones on the salivary gland chromosomes. A physical map of chromosome 2 of Drosophila uniseta (one of the cluster members) was generated by in situ hybridization of 82 BAC clones from the physical map of the Drosophila buzzatii genome (an outgroup that represents the ancestral arrangement). By comparing the marker positions, we determined the number, order, and orientation of conserved chromosomal segments between chromosome 2 of D. buzzatii and D. uniseta. GRIMM software was used to infer that a minimum of five chromosomal inversions are necessary to transform the chromosome 2 of D. buzzatii into that of D. uniseta. Two of these inversions have been overlooked in previous cytological analyses. The five fixed inversions entail two breakpoint reuses because only nine syntenic segments and eight interruptions were observed. We tested for the presence of the five inversions fixed in D. uniseta in the other three species of the martensis cluster by in situ hybridization of eight breakpoint-bearing BAC clones. The results shed light on the chromosomal phylogeny of the martensis cluster, yet leave a number of questions open.

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Abbreviations

BAC:

Bacterial artificial chromosome

EMD:

Emerin

FLNA:

Filamin A, alpha

GRB:

Genomic regulatory blocks

kb:

Kilobase

Mb:

Megabase

mtDNA:

Mitochondrial DNA

mya:

Million years ago

myr:

Million years

TE:

Transposable element

Xdh :

Xanthine dehydrogenase

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Acknowledgements

We thank Julio Rozas, Mario Cáceres and Roger Vila for constructive comments and Francisco Rodriguez-Trelles for help. This work was supported by grant BFU2008-04988 from the Ministerio de Ciencia e Innovación (Spain) awarded to A.R. and by a PIF-UAB doctoral fellowship awarded to C.F.P.

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Correspondence to Alfredo Ruiz.

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Supplementary Table 1

List of BAC clones from the Drosophila buzzatii chromosome 2 (González et al. 2005) hybridized to the chromosomes of Drosophila uniseta. Chromosomal localization is given in terms of the D. buzzatii map that differs from the reference Drosophila repleta chromosome 2 (Wharton 1942) by nine fixed inversions (Gonzalez et al. 2005). Clones giving one signal in D. buzzatii and two or three signals in D. uniseta (shown in boldface) contain inversion breakpoints. See Figs. 3 and 4 for the arrangement of conserved segments in D. uniseta. (DOC 108 kb)

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Prada, C.F., Delprat, A. & Ruiz, A. Testing chromosomal phylogenies and inversion breakpoint reuse in Drosophila. The martensis cluster revisited. Chromosome Res 19, 251–265 (2011). https://doi.org/10.1007/s10577-011-9195-6

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