Tracking chromosome evolution in southern African gerbils using flow-sorted chromosome paints

Abstract

Desmodillus and Gerbilliscus (formerly Tatera) comprise a monophyletic group of gerbils (subfamily Gerbillinae) which last shared an ancestor approximately 8 million years ago; diploid chromosome number variation among the species ranges from 2n = 36 to 2n = 50. In an attempt to shed more light on chromosome evolution and speciation in these rodents, we compared the karyotypes of 7 species, representing 3 genera, based on homology data revealed by chromosome painting with probes derived from flow-sorted chromosomes of the hairy footed gerbil, Gerbillurus paeba (2n = 36). The fluorescent in situ hybridization data revealed remarkable genome conservation: these species share a high proportion of conserved chromosomes, and differences are due to 10 Robertsonian (Rb) rearrangements (3 autapomorphies, 3 synapomorphies and 4 hemiplasies/homoplasies). Our data suggest that chromosome evolution in Desmodillus occurred at a rate of ~1.25 rearrangements per million years (Myr), and that the rate among Gerbilliscus over a time period spanning 8 Myr is also ~1.25 rearrangements/Myr. The recently diverged Gerbillurus (G. tytonis and G. paeba) share an identical karyotype, while Gerbilliscus kempi, G. afra and G. leucogaster differ by 6 Rb rearrangements (a rate of ~1 rearrangement/Myr). Thus, our data suggests a very slow rate of chromosomal evolution in Southern African gerbils.

Fig. 1

Bivariate flow karyotype of a male fibroblast cell line from G. paeba (2n = 36).

Fig. 2

Partial homology map among G. paeba (GPA), G. tytonis (GTY), G. leucogaster (GLE), G. afra (GAF), and G. kempi (GKE) based on chromosome painting and G-banding, with GPA chromosomes as references. Chromosomes that were conserved in their entirety in all Gerbilliscus taxa are in the inset. The regions of homology are indicated by the vertical lines and GPA chromosome numbers (large font). Centromere positions are indicated by closed circles, and the brackets indicate the boundaries of inversions. Chromosome numbers correspond to those in the respective species' karyotypes.

Fig. 3

G-banded haploid karyotype of a male D. auricularis with regions of orthology to G. paeba indicated by vertical lines (numbered to the right) as determined by cross-species chromosome painting. Centromere positions are indicated by closed circles.

Fig. 4

G-banded haploid karyotype of a male P. obesus with regions of orthology to G. paeba indicated by vertical lines (numbered to the right) as determined by cross-species chromosome painting. Centromere positions are indicated by closed circles.

Fig. 5

Examples of FISH of G. paeba (GPA) painting probes onto G. tytonis (GTY), G. kempi (GKE), D. auricularis (DAU), and P. obesus (POB). a Hybridization of GPA14 (Cy3) on GTY13. b Hybridization of GPA12 and GPA14 on GKE10proximal and 20, and GKE10distal, respectively. c FISH of GPA5 on DAU5 and 24. d FISH of GPA1 and GPA6 on POB2p,7q, and 20 and POB2q and 12, respectively. Chromosomes are counterstained with DAPI.

Fig. 6

A consensus tree derived from mtDNA and nuclear sequence data [Chevret and Dobigny, 2005; Colangelo et al., 2005, 2007; Granjon et al., 2012]. The diploid numbers and the approximate divergence dates were obtained from Colangelo et al. [2007]. Node A is characterised by gross chromosomal homeologies in all species identified with GPA7, 9, 13, 15-17, and the syntenic association GPA4q/3q defines split of D. auricularis at node B. The nodes C-F contain 10 Robertsonian rearrangements of which 4 (involving GPA1, 2, 3, 5) were characterised as hemiplasies or homoplasies [Avise and Robinson, 2008]. For detailed discussion see text and table 2.