Identification of two independent X-autosome translocations in closely related mammalian (Proechimys) species

Abstract

Multiple sex chromosome systems have been described for several mammalian orders, with different species from the same genus sharing the same system (e.g., X₁X₂Y or XY₁Y₂). This is important because the translocated autosome may be influenced by the evolution of the recipient sex chromosome, and this may be related to speciation. It is often thought that the translocation of an autosome to a sex chromosome may share a common origin among phylogenetically related species. However, the neo-X chromosomes of Proechimys goeldii (2n = 24♀, 25♂/NFa = 42) and Proechimys gr. goeldii (2n = 16♀, 17♂/NFa = 14) have distinct sizes and morphologies that have made it difficult to determine whether they have the same or different origins. This study investigates the origins of the XY₁Y₂ sex chromosome determination system in P. goeldii (PGO) and P. gr. goeldii (PGG) and elucidates the chromosomal rearrangements in this low-diploid-number group of Proechimys species. Toward this end, we produced whole-chromosome probes for P. roberti (PRO; 2n = 30♂/NFa = 54) and P. goeldii (2n = 25♂/NFa = 42) and used them in comparative chromosomal mapping. Our analysis reveals that multiple translocations and inversions are responsible for the karyotype diversity of these species, with only three whole-chromosomes conserved between PRO and PGO and eight between PGO and PGG. Our data indicate that multiple sex chromosome systems have originated twice in Proechimys. As small populations are prone to the fixation of chromosomal rearrangements, we speculate that biological features of Rodentia contribute to this fixation. We also highlight the potential of these rodents as a model for studying sex chromosome evolution.

Figure 1

Map showing the distribution areas of Proechimys roberti and P. goeldii. The numbers refer to the collection points for the samples of P. roberti, P. goeldii and P. gr. goeldii karyotyped in the present study (localities 1 and 7) and in the literature (localities 2–6, 8–13), as detailed in Supplementary Table 1.

Figure 2

Flow karyotypes of (a) Proechimys roberti (PRO, 2n = 30♂) and (b) P. goeldii (PGO, 2n = 25♂).

Figure 3

FISH results obtained from (a) Proechimys roberti (PRO♂), (b) P. goeldii (PGO♂) and (c) P. gr. goeldii (PGG♂) using the PGO (left) and PRO (right) probes. Each chromosome pair is shown in a box. For some pairs, multiple photos showing different probes are presented to exhibit that the chromosomes were completely covered by the whole-chromosome probes. An asterisk indicates a centromere. Whole-chromosome probes are shown in green (FITC), red (CY3) and yellow (FITC + CY3). Counterstaining is shown in blue (DAPI). Scale bar: 100 pixels.

Figure 4

G-banded karyotypes of (a) Proechimys roberti (PRO♂), (b) P. goeldii (PGO♂), and (c) P. gr. goeldii (PGG♂). The left and right panels show the PGO and PRO whole-chromosome probes, respectively. An asterisk indicates a centromere.

Figure 5

(a) Ideograms of the karyotypes of Proechimys roberti (PRO♂), Proechimys goeldii (PGO♂) and Proechimys gr. goeldii (PGG♂), as assessed based on the PRO probes. (b) Hypothetical evolutionary transition from the chromosomes involved in the X-autosome translocation of PGO and PGG, based on the results obtained using the PRO probes.