On the Origin and Evolution of the Extant System of B Chromosomes in Oryzomyini Radiation (Rodentia, Sigmodontinae)

Abstract

Heterogeneous supernumerary chromosomes (Bs) are recognized in the oryzomyines Holochilus brasiliensis, Nectomys rattus, N. squamipes, Oligoryzomys flavescens and Sooretamys angouya, representing about 10% of all known B-containing rodent species. They provide an outstanding model for understanding the origin, evolution and diversity of Bs in a phylogenetic context. Therefore, whole chromosome-specific probes were generated from flow-sorted Holochilus brasiliensis (HBR) autosomes 11 and 25+26 and chromosomes X, Y and Bs. Hybridizations were performed on male metaphases of 15 Oryzomyini species of which 3 are B-containing species. The results reveal that among the species sampled, 12 of them, belonging to a monophyletic Oryzomiyini subclade, are positive for an anonymous Oryzomyini shared heterochromatic region (OSHR) on both sex chromosomes. The OSHR is also present on Bs of Holochilus brasiliensis, Nectomys rattus and N. squamipes but not on Bs of O. flavescens and S. angouya. Two distinct additional OSHR/autosome associations are observed on S. angouya. The three species that are OSHR negative belong to an outgroup. Molecular dating suggests that the OSHR originated between 7.8 and 3 Mya on ancestral sex chromosomes. A tentative explanation for the OSHR-positive nature of B regions in three species could be that transposable elements (TEs) from this specific sex chromosome region may have invaded existing B chromosomes. The presence of the OSHR on entire Xp and Yp adjacent to interstitial telomeric sequences at pericentromeric positions, as observed in Drymoreomys albimaculatus, show a similar organization as on B chromosomes in Nectomys squamipes. The diversity of the Oryzomyini Bs in number, size, morphology and genetic content may be explained by the independent origin of B chromosomes in different subgroups of species, with Bs in Holochilus brasiliensis, Nectomys squamipes and N. rattus sharing the OSHR with sex chromosomes, and those in Oligoryzomys flavescens and Sooretamys angouya lacking OSHR in Bs. The species-specific pattern of Bs is probably a consequence of their independent evolutionary origin.

Advances in cytogenetics of Brazilian rodents: cytotaxonomy, chromosome evolution and new karyotypic data

“…Differences were also described in Bs of Holochilus brasiliensis, Nectomys rattus Pelzeln, 1883, and Oligoryzomys flavescens (Waterhouse, 1837) (Silva and Yonenaga-Yassuda 2004). Recently, FISH with Holochilus brasiliensis probes of sex chromosomes (X and Y) and both supernumeraries (B1 and B2) were performed, revealing positive signal on sex chromosome of 12 Oryzomyini species and Bs of Holochilus brasiliensis, Nectomys rattus and N. squamipes (Ventura et al 2015). No signal was observed in Bs of Oligoryzomys flavescens and Sooretamys angouya (G. Fischer, 1814), though, corroborating that supernumeraries in this group may have had independent origins (Ventura et al 2015).…”

B Chromosome Diversity and Repetitive Sequence Distribution in an Isolated Population of <b><i>Akodon montensis</i></b> (Rodentia, Sigmodontinae)

“…We estimate that the founder AMO population must have colo- nized the island at least 11,500 years ago due to the geological formation of most of the island that dates to the Holocene and Pleistocene [Possomai et al, 2010] coinciding with the last glacial maximum when the continental shelf was exposed by falling sea levels, permitting the dispersal of a wide range of organisms [Leite et al, 2016]. Ventura et al [2015] showed a shared heterochromatic region in Orizomyini rodents which occurs in both A and B chromosomes in the Orizomyini tribe and dates about 3-7 million years, giving evidence that the total differentiation of the B chromosome system in this tribe is not completed. Therefore, our findings suggest that the B chromosomes of this AMO population are older than the estimated colonization of the island and likely are the result of a founder effect, which could have culminated the high frequency in the population.…”

Chromosomal variation in Argentine populations of Akodon montensis Thomas, 1913 (Rodentia, Cricetidae, Sigmodontinae)

“…B chromosomes (Bs) appear as supernumerary elements to the standard chromosome complement and are highly variables (Silva and Yonenaga 2004; Vujošević and Blagojević 2004; Ventura et al 2015). The B of Akodon montensis studied here had identical morphology to those detected in Brazil (Yonenaga-Yassuda et al 1975; Kasahara and Yonenaga-Yassuda 1982; Yonenaga-Yassuda et al 1992; Fagundes et al 2000; Silva and Yonenaga-Yassuda 2004).…”

“…Variation in the frequency of B chromosomes is common among populations (Silva and Yonenaga Yassuda 2004; Vujošević and Blagojević 2004; Ventura et al 2015). In Akodon montensis the frequency of individuals with Bs appears to vary among localities, but several populations were studied with low sample size.…”