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.

Highlights

  • Supernumerary (B) chromosomes are found in about 15% of eukaryotic species, including animals, plants and fungi [1], and, in most cases, their genomic functions and molecular composition remain obscure [1,2]

  • Given the specific Holochilus brasiliensis (HBR) B painting patterns observed on segments of the sex chromosomes and on the autosomes of S. angouya, the genomes of the other 10 species (8 genera), without supernumeraries, were included in the sample, giving a total of 15 species investigated by painting probes

  • This study indicates the valuable contribution of chromosome painting to the recognition of an anonymous sequence shared by sex chromosomes, B chromosomes and autosomes in some species belonging to the Oryzomyini tribe

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Summary

Introduction

Supernumerary (B) chromosomes are found in about 15% of eukaryotic species, including animals, plants and fungi [1], and, in most cases, their genomic functions and molecular composition remain obscure [1,2]. Oryzomyini have an exceptional range of diploid and fundamental numbers, with polymorphism of autosomes and sex chromosomes in some species [11,12,13,14,15,16]. Their B chromosomes show great diversity in terms of number, size, morphology of Bs, DNA replication, banding patterns and presence/absence of interstitial telomeric signals (ITS) [4,11]

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