Comparative genomic mapping reveals mechanisms of chromosome diversification in Rhipidomys species (Rodentia, Thomasomyini) and syntenic relationship between species of Sigmodontinae.

Vergiana Dos Santos Paixão,Willam Oliveira Da Silva,Malcolm Andrew Ferguson-Smith,Rogério Vieira Rossi,Cleusa Yoshiko Nagamachi,Patricia Caroline Mary O’Brien,Ana Cristina Mendes-Oliveira,Pablo Suárez,Lena Geise,Julio Cesar Pieczarka,Maykon Passos Cristiano

doi:10.1371/journal.pone.0258474

Abstract

Rhipidomys (Sigmodontinae, Thomasomyini) has 25 recognized species, with a wide distribution ranging from eastern Panama to northern Argentina. Cytogenetic data has been described for 13 species with 12 of them having 2n = 44 with a high level of autosomal fundamental number (FN) variation, ranging from 46 to 80, assigned to pericentric inversions. The species are grouped in groups with low FN (46–52) and high FN (72–80). In this work the karyotypes of Rhipidomys emiliae (2n = 44, FN = 50) and Rhipidomys mastacalis (2n = 44, FN = 74), were studied by classical cytogenetics and by fluorescence in situ hybridization using telomeric and whole chromosome probes (chromosome painting) of Hylaeamys megacephalus (HME). Chromosome painting revealed homology between 36 segments of REM and 37 of RMA. We tested the hypothesis that pericentric inversions are the predominant chromosomal rearrangements responsible for karyotypic divergence between these species, as proposed in literature. Our results show that the genomic diversification between the karyotypes of the two species resulted from translocations, centromeric repositioning and pericentric inversions. The chromosomal evolution in Rhipidomys was associated with karyotypical orthoselection. The HME probes revealed that seven syntenic probably ancestral blocks for Sigmodontinae are present in Rhipidomys. An additional syntenic block described here is suggested as part of the subfamily ancestral karyotype. We also define five synapomorphies that can be used as chromosomal signatures for Rhipidomys.

Highlights

The Sigmodontinae subfamily is the most diverse and complex group of cricetid rodents in the New World, with 74 genera and 380 species grouped in 10 tribes (Abrotrichini, Akodontini, Ichthyomyini, Oryzomyini, Phyllotini, Reithrodontini, Sigmodontini, Thomasomyini, Wiedomyini, Euneomyini), and 12 genera not included in any of the mentioned tribes [1,2,3,4].The genus Rhipidomys Tschudi, 1845 is the only arboreal representative of the Thomasomyini tribe [1, 5, 6]
Eleven species occur in the Brazilian biomes [6], among them, Rhipidomys emiliae Allen 1916 is distributed in the Amazon biome and the Amazon-Cerrado ecotone, from Parato Mato Grosso; Rhipidomys mastacalis Lund 1840 is found in the Atlantic Forest biome and in central Brazil [6, 11] (Fig 1)
The results of this work demonstrate that the rearrangements responsible for genomic diversification between the karyotypes of R. emiliae and R. mastacalis and, possibly, of the other species of Rhipidomys, involve a combination of translocations, centromeric repositioning and pericentric inversions

Summary

Introduction

The Sigmodontinae subfamily is the most diverse and complex group of cricetid rodents in the New World, with 74 genera and 380 species grouped in 10 tribes (Abrotrichini, Akodontini, Ichthyomyini, Oryzomyini, Phyllotini, Reithrodontini, Sigmodontini, Thomasomyini, Wiedomyini, Euneomyini), and 12 genera not included in any of the mentioned tribes (incertae sedis) [1,2,3,4].The genus Rhipidomys Tschudi, 1845 is the only arboreal representative of the Thomasomyini tribe [1, 5, 6]. Twenty-five species are currently recognized, with a high degree of morphological similarity that comprises a taxonomically complex group [1, 5,6,7,8,9] The species of this genus range in length from 90 mm to 210 mm, are difficult to capture due to their arboreal habits, and are among the least well-known species in the Neotropical region [5, 6, 10]. Eleven species occur in the Brazilian biomes [6], among them, Rhipidomys emiliae Allen 1916 is distributed in the Amazon biome and the Amazon-Cerrado ecotone, from Parato Mato Grosso; Rhipidomys mastacalis Lund 1840 is found in the Atlantic Forest biome and in central Brazil [6, 11] (Fig 1) These two species form a clade together with the Cerrado species, R. ipukensis Rocha, Costa & Costa, 2011. This latter species is closely related to R. emiliae; together, they form a sister group with R. mastacalis [7, 12]

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Discussion

Conclusion