Extensive Chromosomal Reorganization in the Evolution of New World Muroid Rodents (Cricetidae, Sigmodontinae): Searching for Ancestral Phylogenetic Traits.

Adenilson Leão Pereira,Patricia Caroline Mary O’Brien,Stella Miranda Malcher,Julio Cesar Pieczarka,Malcolm Andrew Ferguson-Smith,Cleusa Yoshiko Nagamachi,Ana Cristina Mendes-Oliveira,Riccardo Castiglia

doi:10.1371/journal.pone.0146179

Abstract

Sigmodontinae rodents show great diversity and complexity in morphology and ecology. This diversity is accompanied by extensive chromosome variation challenging attempts to reconstruct their ancestral genome. The species Hylaeamys megacephalus–HME (Oryzomyini, 2n = 54), Necromys lasiurus—NLA (Akodontini, 2n = 34) and Akodon sp.–ASP (Akodontini, 2n = 10) have extreme diploid numbers that make it difficult to understand the rearrangements that are responsible for such differences. In this study we analyzed these changes using whole chromosome probes of HME in cross-species painting of NLA and ASP to construct chromosome homology maps that reveal the rearrangements between species. We include data from the literature for other Sigmodontinae previously studied with probes from HME and Mus musculus (MMU) probes. We also use the HME probes on MMU chromosomes for the comparative analysis of NLA with other species already mapped by MMU probes. Our results show that NLA and ASP have highly rearranged karyotypes when compared to HME. Eleven HME syntenic blocks are shared among the species studied here. Four syntenies may be ancestral to Akodontini (HME2/18, 3/25, 18/25 and 4/11/16) and eight to Sigmodontinae (HME26, 1/12, 6/21, 7/9, 5/17, 11/16, 20/13 and 19/14/19). Using MMU data we identified six associations shared among rodents from seven subfamilies, where MMU3/18 and MMU8/13 are phylogenetic signatures of Sigmodontinae. We suggest that the associations MMU2entire, MMU6proximal/12entire, MMU3/18, MMU8/13, MMU1/17, MMU10/17, MMU12/17, MMU5/16, MMU5/6 and MMU7/19 are part of the ancestral Sigmodontinae genome.

Highlights

Muroids are the most diverse group of extant rodents, with approximately 1500 species distributed in six families [1]
In the present study we found all syntenies between the karyotypes of Hylaeamys megacephalus (HME) and Necromys lasiurus (NLA), including rearrangements not found before in mapping between Mus musculus (MMU) and NLA [22], such as the insertion or inversion that led to NLA15 (HME19/14/19; Fig 1a) or the translocation that led to NLA14 (HME5/22; Fig 1a)
In the map of Hass et al [22], chromosome NLA16 did not show any homology with MMU

Summary

Introduction

Muroids are the most diverse group of extant rodents, with approximately 1500 species distributed in six families [1]. Sigmodontinae comprises approximately 400 species with the tribes Akodontini, Abothrichini, Ichthyomyini, Oryzomyini, Phyllotini, Reithrodontini, Sigmodontini, Thomasomyini, Wiedomyini and Euneomyini, and 381 of these species are present in South America [1, 4,5,6,7]. Recent phylogenetic studies based on molecular data recognize this subfamily and its ten tribes as a monophyletic group [3, 7,8,9,10]. Two of these tribes are noteworthy for their taxonomic complexity, diversity and number of species. Akodontini is the second most speciose tribe, with 85 species in 15 genera, mainly in the tropical and sub-tropical forests of South America [1, 5]

Methods

Results

Conclusion