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

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.

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

“…Hass et al (2008) compared Mus musculus (family Muridae) to Akodon species (family Cricetidae); Nagamachi et al (2013) compared two different, unrelated genera of the tribe Oryzomiyni (Cerradomys and Hylaeamys) and Suárez et al (2015) and Pereira et al (2016) compared homologies between the tribes Akodontini and Oryzomyini.…”

“…Comparisons between Hylaeamys megacephalus (G. Fischer, 1814) and Cerradomys langguthi Percequillo, Hingst-Zaher & Bonvicino, 2008 were performed by Nagamachi et al (2013), and Di-Nizo et al (2015) studied chromosome evolution within the genus Oligoryzomys. In addition, chromosome painting using Hylaeamys megacephalus probes was performed to compare the Akodontini and Oryzomyini tribes (Suárez et al 2015, Pereira et al 2016) and, more recently, two populations of Oecomys catherinae Thomas, 1909 were also evaluated (Malcher et al 2017). …”

Chromosomal Signatures Corroborate the Phylogenetic Relationships within Akodontini (Rodentia, Sigmodontinae)

“…For example, the karyotype with 2n = 28, FN = 50 was assessed only by G-banding and telomeric FISH techniques [42]. Taking into account that comparative cytogenetic data are often phylogenetically informative [14] and chromosomal signatures are maintained in rodent lineages regardless of the high rate of chromosomal change that may occur within each group [9,25], we set out to detect chromosomal signatures that can be used as phylogenetic markers to elucidate the phylogenetic relationships of some Akodontini members. Towards this, we performed comparative chromosome painting using HME whole-chromosome probes [23] on representatives from three Akodontini divisions [27]: Oxymycterus amazonicus (Oxymycterus division; present work), Blarinomys breviceps (Blarinomys division; present work), Akodon sp., A. montensis, Necromys lasiurus, and Thaptomys nigrita (Akodon division) [24,25]; we also compared these species with data obtained using HME probes in other taxa [8,9,23,26].…”

“…Data obtained with whole-chromosome probes from Mus musculus (MMU) were used to propose chromosomal signatures MMU 3/18 and 6/12 for the Sigmodontinae subfamily (Rodentia, Cricetidae) [7,20,21] but, considering that the mouse chromosomes are highly reorganized, the authors did not attempt to reconstruct the putative ancestral karyotype of this subfamily. More recently, Sigmodontinae rodents have been analyzed by chromosome painting with whole-chromosome probes of a subfamily member, Hylaeamys megacephalus (HME) on representatives of the Oryzomyini and Akodontini lineages [8,9,[22][23][24][25][26]. These studies have shed light on the karyotype evolution of New World rodents demonstrating syntenic associations for Sigmodontinae: HME 7/(9,10), 1/12, 6/21, 20/(13,22), 19/14 /19, 8, 11/(16,17), 5/(16,17), 15, 24, and 26.…”

“…These studies have shed light on the karyotype evolution of New World rodents demonstrating syntenic associations for Sigmodontinae: HME 7/(9,10), 1/12, 6/21, 20/(13,22), 19/14 /19, 8, 11/(16,17), 5/(16,17), 15, 24, and 26. In Akodontini, four species of three genera (Akodon, Thaptomys, and Necromys) were analyzed and the associations HME 2/18, 3/25, 18/25, and 4/11/ (16,17) were identified as traits for this tribe [25].…”