Chromosomal phylogeny and comparative chromosome painting among Neacomys species (Rodentia, Sigmodontinae) from eastern Amazonia

Abstract

Background The Neacomys genus is predominantly found in the Amazon region, and belongs to the most diverse tribe of the Sigmodontinae subfamily (Rodentia, Cricetidae, Oryzomyini). The systematics of this genus and questions about its diversity and range have been investigated by morphological, molecular (Cytb and COI sequences) and karyotype analysis (classic cytogenetics and chromosome painting), which have revealed candidate species and new distribution areas. Here we analyzed four species of Neacomys by chromosome painting with Hylaeamys megacephalus (HME) whole-chromosome probes, and compared the results with two previously studied Neacomys species and with other taxa from Oryzomyini and Akodontini tribes that have been hybridized with HME probes. Maximum Parsimony (MP) analyses were performed with the PAUP and T.N.T. software packages, using a non-additive (unordered) multi-state character matrix, based on chromosomal morphology, number and syntenic blocks. We also compared the chromosomal phylogeny obtained in this study with molecular topologies (Cytb and COI) that included eastern Amazonian species of Neacomys, to define the phylogenetic relationships of these taxa. Results The comparative chromosome painting analysis of the seven karyotypes of the six species of Neacomys shows that their diversity is due to 17 fusion/fission events and one translocation, pericentric inversions in four syntenic blocks, and constitutive heterochromatin (CH) amplification/deletion of six syntenic autosomal blocks plus the X chromosome. The chromosomal phylogeny is consistent with the molecular relationships of species of Neacomys. We describe new karyotypes and expand the distribution area for species from eastern Amazonia and detect complex rearrangements by chromosome painting among the karyotypes. Conclusions Our phylogeny reflects the molecular relationships of the Akodontini and Oryzomyini taxa and supports the monophyly of Neacomys. This work presents new insights about the chromosomal evolution of this group, and we conclude that the karyotypic divergence is in accord with phylogenetic relationships.

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

“…Several studies using chromosome painting were able to detect conserved syntenic associations shared among distinct taxa (chromosomal signatures). These signatures have been used in the construction of chromosomal topologies and as phylogenetic markers, as they are often group-specific, evolutionarily conserved, and phylogenetically informative, and corroborate the phylogenetic relationships obtained from molecular topologies [2,3,9,10,[12][13][14][15][16][17]. As an example, the monophyly of Afrotheria was debated due to the lack of morphological evidence, but the identification of syntenic associations HSA 1/19 and 5/21 provided support for the Afrotheria monophyly [5].…”

“…We also compared the distribution of constitutive heterochromatin and noticed that four previously reported karyomorphs (2n = 52, 43, 37, 31) had heterochromatin signals in the pericentromeric regions of only some autosomes [42], while our karyotype (2n = 28; MN68882) presented heterochromatin in all autosomes. Differences in the amount of constitutive heterochromatin in karyotypes of the same species or genus are frequent in rodents [45], as observed in Neacomys that showed heterochromatin blocks in from three to five bi-armed pairs among samples from distinct localities in eastern Amazon [9,46].…”

“…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].…”

“…In some mammalian orders that exhibit extensive karyotypic diversification (e.g., Artiodactyla, Carnivora, Chiroptera, and Rodentia), comparative analysis of chromosome-painting data has revealed the occurrence of complex rearrangements that were not identified by classical cytogenetics alone (conventional staining, C-, G-banding) [7][8][9][10][11][12][13]. The Asian muntjacs (Artiodactyla) exhibit chromosomal variability from 2n = 6/7 in Muntiacus muntjak vaginalis to 2n = 46 in Muntiacus reevesi; this was most likely caused by tandem and centromeric fusions from a hypothetical ancestral karyotype with 46 chromosomes [12].…”

“…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.…”