Chromosomal diversity and molecular divergence among three undescribed species of Neacomys (Rodentia, Sigmodontinae) separated by Amazonian rivers

Abstract

The Neacomys genus (Rodentia, Sigmodontinae) is distributed in the Amazon region, with some species limited to a single endemic area, while others may occur more widely. The number of species within the genus and their geographical boundaries are not known accurately, due to their high genetic diversity and difficulties in taxonomic identification. In this work we collected Neacomys specimens from both banks of the Tapajós River in eastern Amazon, and studied them using chromosome painting with whole chromosome probes of Hylaeamys megacephalus (HME; Rodentia, Sigmodontinae), and molecular analysis using haplotypes of mitochondrial genes COI and Cytb. Chromosome painting shows that Neacomys sp. A (NSP-A, 2n = 58/FN = 68) and Neacomys sp. B (NSP-B, 2n = 54/FN = 66) differ by 11 fusion/fission events, one translocation, four pericentric inversions and four heterochromatin amplification events. Using haplotypes of the concatenated mitochondrial genes COI and Cyt b, Neacomys sp. (2n = 58/FN = 64 and 70) shows a mean divergence of 6.2% for Neacomys sp. A and 9.1% for Neacomys sp. B, while Neacomys sp. A and Neacomys sp. B presents a medium nucleotide divergence of 7.4%. Comparisons were made with other published Neacomys data. The Tapajós and Xingu Rivers act as geographic barriers that define the distribution of these Neacomys species. Furthermore, our HME probes reveal four synapomorphies for the Neacomys genus (associations HME 20/[13,22]/4, 6a/21, [9,10]/7b/[9,10] and 12/[16,17]) and demonstrate ancestral traits of the Oryzomyini tribe (HME 8a and 8b, 18 and 25) and Sigmodontinae subfamily (HME 15 and 24), which can be used as taxonomic markers for these groups.

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

“…Chromosome-painting data and those obtained using HME whole-chromosome probes were compared between representatives of the Oryzomyini and Akodontini tribes ( Supplementary Table S1). However, we will not discuss herein the signatures of Oryzomyini and its representatives, as we found nothing that we could add to the previous discussion of this from the results with HME probes [8,9,[23][24][25][26]. Rather, we confirm their proposals about the ancestral traits for the Sigmodontinae The Akodontini topology recovered by D'Elía [27] using a Maximum Parsimony strict consensus tree (Cytb and/or IRBP) exhibited five weakly supported divisions (Akodon, Bibimys, Blarinomys, Oxymycterus, and Scapteromys).…”

“…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].…”

“…FISH with HME probes showed 39 hybridization signals in OAM (Figure 2a, Table 3). Twelve autosomes showed conserved synteny; of them, seven (HME 2, 8, 12, 15, 23, 24, and 26) hybridized to whole chromosomes of OAM (8,10,18,19,20,22, and 6, respectively), and five (HME 3,6,19,20,21) hybridized to parts of other chromosomes (OAM 1q distal, 7q proximal, 21q proximal and distal, 14q proximal and 7q distal, respectively). The other 11 autosomal probes showed multiple signals in OAM; nine (HME 1, 4, 7, (9,10), 11, 14, (16,17), 18, and 25) hybridized to two chromosomes each, while HME (13,22) showed signals in three chromosomes and HME 5 showed signals in four chromosomes.…”

“…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.…”