Abstract
South American subterranean rodents of the genus Ctenomys are among the most diverse mammals at the species level, integrating a monotypic family of recent origin. Contrasting with their general morphological conservatism, chromosome variability is very high. Also, molecular data showed a shallow genetic divergence within several species groups with mitochondrial markers, leaving doubts about the taxonomic status of some lineages and the evolutionary significance of their chromosomal diversity. Here, we reviewed and reanalysed published chromosome data of Ctenomys and contrasted it with molecular data, including ancestral chromosomal state reconstructions in a phylogenetic hypothesis based on mitochondrial cytochrome b gene sequences. One hundred seventy-eight different chromosome complements were recorded for 48 Ctenomys species. Some species are polymorphic and/or polytypic, with differentiated populations. Both 2n and FNa showed a wide variation, but FNa had a greater dispersion. With the exceptions of C. lessai and C. maulinus, in all other species, the X chromosome is biarmed. The Y chromosome is quite variable in morphology and size. In general, biarmed and uniarmed autosomes within karyotypes are nearly equally represented, departing from the pattern of other mammals. This may be due to fast-evolving heterochromatin. The chromosomal reconstructions suggest that the ancestral karyotype of the genus could have had an intermediate 2n and high FNa. Most of the species groups recovered in the phylogeny show wide chromosomal variability, the most extreme being the torquatus group. This diversity was apparently generated in a short time, indicating an accelerated rate of chromosome evolution in this clade and the whole family.
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Acknowledgements
We are very grateful to Dr. Claudio J. Bidau for making us see the world through the light of evolution and transmitting his passion for knowledge. We thank the anonymous referees for their critical review of an early version of this paper. The authors thank to the Consejo Nacional de Investigaciones Científicas y Técnicas. This work was partially financed by PIP-CONICET 2015-0258 CO, PICT 2016-0537, and PICT 2020-01989.
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Supplementary Information
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Supplementary file1 Complete phylogenetic hypothesis obtained by the Bayesian analysis of the molecular dataset of cytochrome b gene sequences. Species groups recovered are in boxes. Numbers above the nodes are posterior probabilities in the Bayesian inference (JPG 7714 KB)
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Supplementary file2 Phylogenetic hypothesis obtained by the Maximum Parsimony analysis of the molecular dataset of cytochrome b gene sequences. Species groups recovered are in boxes. Numbers below the nodes are bootstrap supports (JPG 5688 KB)
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Supplementary file3 Phylogenetic hypothesis obtained by the Maximun Likelihood analysis of the molecular dataset of cytochrome b gene sequences. Species groups recovered are in boxes. Numbers below the nodes are bootstrap supports (JPG 7681 KB)
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Supplementary file4 Diploid number (2n), fundamental number of autosomal arms (FNa), number of autosomes (NA), number of bi-armed and acrocentric chromosomes, % of acrocentric chromosomes, morphology, and size of sex chromosomes (meta= metacentric, submeta=submetacentric, subtelo= subtelocentric, acro= acrocentric), and bibliographic references. Names between parenthesis correspond to those used in the original references. In quotation marks are informal names. In bold are numbers used in the reduced dataset. Numbers in the first column (N°) correspond to the nominal species count (XLSX 29 KB)
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Supplementary file5 Sequences used in phylogenetic analyses. Species name, group to which it belongs, and chromosomal data related to those sequences. The codes used in the ancestral state reconstructions of chromosome characters are indicated in square brackets (first the 2n and second the FNa). Green cells indicate sequences to which part of chromosomal variability of the species was added but which do not belong to that sequence (XLSX 39 KB)
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Supplementary file6 Uncorrected p-genetic distances of mitochondrial cytochrome b gene sequences of Ctenomys, and other octodontids obtained from GenBank. The distances involving the outgroups are indicated. The species groups are shown in boxes. Numbers in red indicate intraspecific distances. In yellow are marked low values of interspecific distances. In light blue are marked high values of intraspecific distances (XLSX 166 KB)
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Supplementary file7 Uncorrected p-genetic distances of mitochondrial cytochrome b gene of all available sequences of Ctenomys species. The curated dataset included 372 nucleotide sequences belonging to 49 Ctenomys species. (a) Intraspecific comparisons. (b) Interespecific comparisons. (c) Complete dataset (XLS 1792 KB)
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Buschiazzo, L.M., Caraballo, D.A., Labaroni, C.A. et al. Comprehensive cytogenetic analysis of the most chromosomally variable mammalian genus from South America: Ctenomys (Rodentia: Caviomorpha: Ctenomyidae). Mamm Biol 102, 1963–1979 (2022). https://doi.org/10.1007/s42991-022-00312-9
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DOI: https://doi.org/10.1007/s42991-022-00312-9