Karyotype Evolution in 10 Pinniped Species: Variability of Heterochromatin versus High Conservatism of Euchromatin as Revealed by Comparative Molecular Cytogenetics

Abstract

Pinnipedia karyotype evolution was studied here using human, domestic dog, and stone marten whole-chromosome painting probes to obtain comparative chromosome maps among species of Odobenidae (Odobenus rosmarus), Phocidae (Phoca vitulina, Phoca largha, Phoca hispida, Pusa sibirica, Erignathus barbatus), and Otariidae (Eumetopias jubatus, Callorhinus ursinus, Phocarctos hookeri, and Arctocephalus forsteri). Structural and functional chromosomal features were assessed with telomere repeat and ribosomal-DNA probes and by CBG (C-bands revealed by barium hydroxide treatment followed by Giemsa staining) and CDAG (Chromomycin A3-DAPI after G-banding) methods. We demonstrated diversity of heterochromatin among pinniped karyotypes in terms of localization, size, and nucleotide composition. For the first time, an intrachromosomal rearrangement common for Otariidae and Odobenidae was revealed. We postulate that the order of evolutionarily conserved segments in the analyzed pinnipeds is the same as the order proposed for the ancestral Carnivora karyotype (2n = 38). The evolution of conserved genomes of pinnipeds has been accompanied by few fusion events (less than one rearrangement per 10 million years) and by novel intrachromosomal changes including the emergence of new centromeres and pericentric inversion/centromere repositioning. The observed interspecific diversity of pinniped karyotypes driven by constitutive heterochromatin variation likely has played an important role in karyotype evolution of pinnipeds, thereby contributing to the differences of pinnipeds’ chromosome sets.

A chromosome-length assembly of the Hawaiian Monk seal (Neomonarchus schauinslandi) confirms genomic stability in the Pinnipeds and a prolonged history of “genetic purging”

“…All the pinnipeds for which chromosomal-length assemblies are available have well conserved synteny. Our D-GENIES comparisons of RE74 to other seals are in agreement with their relatedness both in terms of chromosome counts and overall synteny and supports previous cytogenetics studies (e.g., Beklemisheva et al, 2020). The genome of the domestic cat also shows similarity to the pinnipeds with several autosomes completely syntenic suggesting that seals and felids may share a conserved genome architecture with early carnivorans.…”

“…We interpret this result to mean that many of the missing genes are truly absent in these related taxa and reflect a shared history or shared biology. (Beklemisheva, et al, 2020). Our earlier methods could not definitively resolve the correct number of HMS chromosomes but the addition of Hi-C confirmed 16 autosomes.…”

“…Arnason (1974) observed that pinniped chromosomes show “pronounced karyotypic uniformity” and have either 15 or 16 autosomes (Beklemisheva, et al, 2020). Our earlier methods could not definitively resolve the correct number of HMS chromosomes but the addition of Hi-C confirmed 16 autosomes.…”

Derivation of ringed seal (Phoca hispida) induced multipotent stem cells

“…1974). We also observed a certain proportion of tetraploid cells in primary fibroblast cell lines established from different pinniped species (Beklemisheva et al, 2020. This feature depended on the passage number, but the species karyotypes were found to be stable in diploid cells.…”

Genomics of Adaptation and Speciation

“…Answering questions about speciation, adaptation, and extinction does not require the newest and most advanced sequencing technologies, and limited sets of data can be used. The examples in this issue included studies of large structural and chromosomal variation [9,13] However, newer, more contiguous assemblies may allow for a better estimation of the genetic diversity, localization, and visualization of the distribution of genome diversity in the evolutionary context of adaptation and speciation [21] (Totikov et al, 2021).…”