Low, Complex and Probably Reticulated Chromosome Evolution of Sciuromorpha (Rodentia) and Lagomorpha

Abstract

Lagomorpha (rabbits and pikas) and Sciuromorpha (squirrels) are grouped in the Glires superorder. Their chromosome diversification, since their separation from the eutherian mammalian common ancestor, was characterized by a low rate of chromosome rearrangements. Consequently, the structure of some chromosomes was either conserved or only slightly modified, making their comparison easy at the genus, family and even order level. Interspecific in situ hybridization (Zoo-FISH) largely corroborates classical cytogenetic data but provides much more reliability in comparisons, especially for distant species. We reconstructed common ancestral karyotypes for Glires, Lagomorpha, Sciuromorpha, and Sciuridae species, and then, determined the chromosome changes separating these ancestors from their common eutherian ancestor. We propose that reticulated evolution occurred during the diversification of Glires, which implies that several pericentric inversions and Robertsonian translocations were conserved in the heterozygous status for an extensive period. Finally, among Lagomorpha and Sciuromorpha, we focused on Leporidae and Sciuridae chromosome evolution. In the various attempts to establish dichotomic evolutionary schemes, it was necessary to admit that multiple homoplasies (convergent and reverse rearrangements) occurred in Sciuridae and in a lesser degree, in Leporidae. In Leporidae, additional rearrangements were sufficient to propose a resolved phylogeny. However, a resolved phylogeny was not possible for Sciuridae because most of the rearrangements occurred in terminal branches. We conclude that a reticulated evolution took place early during the evolution of both families and lasted longer in Sciuridae than in Leporidae. In Sciuridae, most chromosome rearrangements were pericentric inversions involving short fragments. Such rearrangements have only mild meiotic consequences, which may explain the long persistence of the heterozygous status characterizing reticulated evolution.

A First Generation Comparative Chromosome Map between Guinea Pig (Cavia porcellus) and Humans

“…[ 22 , 23 ]). Although comparisons between human and rodent genomes using chromosome painting have had limited success, results in Sciuromorpha, Castorimorpha, and Anomaluromorpha showed that most of the ancestral eutherian syntenic associations were conserved [ 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 ]. However, some rodents such as Myomorpha have experienced massive chromosomal rearrangements [ 32 ].…”

Karyotype diversity suggests that Laonastes aenigmamus (Laotian rock rat) (Rodentia, Diatomyidae) is a multi-specific genus

“…The main characteristic of the various karyotypes of Laonastes is the presence of very large chromosomes, obviously derived from multiple rearrangements, as demonstrated by the presence of up to eight fragments homologous to human chromosomes on a single chromosome. In these large chromosomes, no additional adjacent syntheny corresponds to those proposed for the ancestors of other rodents such as Glires, Sciuridae, or Muroidea (Romanenko et al 2006;Graphodatsky et al 2008;Sannier et al 2011;Beklemisheva et al 2011;Richard and Dutrillaux 2012). Interestingly, the size increase of some chromosomes was a tendency yet at work in the evolution of genus Laonastes: three of the six rearrangements differentiating the karyotypes of our specimens are tandem fusions increasing the size of pairs 3 and 4.…”

A review of bristly ground squirrels Xerini and a generic revision in the African genus Xerus

“…The X chromosome is submetacentric in all species while the small Y chromosomes is acrocentric in Euxerus and metacentric in Xerus, both species of Geo sciurus and Spermophilopsis; the details are not known for Atlantoxerus. Differences in morphology of the Y chromosome most probably originate from the pericentric inversion which is the predominant drive of chromosomal change in squirrels (Richard and Dutrillaux 2012). Such differences provide little useful information for phylogenetic reconstructions of interrelationships in Sciuridae because of convergent and reverse rearrangements of the karyotype (Romanenko et al 2011, Richard andDutrillaux 2012).…”

“…Differences in morphology of the Y chromosome most probably originate from the pericentric inversion which is the predominant drive of chromosomal change in squirrels (Richard and Dutrillaux 2012). Such differences provide little useful information for phylogenetic reconstructions of interrelationships in Sciuridae because of convergent and reverse rearrangements of the karyotype (Romanenko et al 2011, Richard andDutrillaux 2012). Evidently, Xerini have retained a conservative karyotype which remains similar to the ancestral condition in squirrels (Li et al 2006, Beklemisheva et al 2011).…”