Reconstruction of karyotype evolution in core Glires. I. The genome homology revealed by comparative chromosome painting

Abstract

Glires represent a eutherian clade consisting of rodents and lagomorphs (hares, rabbits, and pikas). Chromosome evolution of Glires is known to have variable rates in different groups: from slowly evolving lagomorphs and squirrels to extremely rapidly evolving muroids. Previous interordinal homology maps between slowly evolving Glires were based on comparison with humans. Here, we used sets of chromosome-specific probes from Tamias sibiricus (Sciuridae), Castor fiber (Castoridae) and humans to study karyotypes of six ground squirrels (genera Marmota and Spermophilus) and one tree squirrel (genus Sciurus), mountain hare (genus Lepus), and rabbit (genus Oryctolagus). These data supplemented with GTG banding comparisons allowed us to build comparative chromosome maps. Our data showed the absence of previously found squirrel associations HSA 1/8 and 2/17 in the Eurasian ground squirrels--sousliks and woodchucks, and disruptions of squirrel HSA 10/13 and HSA 8/4/8/12/22 syntenies in the four Spermophilus species studied here. We found that the karyotypes of Sciuridae and Leporidae are highly conserved and close to the Rodentia ancestral karyotype, while Castoridae chromosomes underwent many more changes. We suggest that Lagomorpha and Sciuridae (in contrast to all other rodent families) should be considered as core Glires lineages, characterized by cytogenetically conserved karyotypes which contain chromosomal elements inherent to karyotype of common Glires ancestor. Our data allowed us to further refine the putative ancestral karyotypes of Rodentia. We also describe here the putative ancestral karyotypes of Glires and lagomorphs.

Chromosomal evolution in Rodentia

“…Three species of Gliridae have also been studied. These investigations relied predominantly on human (Homo sapiens, HSA) paints, although two sciuromorph-specific sets of painting probes were developed from the flow-sorted chromosomes of Sciurus carolinensis and Tamias sibiricus and used in comparative painting experiments (Li et al, 2004;Beklemisheva et al, 2011).…”

“…The HSA 1/8 and HSA 2/17 associations previously found in sciuromorphs (and considered to represent the sciurid ancestral condition) are absent in the Eurasian ground squirrels-sousliks and woodchucks-while HSA 10/ 13 and HSA 8/4/8/12/22 are disrupted in four Spermophilus species. Some ground squirrels (Xerus, Menetes) and the flying squirrel (Petaurista) have highly conserved karyotypes that are probably very similar to the ancestral squirrel karyotype and do not differ significantly from that of Rodentia (Richard et al, 2003;Stanyon et al, 2003;Li et al, 2004Li et al, , 2006aBeklemisheva et al, 2011). In contrast to the general conservation of syntenic groups, most sciurid genomes are characterized by variation in the size and distribution of heterochromatin; additionally, multiple centromeric shifts have been reported in some species (Beklemisheva et al, 2011).…”

“…Some ground squirrels (Xerus, Menetes) and the flying squirrel (Petaurista) have highly conserved karyotypes that are probably very similar to the ancestral squirrel karyotype and do not differ significantly from that of Rodentia (Richard et al, 2003;Stanyon et al, 2003;Li et al, 2004Li et al, , 2006aBeklemisheva et al, 2011). In contrast to the general conservation of syntenic groups, most sciurid genomes are characterized by variation in the size and distribution of heterochromatin; additionally, multiple centromeric shifts have been reported in some species (Beklemisheva et al, 2011). Importantly, however, because of the slow rate of karyotype change and some convergence of characters, cytogenetic evidence failed to resolve close associations within Sciuridae.…”

“…The availability of comparative banding and painting data led to suggestions of a putative ancestral karyotype for Sciuridae (Richard et al, 2003;Li et al, 2004;Beklemisheva et al, 2011). The consensus is that this comprised 38 elements corresponding to the following human chromosomes and/or segmental associations: HSA 9/11, 1/ 10p, 3/21, 16q/19q, 7/16p, 20/15/14, 1pq/8q, 10q/13, 2q/17, 7/ 22qprox/12qdist, 8p/4q/8p/12pq/22qdiss, 3/19p (Supplement Data 3) (Li et al, 2004(Li et al, , 2006aBeklemisheva et al, 2011).…”

“…The consensus is that this comprised 38 elements corresponding to the following human chromosomes and/or segmental associations: HSA 9/11, 1/ 10p, 3/21, 16q/19q, 7/16p, 20/15/14, 1pq/8q, 10q/13, 2q/17, 7/ 22qprox/12qdist, 8p/4q/8p/12pq/22qdiss, 3/19p (Supplement Data 3) (Li et al, 2004(Li et al, , 2006aBeklemisheva et al, 2011). The karyotypes of Gliridae are also relatively conserved.…”