Defining the ancestral eutherian karyotype: A cladistic interpretation of chromosome painting and genome sequence assembly data

Abstract

A cladistic analysis of genome assemblies (syntenic associations) for eutherian mammals against two distant outgroup species--opossum and chicken--permitted a refinement of the 46-chromosome karyotype formerly inferred in the ancestral eutherian. We show that two intact chromosome pairs (corresponding to human chromosomes 13 and 18) and three conserved chromosome segments (10q, 19p and 8q in the human karyotype) are probably symplesiomorphic for Eutheria because they are also present as unaltered orthologues in one or both outgroups. Seven additional syntenies (4q/8p/4pq, 3p/21, 14/15, 10p/12pq/22qt, 19q/16q, 16p/7a and 12qt/22q), each involving human chromosomal segments that in various combinations correspond to complete chromosomes in the ancestral eutherian karyotype, are also present in one or both outgroup taxa and thus are probable symplesiomorphies for Eutheria. Interestingly, several of the symplesiomorphic characters identified in chicken and/or opossum are present in more distant outgroups such as pufferfish and zebrafish (for example 3p/21, 14/15, 19q/16q and 16p/7a), suggesting their retention since vertebrate common ancestry approximately 450 million years ago. However, eight intact pairs (corresponding to human chromosomes 1, 5, 6, 9, 11, 17, 20 and the X) and three chromosome segments (7b, 2p-q13 and 2q13-qter) are derived characters potentially consistent with eutherian monophyly. Our analyses clarify the distinction between shared-ancestral and shared-derived homology in the eutherian ancestral karyotype.

Molecular cytogenetic and genomic insights into chromosomal evolution

“…In the present context, it is important to make the distinction between segmental associations (the adjacent syntenies of some terminologies) and syntenic blocks that are retained in toto among lineages. The detection of segmental associations such as 4q/8p/4pq, 3p/21, 14/15, 10p/12pq/ 22qt, 16q/19q, 7a/16p and 12qt/22q (each of which involve segments of human chromosomes that in combination correspond to complete chromosomes in the ancestral eutherian karyotype) in placentals, chicken and opossum was based on the evidence of the entire adjacent segment having been retained in representative genomes (Robinson and Ruiz-Herrera, 2008). However, the incomplete nature of the genome assemblies of platypus and frog does not permit the same level of resolution.…”

“…This permitted the distinction between shared ancestral characters (symplesiomorphies) and those that are unique to the ingroup Placentalia (that is, showing shared derived similarity and referred to as synapomorphies) allowing firm conclusions on the evolutionary history of each (Robinson and Ruiz-Herrera, 2008). The PAK is considered to comprise two chromosome pairs (corresponding to human chromosomes 13 and 18) and three conserved chromosome segments (10q, 19p and 8q in the human karyotype) that are probable symplesiomorphies as they are also present as unaltered orthologues in one or both outgroup species.…”

The evolutionary history of HSA7/16 synteny in vertebrates: a critical interpretation of comparative cytogenetic and genome sequence data

“…The first (Figure 1a), takes into account the genome organization in Aves (Gallus gallus, GGA) and Metatherian (Monodelphis domestica-MDO) (see also Robinson & Ruiz-Herrera 2008). M. domestica (chromosome 6-MDO6) and G. gallus (chromosome 14) are characterized by the HSA7a 1 /16, where 7a 1 has a 7p22-pter composition.…”

The evolution of human synteny 4 by mapping sub-chromosomal specific probes in Primates

“…Starting from the proposed ancestral genome of primates (Ferguson-Smith and Trifonov 2007;Robinson and Ruiz-Herrera 2008) it has been possible to reconstruct the most important steps leading to the formation of human chromosomes over the last 100 million years (Stanyon et al 2008). However, although chromosome painting gives considerable data on inter-chromosomal rearrangements (translocations), the knowledge of intra-chromosomal rearrangements in the different lineages remains limited.…”

“…In most mammals the homologues to human chromosome 4 are associated with the small arm of the human chromosome 8 (4/8p) (Richard et al 2001;Svartman et al 2004;Wienberg 2005;Dumas et al 2012). For this reason, and because of the 4/8 association is present in the marsupial Monodelphis domestica (Mikkelsen et al 2007) and in the bird Gallus gallus (Murphy et al 2005;Robinson and Ruiz-Herrera 2008), it has been considered as an ancestral association in the reconstruction of the ancestral karyotype of all eutherian mammals (Ferguson-Smith and Trifonov 2007;Stanyon et al 2008). As already demonstrated (Graphodasky et al 2011), the 4/8 association has been subject to numerous rearrangements, forming new associations with other (human) syntenies in Muridae and Canidae or it has even been diversely disrupted in Primates (Stanyon et al 2008), Sirenia (Kellog et al 2007) and Proboscidea (Yang et al 2003).…”