Cross-species chromosome painting in Cetartiodactyla: Reconstructing the karyotype evolution in key phylogenetic lineages

Abstract

Recent molecular and morphological studies place Artiodactyla and Cetacea into the order Cetartiodactyla. Within the Cetartiodactyla such families as Bovidae, Cervidae, and Suidae are well studied by comparative chromosome painting, but many taxa that are crucial for understanding cetartiodactyl phylogeny remain poorly studied. Here we present the genome-wide comparative maps of five cetartiodactyl species obtained by chromosome painting with human and dromedary paint probes from four taxa: Cetacea, Hippopotamidae, Giraffidae, and Moschidae. This is the first molecular cytogenetic report on pilot whale, hippopotamus, okapi, and Siberian musk deer. Our results, when integrated with previously published comparative chromosome maps allow us to reconstruct the evolutionary pathway and rates of chromosomal rearrangements in Cetartiodactyla. We hypothesize that the putative cetartiodactyl ancestral karyotype (CAK) contained 25-26 pairs of autosomes, 2n = 52-54, and that the association of human chromosomes 8/9 could be a cytogenetic signature that unites non-camelid cetartiodactyls. There are no unambiguous cytogenetic landmarks that unite Hippopotamidae and Cetacea. If we superimpose chromosome rearrangements on the supertree generated by Price and colleagues, several homoplasy events are needed to explain cetartiodactyl karyotype evolution. Our results apparently favour a model of non-random breakpoints in chromosome evolution. Cetariodactyl karyotype evolution is characterized by alternating periods of low and fast rates in various lineages. The highest rates are found in Suina (Suidae+Tayasuidae) lineage (1.76 rearrangements per million years (R/My)) and the lowest in Cetaceans (0.07 R/My). Our study demonstrates that the combined use of human and camel paints is highly informative for revealing evolutionary karyotypic rearrangements among cetartiodactyl species.