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Understanding the evolution of chromatin conformation among species is fundamental to elucidate the architecture and plasticity of genomes. Nonrandom interactions of linearly distant loci regulate gene function in species-specific patterns, affecting genome function, evolution, and, ultimately, speciation. Yet, data from nonmodel organisms are scarce. To capture the macroevolutionary diversity of vertebrate chromatin conformation, here we generate de novo genome assemblies for two cryptodiran (hidden-neck) turtles via Illumina sequencing, chromosome conformation capture, and RNA-seq:Apalone spinifera(ZZ/ZW, 2n= 66) andStaurotypus triporcatus(XX/XY, 2n= 54). We detected differences in the three-dimensional (3D) chromatin structure in turtles compared to other amniotes beyond the fusion/fission events detected in the linear genomes. Namely, whole-genome comparisons revealed distinct trends of chromosome rearrangements in turtles: (1) a low rate of genome reshuffling inApalone(Trionychidae) whose karyotype is highly conserved when compared to chicken (likely ancestral for turtles), and (2) a moderate rate of fusions/fissions inStaurotypus(Kinosternidae) andTrachemys scripta(Emydidae). Furthermore, we identified a chromosome folding pattern that enables “centromere–telomere interactions” previously undetected in turtles. The combined turtle pattern of “centromere–telomere interactions” (discovered here) plus “centromere clustering” (previously reported in sauropsids) is novel for amniotes and it counters previous hypotheses about amniote 3D chromatin structure. We hypothesize that the divergent pattern found in turtles originated from an amniote ancestral state defined by a nuclear configuration with extensive associations among microchromosomes that were preserved upon the reshuffling of the linear genome. 

Abstract Many evolutionary relationships remain controversial despite whole-genome sequencing data. These controversies arise, in part, due to challenges associated with accurately modeling the complex phylogenetic signal coming from genomic regions experiencing distinct evolutionary forces. Here, we examine how different regions of the genome support or contradict well-established relationships among three mammal groups using millions of orthologous parsimony-informative biallelic sites (PIBS) distributed across primate, rodent, and Pecora genomes. We compared PIBS concordance percentages among locus types (e.g. coding sequences (CDS), introns, intergenic regions), and contrasted PIBS utility over evolutionary timescales. Sites derived from noncoding sequences provided more data and proportionally more concordant sites compared with those from CDS in all clades. CDS PIBS were also predominant drivers of tree incongruence in two cases of topological conflict. PIBS derived from most locus types provided surprisingly consistent support for splitting events spread across the timescales we examined, although we find evidence that CDS and intronic PIBS may, respectively and to a limited degree, inform disproportionately about older and younger splits. In this era of accessible wholegenome sequence data, these results:1) suggest benefits to more intentionally focusing on noncoding loci as robust data for tree inference and 2) reinforce the importance of accurate modeling, especially when using CDS data.