Reconstruction of hundreds of reference ancestral genomes across the eukaryotic kingdom

Abstract

Ancestral sequence reconstruction is a fundamental aspect of molecular evolution studies and can trace small-scale sequence modifications through the evolution of genomes and species. In contrast, fine-grained reconstructions of ancestral genome organizations are still in their infancy, limiting our ability to draw comprehensive views of genome and karyotype evolution. Here we reconstruct the detailed gene contents and organizations of 624 ancestral vertebrate, plant, fungi, metazoan and protist genomes, 183 of which are near-complete chromosomal gene order reconstructions. Reconstructed ancestral genomes are similar to their descendants in terms of gene content as expected and agree precisely with reference cytogenetic and in silico reconstructions when available. By comparing successive ancestral genomes along the phylogenetic tree, we estimate the intra- and interchromosomal rearrangement history of all major vertebrate clades at high resolution. This freely available resource introduces the possibility to follow evolutionary processes at genomic scales in chronological order, across multiple clades and without relying on a single extant species as reference.

Inferring inter-chromosomal rearrangements and ancestral linkage groups from synteny

“…This problem could be alleviated by considering four or five closely related genomes at a time (at the expense of computation time) or by using a weighted graph as in Kim et al . (2017) and Muffato et al . (2023).…”

“…Chromosome rearrangements are another mechanism by which genomes undergo large-scale changes, and they are common across eukaryotes (Zhao and Schranz 2019; Li et al . 2022; Muffato et al . 2023).…”

“…2022). Typically, such analyses rely on genome sequences or linkage map data for tens of genomes (or less), but it is becoming more common to analyse hundreds of chromosome-level genome assemblies (Muffato et al . 2023; Wright et al .…”

“…This task is straightforward when gene-order is well conserved, but becomes more challenging when the intra-chromosomal rearrangement rate is high or if taxa are very distantly related (Farré et al . 2019; Muffato et al . 2023).…”

Evolution of the spider homeobox gene repertoire by tandem and whole genome duplication

“…Hierarchical orthogroups (HOGs) of all non-homeobox genes were identified using Orthofinder (Emms and Kelly 2019) with default settings, specifying the species tree: ((Dmel,Tcas)N1,(Isca,(Dsil,((Ptep,Lele)N5,(Hgra,(Abru,(Tcla,Tant)N8)N7) N6)N4)N3)N2)N0);. These were combined with HOGs of our homeobox orthology and used to reconstruct ancestral gene orders with Agora (Muffato et al 2023), using the basic pipeline. However, we used Agora to illustrate chromosomes with macrosynteny and orthology relationships, rather than the ancestral synteny blocks, termed Contiguous Ancestral Regions (CARs) detected by Agora, because it resolved a better signal of chromosomal rearrangements across the whole genome compared to the smaller coverage of CARs.…”