Individual gene translocations during metazoan evolution

In contrast to the extensively studied translocation of large sections of DNA between chromosomes, this paper investigates the translocation of individual genes onto different chromosomes during metazoan evolution. We begin by extending the analysis of deeply conserved synteny of metazoan chromosomes reported by Simakov et al. (2022) [Science Advances 8:eabi5884] to a set of 46 invertebrate species that have annotated chromosome-level genome assemblies, and in each species we map the extant chromosome(s) that represent the proposed 29 ancestral chromosomes. Then, for more than 6000 gene families, we extract orthologs across the 46 species and we interrogate the patterns of chromosomes on which those orthologs reside, to determine a consensus ancestral chromosome for each gene family. A substantial proportion of families exhibit outliers, where the gene for a given species resides on an 'unexpected' chromosome, and we search for and locate ancestral gene translocation events that can explain batches of unexpected chromosomes across multiple species within a clade. We compare our orthology inference under three conditions: unconstrained; constrained to expected chromosomes; and conditional, where there is a preference for expected chromosomes. For the conditional case, we identify 4740 ancestral translocations plus 7164 subsequent translocations (a total of 11,904 gene translocations) within the 6495 gene families represented across our selection of 46 species from 32 clades. Correlating translocation numbers with branch length in the time tree indicates a very low translocation rate, below 1% of gene families per 100 million years (My) in our selected taxa.