The rapid variation of Hox clusters reveals a clear evolutionary path in a crucian carp-like homodiploid fish lineage

Abstract

The surprising variation in the number of Hox clusters and genome structure in ray-finned fish lineages reflects the history of duplications and subsequent lineage-specific gene loss. However, there are few studies on whether Hox clusters in the early generations of hybrid lineages show more significant variation due to the continuous genomic oscillation caused by distant hybridization. We sequenced and analyzed Hox gene clusters from a crucian carp-like homodiploid fish (NCRC) lineage (a new hybrid lineage derived from common carp (Cyprinus carpio) (♀) ​× ​blunt snout bream (Megalobrama amblycephala) (♂)). In the NCRC lineage, we reconstructed seven Hox clusters consisting of 48 Hox genes, ten of which were pseudogenes. The number of putative Hox clusters generated in NCRC-F1 was increased greatly by distant hybridization to an average number almost twice that in the maternal parent. This increasing trend continued in the subsequent self-mating generations of NCRC-F1. In contrast, the number of Hox cluster fragments inherited from the original parents gradually decreased as the number of NCRC lineage generations increased. This pattern was also found in the inheritance of recombinant Hox clusters. In terms of base composition, some genetic rules for the inheritance of these Hox clusters between different generations of the NCRC lineage were identified. Furthermore, the newly derived mutated Hox clusters in the NCRC lineage showed phylogenetic relationships that were closer to either crucian carp or silver crucian carp, revealing a clear evolutionary path. This study deepens our understanding of the evolution of Hox genes in the ray-finned fish clade.