Ancestral genomic stasis and coordinated genome erosion underlies asymmetric acarine diversification

Abstract

Mites and ticks (Acari) constitute one of the most species-rich and ecologically diverse arachnid radiations, yet their interrelationships and genomic mechanisms underlying their diversification remain poorly resolved. Here, we reconstructed the evolutionary relationships and trajectory of Parasitiformes using phylogenetics and comparative genomics to test the phylogenetic signal in rare genomic changes. Maximum likelihood and macrosynteny analysis revealed multiple shared chromosomal fusion-with-mixing events that unite Opilioacaridae and Ixodida as sister taxa, with Mesostigmata as a derived sister clade, overturning the prior basal placement of Opilioacaridae as a slowly evolving "living fossil" lineage. We show that major parasitiform lineages diversified through asymmetric, large-scale genome and regulatory rewiring. Opilioacaridae genome retains ancestral chelicerate genomic features, including an intact, contiguous Hox gene cluster, high repetitive-element content, and a conserved microRNA repertoire, all shared with Ixodida. By contrast, the hyperdiverse Mesostigmata shows marked genome compaction, with shortened introns, disrupted and fragmented Hox clusters, and widespread loss of microRNA families, despite retention of developmentally essential miRNAs. Comparative analysis of gene-family evolution further identifies lineage-specific expansions in Ixodida associated with blood feeding and immune evasion, alongside independent, convergent expansion of cuticle-protein gene families in ectoparasitic Mesostigmata. These findings demonstrate that contrasting modes of genome evolution, long-term structural stasis versus rapid compaction, together with convergent gene-family expansion linked to independent origins of parasitism, can coexist within a single arachnid radiation, offering new insight into the molecular basis of developmental regulatory evolution and adaptive diversification in Acari.