Genomic expansion in the dark: A repeat-rich genome of a cave-dwelling remipede sheds light on the evolution of the hexapod sister group.

Abstract

Remipedes are enigmatic blind, venomous crustaceans endemic to anchialine cave ecosystems (aphotic, hypoxic subterranean environments) and occupy a pivotal phylogenomic position within Pancrustacea as the sister group to Hexapoda. A high-quality genome assembly has long proven elusive for this taxon, due to accessibility challenges and the fragility of remipedes when removed from their habitat. Here we present a highly contiguous, chromosome-level genome assembly for the remipede Xibalbanus tulumensis (Xibalbanidae) spanning 8.05 Gb on 30 chromosome-scale scaffolds, placing it among the largest arthropod genomes reported to date. The protein-coding gene repertoire was highly conserved, with over 97% of arthropod orthologs recovered, and microRNA surveys showed a high level of completeness (94%) relative to pancrustacean genomes. Genome expansion appears to be driven primarily by proliferation of intronic and repetitive elements, which comprise ~71% of the genome. Comparative genomic analyses reveal extensive gene family turnover, with relatively few families showing lineage-specific expansions and contractions. Venom-associated gene families included the remipede-specific Xibalbins, while significant expansion and episodic positive selection affected other venom-associated gene families. Comparative analysis of macrosynteny revealed that the remipede genome retains the signature of ancient fusion-with-mixing events that unite Pancrustacea and Allotriocarida, with considerable similarity in the chromosome architecture of remipedes and basally branching insect orders. Our findings provide the first genomic framework for Remipedia and reveal a highly expanded, repeat-rich genome that retains deep phylogenetic signals in its architecture, despite being adapted to a highly unusual environment.