A T2T Genome of the Lobed-Lip Iguazu Joana (Crenicichla tuca) Reveals Intrachromosomal Rearrangements and Trans-species Polymorphism in Cichlid Fishes.

Abstract

Genomic architecture is a key factor shaping the landscape of linkage disequilibrium between divergently selected traits. By facilitating the detection of intrachromosomal variants, long-read data fueled recent interest in the role of structural variants in adaptive radiation. The Neotropical cichlid genus Crenicichla provides a compelling system for replicated adaptive radiation in riverine environments in which at least two lineages show repeated ecomorphological evolution. The lack of South American cichlid reference genomes has thus far limited investigation of chromosomal evolution across cichlid radiations and precluded testing the role of structural variants in Crenicichla adaptive radiation. Here, we generated a complete assembly of Crenicichla tuca (iguassuensis group) collected from the type locality. To investigate structural variants within Crenicichla, we produced ultra-long reads for Crenicichla missioneira. We then conduct comparative genomics across cichlids using published chromosome-level genomes. Despite karyotypic stability in Crenicichla, intrachromosomal structural variants are abundant and enriched in repetitive genomic regions. Comparisons with other cichlid radiations indicate the predominance of intrachromosomal rearrangements. Chromosomes LG03, LG23, LG10, and LG11 show signatures of chromosomal instability, which seem to be associated with highly repetitive DNA composition and enrichment of immune-related genes. Structural variants polymorphic in both Crenicichla species are consistent with the maintenance of trans-species polymorphism through balancing selection on immune-related genes. Our results add to the growing evidence that structural variation is widespread, even when overall chromosomal morphology remains unchanged. Our approach combining field-based extractions with PacBio HiFi and ONT UL proved sufficient to generate a T2T assembly and holds great potential for evolutionary and conservation genomics in biodiversity hotspots.