Dramatic evolutionary changes of conserved noncoding elements accompanied by extraordinary features ofCaenorhabditis inopinata

Phenotypic evolution is driven by genetic mutations occurring in both protein-coding and noncoding regions of the genome. Conserved noncoding elements (CNEs) have—at least partially—gene regulatory functions and contribute to the evolution of organisms by altering their gene expression. Evolutionary changes in CNEs, including their loss and accelerated evolution, can play crucial roles in shaping species-specific traits. The extensive functional genomic information available for the model nematode Caenorhabditis elegans , together with the recent accumulation of high-quality genome sequences from related species, has made Caenorhabditis nematodes a powerful system for comparative genomics focused on CNE evolution. The recently described species Caenorhabditis inopinata has several peculiar traits notable for its unusually large body size and is regarded as an appropriate species that links phenotypic evolution with genomic changes. Here, using comparative genomics and transcriptomics in C. inopinata , we analyzed the evolution of CNEs and inferred their influence during phenotypic evolution. We detected substantial evolutionary changes in CNEs in C. inopinata compared to other relatives—changes frequently associated with body morphology and behavior corresponding to distinct ecological traits. Our findings suggest that loss and accelerated evolution of CNE are associated with species-specific traits and provide new insight into the impact of noncoding elements on evolution. Significance statement Large-scale phenotypic evolution has been observed across a wide range of taxa and may be accompanied by substantial genomic changes. Caenorhabditis inopinata , a nematode species closely related to C. elegans , shows several distinctive morphological and behavioral traits compared with its congeners, and through comparative genomics and transcriptomics, we identify substantial evolutionary changes in conserved noncoding elements (CNEs)— including their loss and accelerated sequence evolution. Furthermore, these changes are frequently associated with genes involved in morphology and behavior, suggesting a potential link between CNE evolution and species-specific phenotypes.