Genomics of eye number evolution in spiders

Abstract

Spiders exhibit tremendous variations in eye numbers, but the genomic basis underlying this diversity remains largely unexplored. Here, we analyzed the genomic data of 148 spider species in 31 families, representing all phenotypes of eye numbers including 8, 6, 4, 2, and 0. Our analyses revealed that a core set of 29 genes involved in eye development and phototransduction is conserved across all spiders, irrespective of their eye number, indicating that eye reduction is not caused by the loss of key developmental genes. We found that evolutionary transitions leading to reduced numbers of eyes are primarily associated with parallel genome-wide relaxed selection. While these independent reduction events shared several genes under consistent selective pressures, they did not share any genes under positive selection, indicating putatively divergent molecular mechanisms. In contrast, the evolution of complete eye loss in cave-dwelling spiders is associated with parallel genome-wide intensified selection. Notably, we identified shared genes under both intensified and positive selection across independent origins of eyelessness, suggesting a parallel molecular mechanism. Altogether, our study provides genomic insights into the parallel evolution of eye reduction and complete eye loss in spiders.