Cross-species cochlear transcriptomes provide novel insights into the origin of the laryngeal echolocation in bats

This study aimed to elucidate the molecular mechanisms underlying the evolutionary origin of laryngeal echolocation in bats. We employed three different approaches to analyze cochlear transcriptome data from multiple bat species, providing valuable insights into the genetic basis of this complex trait. Firstly, pairwise differential expression analysis (PDEA) identified specific genes showing differential expression between echolocating and non-echolocating bats. Through this analysis, we identified 367 genes upregulated in echolocating bats, many of which are associated with neural processes and inner ear sound perception, corroborating their importance in this biological function as previously reported. Secondly, weighted gene co-expression network analysis (WGCNA) enabled us to identify co-expressed gene modules significantly associated with echolocation. This approach revealed five modules enriched in genes related to cellular processes such as cell projection morphogenesis, synaptic signaling, and neurogenesis, with substantial overlap with genes identified through PDEA, further supporting their relevance to echolocation. Lastly, utilizing the Phylogenetic Differential Gene Expression Tool (PhyDGET) considering phylogenetic relationships, we identified genes whose expression changes were significantly associated with the origin of laryngeal echolocation in bats. By comparing different evolutionary models, we revealed complex patterns of echolocation evolution within bat lineages, suggesting a stepwise process in the acquisition and subsequent divergence of this trait. Overall, our comprehensive analysis of gene expression data using complementary methods sheds light on the genetic basis of laryngeal echolocation in bats, emphasizing the importance of considering both gene expression and phylogenetic context when studying the evolution of complex traits across multiple species.