Evolutionary repeatability of chromatin accessibility in the hippocampus between echolocating bats and soft-furred...

Echolocation is a compelling example of behavioral convergence in mammals and has evolved independently in at least five mammalian lineages. Despite increasing evidence of convergent evolution in protein-coding regions among echolocating mammals, the evolution of gene regulatory activity underlying mammalian echolocation remains undetermined. Here, we systematically investigate chromatin accessibility and transcriptomic data from the hippocampi of echolocating bats and soft-furred tree mice, as the hippocampus plays a crucial role in processing echolocation signals. Our results showed significant evolutionary repeatability in accessible chromatin regions among echolocating mammals compared with their non-echolocating counterparts. An analysis that paired gene expression with chromatin accessibility revealed that echolocating mammals have more complex gene regulatory networks in the hippocampus than non-echolocating mammals. This complexity is primarily attributed to the observed evolutionary repeatability in accessible chromatin regions among echolocating mammals. The shared gene regulations among echolocating mammals are particularly enriched in functional terms related to synaptic function, which is supported by the higher synaptic and mitochondrial densities in soft-furred tree mice than in laboratory mice. These findings demonstrate significant evolutionary repeatability of gene regulatory activity in the hippocampus among echolocating mammalian species, suggesting crucial contributions of gene regulatory activities to convergent phenotypes in mammals.