Mitonuclear Coevolution in Bumblebees (Bombus): Genomic Signatures and Its Role in Climatic Niche Adaptation.

Abstract

Mitochondria play a central role in cellular respiration, but require close coevolution with the nuclear genome for proper function. This process, termed mitonuclear coevolution, is poorly understood on species-level evolutionary timescales, despite its role in speciation. Here, we investigate mitonuclear coevolution in bumblebees (Bombus), a group of ecologically diverse pollinators with rapid mitochondrial (mt) DNA evolution. Leveraging genomic data from a comprehensive set of 55 bumblebee species, we quantified the evolutionary rate correlation (ERC) between mt genes and nuclear genes that interact with mitochondria (N-mt). We found a strong ERC between mt and N-mt genes, but not among mt genes and random nuclear genes, supporting the mitonuclear coevolution hypothesis. Additionally, we found the strength of mitonuclear ERC seems to be consistent across bumblebee lineages, contrasting with observations in other taxa. Finally, bumblebee species from colder environments showed increased mt evolutionary rates relative to both N-mt genes and random nuclear genes. This suggests potential implications to bumblebee climatic niche adaptation and the thermoregulation of cold-adapted species, possibly driven by selection for enhanced mt function to sustain thermogenesis and flight in low-temperature environments. Our findings are discussed considering the dynamics of mitonuclear coevolution in bumblebees and its potential role in shaping their adaptation to diverse ecological niches.