Hepatic Transcriptome Variations Among Different Evolutionary Lineages of Rhinolophus ferrumequinum During Hibernation

TL;DR

This study shows how two lineages of Rhinolophus ferrumequinum bats adapt differently to hibernation through unique liver gene activity patterns.

Contribution

The study reveals lineage-specific transcriptomic adaptations to hibernation in Rhinolophus ferrumequinum, highlighting distinct metabolic and immune strategies.

Findings

The central–eastern lineage shows more differentially expressed genes during hibernation phases compared to the northeastern lineage.

Both lineages shift from carbohydrate to lipid metabolism during torpor and upregulate immune genes.

Lineage-specific regulatory genes related to energy and metabolism suggest adaptation to local environmental conditions.

Abstract

The northeastern and central–eastern lineages of Rhinolophus ferrumequinum exhibit significantly divergent sets of hepatic differentially expressed genes and pathways, with minimal overlap during the torpor and arousal phases. This indicates lineage-specific transcriptomic adaptations to their respective climatic conditions and varying durations of hibernation.

The greater horseshoe bat (Rhinolophus ferrumequinum), which is widely distributed across the temperate regions of China, primarily consists of two major evolutionary lineages: a northeastern (NE) lineage with a hibernation period of 6–8 months and a central–eastern (CE) lineage with a hibernation period of 4–5 months. This study conducted a comparative analysis of liver transcriptomes from these two lineages during the active, torpor, and arousal phases. The results indicated that the CE lineage exhibited a significantly greater number of differentially expressed genes (DEGs) compared to the NE lineage. During the torpor phase, both lineages transitioned from carbohydrate metabolism to lipid metabolism, substantially downregulating genes and pathways associated with amino acid metabolism, and upregulating immune-related genes to maintain essential defense functions. In the arousal phase, both lineages only moderately activated several genes associated with immunity and metabolic regulation to facilitate a rapid return to torpor. Notably, the number of DEGs co-regulated between the two lineages was very limited, and a large number of lineage-specific regulatory genes related to energy and metabolism were identified. This may reflect the adaptability of different bat lineages to the local environment, highlighting the importance of habitat conditions in lineage differentiation. Therefore, hibernation induces substantial transcriptomic reorganization in the liver of R. ferrumequinum, particularly affecting metabolic and immune processes. Distinct geographic lineages exhibit unique hibernation adaptation strategies through the regulation of specific genes and pathways. This study enhances the understanding of the molecular mechanisms underlying hibernation adaptation across different evolutionary lineages of the same species at the transcriptomic level, providing insights into the evolutionary adaptations of animals to environmental changes.

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