Comparative Transcriptomics and Methylomics Reveal Adaptive Responses of Digestive and Metabolic Genes to Dietary Shift in Giant and Red Pandas

Abstract

Both the giant panda (Ailuropoda melanoleuca) and red panda (Ailurus fulgens) belong to the order Carnivora, but have changed their dietary habits to eating bamboo exclusively. The convergent evolution characteristics of their morphology, genome and gut flora have been found in the two pandas. However, the research on the convergent adaptation of their digestion and metabolism to the bamboo diet, mediated by the dietary shift of the two pandas at the gene-expression and epigenetic regulation levels, is still lacking. We therefore used RNA sequencing among five species (two pandas and three non-herbivore mammals) and bisulfite sequencing among three species (two pandas and a carnivore ferret) to sequence key digestion and metabolism tissues (stomach and small intestine). Our results provide evidence that the convergent differentially expressed genes (related to carbohydrate utilization, bile secretion, Lys and Arg metabolism, vitamin B12 utilization and cyanide detoxification) of the two pandas are adaptive responses to the bamboo diet containing low lipids, low Lys and Arg, low vitamin B12 and high cyanide. We also profiled the genome-wide methylome maps of giant panda, red panda and ferret, and the results indicated that the promoter methylation of the two pandas may regulate digestive and metabolic genes to adapt to sudden environmental changes, and then, transmit genetic information to future generations to evolve into bamboo eaters. Taken together, our study provides new insights into the molecular mechanisms of the dietary shift and the adaptation to a strict bamboo diet in both pandas using comparative transcriptomics and methylomics.

Molecular Mechanisms Underlying Vertebrate Adaptive Evolution: A Systematic Review

“…Bamboo has bitter-tasting substances as a defense mechanism, and the loss of bitter taste receptors is thought to have enabled giant pandas to overcome this challenge [101]. Additionally, epigenetic modifications increasing the expression of thiosulfate sulfurtransferase have also been proposed as an adaptation in red and giant pandas to overcome the toxicity of bamboo [102]. Polar bears underwent a dietary shift to a hypercarnivorous diet, which is thought to have resulted in losses in the copy number of genes associated with a digestive system, (e.g., AMY1B and NOX4) and olfactory receptor genes [103].…”

“…Vampire bats have a mutational bias favoring cytosine and not favoring thymine, which subsequently increases threonine in their proteomes, enabling them to overcome inherent amino acid limitations in their diet [104]. Convergent epigenetic changes in both red and giant pandas have been proposed as the molecular mechanism behind the differential expression patterns of genes involved in lipid digestion (DGAT2, SLC2A3, and PARL), enabling them to overcome nutritional challenges of their low-lipid diet [102].…”

Adaptive Expression and ncRNA Regulation of Genes Related to Digestion and Metabolism in Stomach of Red Pandas during Suckling and Adult Periods

“…Both pandas consume high-nutrient milk during the suckling period, while they exclusively consume low-nutrient bamboo during the adult period. Their morphology, genome, gut microbiota, and gene expression patterns exhibit many convergent evolutionary characteristics [ 13 , 14 , 15 , 16 , 17 , 18 , 19 ]. Research on giant pandas showed that the high expression levels of genes related to cholesterol metabolism and protein digestion and absorption in their early stages of development may help meet their high energy needs for rapid growth and development, while the high expression levels of genes related to metabolism of carbohydrate, amino acid, and protein during the adult period may indicate their high metabolic levels [ 9 ].…”