Enlarged fins of Tibetan catfish provide new evidence of adaptation to high plateau

Abstract

The uplift of the Tibetan Plateau significantly altered the geomorphology and climate of the Euroasia by creating large mountains and rivers. Fishes are more likely to be affected relative to other organisms, as they are largely restricted to river systems. Faced with the rapidly flowing water in the Tibetan Plateau, a group of catfish has evolved greatly enlarged pectoral fins with more numbers of fin-rays to form an adhesive apparatus. However, the genetic basis of these adaptations in Tibetan catfishes remains elusive. In this study, we performed comparative genomic analyses based on the chromosome-level genome of Glyptosternum maculatum in family Sisoridae and detected some proteins with conspicuously high evolutionary rates in particular in genes involved in skeleton development, energy metabolism, and hypoxia response. We found that the hoxd12a gene evolved faster and a loss-of-function assay of hoxd12a supports a potential role for this gene in shaping the enlarged fins of these Tibetan catfishes. Other genes with amino acid replacements and signatures of positive selection included proteins involved in low temperature (TRMU) and hypoxia (VHL) responses. Functional assays reveal that the G. maculatumTRMU allele generates more mitochondrial ATP than the ancestral allele found in low-altitude fishes. Functional assays of VHL alleles suggest that the G. maculatum allele has lower transactivation activity than the low-altitude forms. These findings provide a window into the genomic underpinnings of physiological adaptations that permit G. maculatum to survive in the harsh environment of the Tibetan Himalayas that mirror those that are convergently found in other vertebrates such as humans.