Genomic Insights Into Genetic Basis of Evolutionary Conservatism and Innovation in Frogs.

Abstract

Examining closely related species evolving in similar environments offers valuable insights into the mechanisms driving phylogenetic conservatism and evolutionary lability. This can elucidate the intricate relationship between inheritance and environmental factors. Nonetheless, the precise genomic dynamics and molecular underpinnings of this process remain enigmatic. This study explores the evolutionary conservatism and adaptation exhibited by two closely related high-altitude frog species: Nanorana parkeri and N. pleskei. We assembled a high-quality genome for Tibetan N. pleskei and compared it to the genomes of N. parkeri and their lowland relatives. Our findings reveal that these two Tibetan frog species diverged approximately 16.6 million years ago, pointing to a possible ancestral colonization of high-elevation habitats. Following this colonization, significant adaptive evolution occurred in both coding and non-coding regions of the ancestral lineage. This evolution led to notable phenotypic alterations, as evidenced by the reduced body size. Also, due to purifying selection, most ancestral adaptive features persisted in descendant species, indicating a strong element of evolutionary conservatism. However, descendant species evolved novel adaptations to exacerbated environmental challenges in the Tibet Plateau, mainly related to hypoxia response. Furthermore, our analysis underscores the critical role of regulatory variations in descendant adaptive evolution. Notably, hub genes in networks, such as EGLN3, accumulated more variations in regulatory regions as they were transmitted from ancestors to descendants. In sum, our study sheds light on the profound and lasting impact of genetic heritage on species' adaptive evolution.