Comparative Analysis of Mitochondrial Genomes in Two Subspecies of the Sunwatcher Toad-Headed Agama (Phrynocephalus helioscopus): Prevalent Intraspecific Gene Rearrangements in Phrynocephalus

Abstract

Intraspecific rearrangements of mitochondrial genomes are rarely reported in reptiles, even in vertebrates. The sunwatcher toad-headed agama, Phryncoephalus helioscopus, can serve as an excellent model for investigating the dynamic mitogenome structure at intraspecific level. To date, seven subspecies of P. helioscopus are well recognized, but little is known about the mitogenomic evolution among different subspecies. In this study, complete mitogenomes of subspecies P. helioscopus varius II and P. helioscopus cameranoi were determined by next-generation sequencing, and another P. helioscopus varius I retrieved from GenBank was compiled for comparative analysis. The nucleotide composition and the codon usage are similar to those previously published from toad-headed agamas. P. helioscopus varius II and P. helioscopus cameranoi have 23 tRNA genes, including standard 22 tRNA genes and one extra tRNA-Phe (tRNA-Phe duplication). Gene order and phylogenetic analyses in the genus Phrynocephalus support prevalent intraspecific gene rearrangement in P. helioscopus and other congener species including P. erythrurus, P. vlangalii, and P. forsythii. Six different mitochondrial gene arrangements are observed in Phrynocephalus. Overall, the occurrence of rearrangements may result from multiple independent structural dynamic events. The split of the two subspecies in P. helioscopus was dated at approximately 2.34 million years ago (Ma). Two types of gene rearrangements are found in the three mitogenomes of P. helioscopus, and this intraspecific rearrangement phenomenon can be explained by the tandem duplication/random loss (TDRL) model. Post duplication, the alternative loss types can occur in 0.23–0.72 Ma, suggesting that the duplication and fixation of these rearrangements can occur quite quickly. These findings highlight the need for more mitogenomes at the population level in order to better understand the potentially rampant intraspecific mitogenomic reorganization in Phrynocephalus.