Accelerated evolution and positive selection of rhodopsin in Tibetan loaches living in high altitude

Abstract

Rhodopsin (RH1), the temperature-sensitive visual pigment, attained cold adaptation by functional trade-offs between protein stability and activity. Recent studies suggested convergent selection pressures drove cold adaptation of rhodopsin in high altitude catfishes through nonparallel molecular mechanisms. Here, we tested whether the similar shift occurred in RH1 of Tibetan loaches on the Qinghai-Tibet Plateau (QTP) by investigating the molecular evolution and potential effect on function of RH1. We sequenced RH1 from 27 Triplophysa species, and four lowland loaches and combined these data with published sequences. Tests using a series of models of molecular evolution resulted in strong evidence for accelerated evolution and positive selection in Triplophysa RH1. Three positively selected sites were near key functional domains modulating nonspectral properties of rhodopsin, substitutions of which were likely to compensate for cold-induced decrease in rhodopsin kinetics in cold environments. Moreover, although accelerated evolutionary rates in Tibetan loaches was convergent with those in high altitude catfishes, the sites under positive selection were nonoverlapping. Our findings provide evidence for convergent shift in selection pressures of RH1 in high altitude fish during the ecological transition to cold environment of the QTP.

Keywords: Cold adaptation; Convergent evolution; Qinghai-Tibetan plateau; Rhodopsin; Tibetan loaches; Visual performance.