Akiyama Tokiho, Uchiyama Hironobu, Yajima Shunsuke, Arikawa Kentaro, Terai Yohey
Department of Evolutionary Studies of Biosystems, SOKENDAI (The Graduate University for Advanced Studies), Shonan Village, Hayama, Kanagawa 240-0193, Japan.
NODAI Genome Research Center, Tokyo University of Agriculture, 1-1-1 Sakuragaoka, Setagaya, Tokyo 156-8502, Japan.
J Exp Biol. 2022 Dec 1;225(23). doi: 10.1242/jeb.244541. Epub 2022 Dec 12.
Light environments differ dramatically between day and night. The transition between diurnal and nocturnal visual ecology has happened repeatedly throughout evolution in many species. However, the molecular mechanism underlying the evolution of vision in recent diurnal-nocturnal transition is poorly understood. Here, we focus on hawkmoths (Lepidoptera: Sphingidae) to address this question by investigating five nocturnal and five diurnal species. We performed RNA-sequencing analysis and identified opsin genes corresponding to the ultraviolet (UV), short-wavelength (SW) and long-wavelength (LW)-absorbing visual pigments. We found no significant differences in the expression patterns of opsin genes between the nocturnal and diurnal species. We then constructed the phylogenetic trees of hawkmoth species and opsins. The diurnal lineages had emerged at least three times from the nocturnal ancestors. The evolutionary rates of amino acid substitutions in the three opsins differed between the nocturnal and diurnal species. We found an excess number of parallel amino acid substitutions in the opsins in three independent diurnal lineages. The numbers were significantly more than those inferred from neutral evolution, suggesting that positive selection acted on these parallel substitutions. Moreover, we predicted the visual pigment absorption spectra based on electrophysiologically determined spectral sensitivity in two nocturnal and two diurnal species belonging to different clades. In the diurnal species, the LW pigments shift 10 nm towards shorter wavelengths, and the SW pigments shift 10 nm in the opposite direction. Taken together, our results suggest that parallel evolution of opsins may have enhanced the colour discrimination properties of diurnal hawkmoths in ambient light.
白天和夜晚的光照环境差异极大。在许多物种的进化过程中，昼夜视觉生态之间的转变反复发生。然而，对于近期昼夜转变过程中视觉进化的分子机制，我们却知之甚少。在此，我们聚焦于天蛾（鳞翅目：天蛾科），通过研究五个夜行性物种和五个昼行性物种来解决这个问题。我们进行了RNA测序分析，并鉴定出了与吸收紫外线（UV）、短波长（SW）和长波长（LW）的视觉色素相对应的视蛋白基因。我们发现夜行性和昼行性物种之间视蛋白基因的表达模式没有显著差异。然后，我们构建了天蛾物种和视蛋白的系统发育树。昼行性谱系至少三次从夜行性祖先中分化出来。夜行性和昼行性物种中三种视蛋白的氨基酸替换进化速率有所不同。我们发现在三个独立的昼行性谱系中，视蛋白存在过多的平行氨基酸替换。这些替换的数量显著多于从中性进化推断出的数量，这表明正选择作用于这些平行替换。此外，我们根据电生理测定的光谱敏感性，预测了属于不同分支的两个夜行性和两个昼行性物种的视觉色素吸收光谱。在昼行性物种中，LW色素的吸收峰向较短波长方向移动了10纳米，而SW色素的吸收峰则向相反方向移动了10纳米。综合来看，我们的结果表明，视蛋白的平行进化可能增强了昼行性天蛾在环境光下的颜色辨别能力。
