Shennard Devin, Sifuentes-Romero Itzel, Ambosie Rianna, Abdelaziz Jennah, Duboue Erik R, Kowalko Johanna E
Department of Biological Sciences, Lehigh University, Bethlehem, Pennsylvania, USA.
Iowa State University, Ames, Iowa, USA.
Evol Dev. 2025 Sep;27(3):e70011. doi: 10.1111/ede.70011.
Uncovering mechanisms by which sensory systems evolve is critical for understanding how organisms adapt to a novel environment. Astyanax mexicanus is a species of fish with populations of surface fish, which inhabit rivers and streams, and cavefish, which have adapted to life within caves. Cavefish have evolved sensory system changes relative to their surface fish counterparts, providing an opportunity to investigate mechanisms underlying sensory system evolution. Here, we report the role of the gene retinal homeobox 3 (rx3) in cavefish eye evolution. We generated surface fish with putative loss-of-function mutations in the rx3 gene using CRISPR-Cas9 to determine the role of this gene in eye development in this species. These rx3 mutant surface fish fail to develop eyes, demonstrating that rx3 is required for surface fish eye development. Further, rx3 mutant surface fish exhibit altered behaviors relative to wild-type surface fish, suggesting that the loss of eyes impacts sensory-dependent behaviors. Finally, eye development is altered in cave-surface hybrid fish that inherit the mutant allele of rx3 from surface fish relative to siblings that inherit a wild-type surface fish rx3 allele, suggesting that cis-regulatory variation at the rx3 locus contributes to eye size evolution in cavefish. Together, these findings demonstrate that, as in other species, rx3 is required for eye development in A. mexicanus. Moreover, they suggest that variation at the rx3 locus plays a role in the evolved reduction of eye size in cavefish, shedding light on the genetic mechanisms underlying sensory system evolution in response to extreme environmental changes.
揭示感觉系统进化的机制对于理解生物体如何适应新环境至关重要。墨西哥丽脂鲤是一种鱼类，其种群包括栖息在河流和溪流中的表层鱼以及适应洞穴生活的洞穴鱼。洞穴鱼相对于其表层鱼同类已经进化出了感觉系统的变化，这为研究感觉系统进化的潜在机制提供了机会。在这里，我们报告了视网膜同源盒3（rx3）基因在洞穴鱼眼睛进化中的作用。我们使用CRISPR-Cas9在rx3基因中产生了具有假定功能丧失突变的表层鱼，以确定该基因在该物种眼睛发育中的作用。这些rx3突变表层鱼无法发育出眼睛，这表明rx3是表层鱼眼睛发育所必需的。此外，rx3突变表层鱼相对于野生型表层鱼表现出行为改变，这表明眼睛的丧失会影响依赖感觉的行为。最后，相对于继承野生型表层鱼rx3等位基因的同胞，从表层鱼继承rx3突变等位基因的洞穴-表层杂交鱼的眼睛发育发生了改变，这表明rx3基因座的顺式调控变异有助于洞穴鱼眼睛大小的进化。总之，这些发现表明，与其他物种一样，rx3是墨西哥丽脂鲤眼睛发育所必需的。此外，它们表明rx3基因座的变异在洞穴鱼眼睛大小的进化性减小中起作用，揭示了响应极端环境变化的感觉系统进化的遗传机制。
