State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming 650223, China.
Sci Adv. 2018 Oct 3;4(10):eaat8821. doi: 10.1126/sciadv.aat8821. eCollection 2018 Oct.
Echolocation allows toothed whales to adapt to underwater habitats where vision is ineffective. Because echolocation requires the ability to detect exceptional high-frequency sounds, fossils related to the auditory system can help to pinpoint the origin of echolocation in whales. However, because of conflicting interpretations of archaeocete fossils, when and how whales evolved the high-frequency hearing correlated with echolocation remain unclear. We address these questions at the molecular level by systematically investigating the convergent evolution of 7206 orthologs across 16 mammals and find that convergent genes between the last common ancestor of all whales (LCAW) and echolocating bats are not significantly enriched in functional categories related to hearing, and that convergence in hearing-related proteins between them is not stronger than that between nonecholocating mammalian lineages and echolocating bats. However, these results contrast with those of parallel analyses between the LCA of toothed whales (LCATW) and echolocating bats. Furthermore, we reconstruct the ancestral genes for the hearing protein for the LCAW and LCATW; we show that the LCAW exhibits the same function as that of nonecholocating mammals, but the LCATW shows functional convergence with that of extant echolocating mammals. Mutagenesis shows that functional convergence of prestin is driven by convergent changes in the prestins S392A and L497M in the LCATW and echolocating bats. Our results provide genomic and functional evidence supporting the origin of high-frequency hearing in the LCAW, not the LCATW, and reveal molecular insights into the origin and evolutionary trajectories of echolocation in whales.
回声定位使齿鲸能够适应水下环境，在水下环境中视力无效。由于回声定位需要检测异常高频声音的能力，因此与听觉系统相关的化石可以帮助确定鲸鱼回声定位的起源。然而，由于对古鲸类化石的解释相互矛盾，鲸鱼何时以及如何进化出与回声定位相关的高频听觉仍然不清楚。我们通过系统研究 16 种哺乳动物中 7206 个直系同源基因的趋同进化，在分子水平上解决了这些问题，发现所有鲸鱼的最后共同祖先（LCAW）与回声定位蝙蝠之间的趋同基因在与听觉相关的功能类别中没有显著富集，并且它们之间的听觉相关蛋白趋同程度并不强于非回声定位哺乳动物谱系和回声定位蝙蝠之间的趋同程度。然而，这些结果与齿鲸的最后共同祖先（LCATW）和回声定位蝙蝠之间的平行分析结果形成对比。此外，我们重建了 LCAW 和 LCATW 的听觉蛋白的祖先基因；我们表明 LCAW 的 具有与非回声定位哺乳动物相同的功能，但 LCATW 的 与现存的回声定位哺乳动物具有功能趋同。诱变显示，LCATW 和回声定位蝙蝠中的 prestin S392A 和 L497M 的趋同变化驱动了 prestin 的功能趋同。我们的研究结果提供了基因组和功能证据，支持 LCAW 而不是 LCATW 高频听觉的起源，并揭示了鲸鱼回声定位起源和进化轨迹的分子见解。
