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 prestin for the LCAW and LCATW; we show that the LCAW prestin exhibits the same function as that of nonecholocating mammals, but the LCATW prestin 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.

中文翻译：

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基因组和功能证据揭示了鲸鱼回声定位起源的分子洞察力。

回声使齿鲸能够适应视力不佳的水下栖息地。由于回声定位需要具有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查明鲸鱼的回声定位的起源。但是，由于古生化石的解释存在矛盾，鲸鱼何时以及如何进化，与回声定位相关的高频听力仍不清楚。我们通过系统地研究16种哺乳动物中7206个直系同源物的趋同进化，在分子水平上解决了这些问题，并发现所有鲸的最后共同祖先（LCAW）和回声蝙蝠之间的趋同基因在与听力相关的功能类别中并未显着丰富，而且它们之间的听力相关蛋白的融合并不强于非定位哺乳动物谱系和回声蝙蝠之间的融合。但是，这些结果与齿鲸的LCA（LCATW）和回声蝙蝠之间的平行分析形成对比。此外，我们重建了听力蛋白的祖先基因LCAW和LCATW的prestin；我们表明，LCAW prestin表现出与非定位哺乳动物相同的功能，但LCATW prestin显示与现存回声哺乳动物的功能融合。诱变表明，在LCATW和回声定位蝙蝠中，prestins S392A和L497M的收敛变化驱动了prestin的功能收敛。我们的结果提供了支持LCAW（而非LCATW）高频听力起源的基因组和功能证据，并揭示了鲸鱼回声定位的起源和进化轨迹的分子洞察力。