Positive selection and inactivation in vision and hearing genes of cetaceans

The transition to an aquatic lifestyle in cetaceans (whales and dolphins) resulted in a radical transformation in their sensory systems. Toothed whales acquired specialized high-frequency hearing tied to the evolution of echolocation, while baleen whales evolved low-frequency hearing. More generally, all cetaceans show adaptations for hearing and seeing underwater. To determine the extent to which these phenotypic changes have been driven by molecular adaptation, we performed large-scale targeted sequence capture of 179 sensory genes across the Cetacea, incorporating up to 54 cetacean species from all major clades as well as their closest relatives, the hippopotamuses. We screened for positive selection in 167 loci related to vision and hearing, and found that the diversification of cetaceans has been accompanied by pervasive molecular adaptations in both sets of genes, including several loci implicated in non-syndromic hearing loss (NSHL). Despite these findings, however, we found no direct evidence of positive selection at the base of odontocetes coinciding with the origin of echolocation, as found in studies examining fewer taxa. By using contingency tables incorporating taxon- and gene-based controls, we show that, while numbers of positively selected hearing and NSHL genes are disproportionately high in cetaceans, counts of vision genes do not differ significantly from expected values. Alongside these adaptive changes, we find increased evidence of pseudogenization of genes involved in cone-mediated vision in mysticetes and deep diving odontocetes.

鲸类（Cetacea，即鲸鱼与海豚）向水生生活方式的转变，使其感官系统发生了根本性重塑。齿鲸（Odontoceti）演化出与回声定位（echolocation）进化相关的特化高频听觉能力，而须鲸（Mysticeti）则进化出低频听觉系统。更广泛而言，所有鲸类均展现出适应水下听觉与视觉的演化特征。为探明这些表型变化（phenotypic changes）在多大程度上由分子适应（molecular adaptation）驱动，我们对鲸类179个感官基因开展了大规模靶向序列捕获（targeted sequence capture）分析，纳入了来自所有主要演化支（clades）的多达54种鲸类，以及它们的近亲——河马科动物（Hippopotamidae）。我们对与视觉和听觉相关的167个基因座（loci）进行了正选择（positive selection）筛选，发现鲸类的演化伴随着两类基因的广泛分子适应性改变，其中包括多个与非综合征性听力损失（non-syndromic hearing loss, NSHL）相关的基因座。尽管如此，我们并未发现如过往少类群研究所示的、与回声定位起源同步的齿鲸基部类群存在正选择的直接证据。通过结合类群与基因层面对照的列联表（contingency tables）分析，我们证实：尽管鲸类中受正选择的听觉基因与非综合征性听力损失相关基因数量远超预期，但视觉基因的数量并未出现显著偏离预期的情况。伴随这些适应性改变，我们还发现须鲸类（Mysticeti）与深潜齿鲸类（deep diving Odontoceti）中，视锥介导视觉（cone-mediated vision）相关基因的假基因化（pseudogenization）证据有所增加。