Chemosensation is the most ubiquitous sense in animals, enacted by the products of complex gene families that detect environmental chemical cues and larger-scale sensory structures that process these cues. While there is a general conception that olfactory receptor (OR) genes evolve rapidly, the universality of this phenomenon across vertebrates, and its magnitude, are unclear. The supposed correlation between molecular rates of chemosensory evolution and phenotypic diversity of chemosensory systems is largely untested. We combine comparative genomics and sensory morphology to test whether OR genes and olfactory phenotypic traits evolve at faster rates than other genes or traits. Using published genomes, we identified ORs in 21 tetrapods, including amphibians, reptiles, birds, and mammals and compared their rates of evolution to those of orthologous non-OR protein-coding genes. We found that, for all clades investigated, most OR genes evolve nearly an order of magnitude faster than other protein-coding genes, with many OR genes showing signatures of diversifying selection across nearly all taxa in this study. This rapid rate of evolution suggests that chemoreceptor genes are in “evolutionary overdrive,” perhaps evolving in response to the ever-changing chemical space of the environment. To obtain complementary morphological data, we stained whole fixed specimens with iodine, µCT-scanned the specimens, and digitally segmented chemosensory and nonchemosensory brain regions. We then estimated phenotypic variation within traits and among tetrapods. While we found considerable variation in chemosensory structures, they were no more diverse than nonchemosensory regions. We suggest chemoreceptor genes evolve quickly in reflection of an ever-changing chemical space, whereas chemosensory phenotypes and processing regions are more conserved because they use a standardized or constrained architecture to receive and process a range of chemical cues.

中文翻译：

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嗅觉受体基因进化在四足动物中异常迅速，并且超过化学感应表型变化

化学感觉是动物中最普遍的感觉，由检测环境化学线索的复杂基因家族的产物和处理这些线索的更大规模的感觉结构产生。虽然普遍认为嗅觉受体 ( OR ) 基因进化迅速，但这种现象在脊椎动物中的普遍性及其重要性尚不清楚。化学感应进化的分子速率与化学感应系统的表型多样性之间假设的相关性在很大程度上未经测试。我们结合比较基因组学和感官形态学来测试OR基因和嗅觉表型特征是否比其他基因或特征以更快的速度进化。使用已发表的基因组，我们确定了ORs 在 21 种四足动物中，包括两栖动物、爬行动物、鸟类和哺乳动物，并将它们的进化速度与直系同源非OR蛋白质编码基因的进化速度进行了比较。我们发现，对于所有研究的进化枝，大多数OR基因的进化速度比其他蛋白质编码基因快近一个数量级，其中许多OR在这项研究中，基因显示出几乎所有分类群中多样化选择的特征。这种快速的进化表明化学感受器基因处于“进化过度驱动”状态，可能是为了响应不断变化的环境化学空间而进化的。为了获得互补的形态学数据，我们用碘对整个固定标本进行染色，对标本进行 μCT 扫描，并对化学感应和非化学感应大脑区域进行数字分割。然后我们估计了性状内和四足动物之间的表型变异。虽然我们发现化学感应结构存在相当大的变化，但它们并不比非化学感应区域更加多样化。我们建议化学感受器基因快速进化以反映不断变化的化学空间，