Hogan Michael P, Holding Matthew L, Nystrom Gunnar S, Lawrence Kylie C, Broussard Emilie M, Ellsworth Schyler A, Mason Andrew J, Margres Mark J, Gibbs H Lisle, Parkinson Christopher L, Rokyta Darin R
Department of Biological Sciences, Florida State University, Tallahassee, FL, United States.
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, United States.
J Hered. 2025 Aug 23;116(5):617-631. doi: 10.1093/jhered/esae078.
Predatory species who hunt for their prey rely on a suite of integrated characters, including sensory traits that are also used for nonpredatory behaviors. Linking the evolution of sensory traits to specific selection pressures therefore requires a deep understanding of the underlying genetics and molecular mechanisms producing these complex phenotypes. However, this relationship remains poorly understood for complex sensory systems that consist of proteins encoded by large gene families. The chemosensory repertoire of rattlesnakes includes hundreds of type-2 vomeronasal receptors and olfactory receptors, representing the two largest gene families found in the genome. To investigate the biological importance of this chemoreceptor diversity, we assessed gene expression in the eastern diamondback rattlesnake (Crotalus adamanteus) and identified sex- and age-biased genes. We found type-2 vomeronasal receptor expression in the vomeronasal epithelium was limited to juvenile snakes, suggesting the sensory programming of this tissue may be correlated with early life development. In the olfactory epithelium, we found subtle expression biases that were more indicative of life history rather than development. We also found transcriptional evidence for dosage compensation of sex-linked genes and trait integration in the expression of transcription factors. We overlay our molecular characterizations in Crotalus adamanteus onto updated olfactory receptor and type-2 vomeronasal receptor phylogenies, providing a genetic road map for future research on these receptors. Finally, we investigated the deeper macroevolutionary context of the most highly expressed type-2 vomeronasal receptor gene spanning the rise of tetrapods and estimated the strength of positive selection for individual amino acid residues in the predicted protein structure. We hypothesize that this gene may have evolved as a conserved signaling subunit to ensure consistent G-protein coupled receptor functionality, potentially relaxing signaling constraints on other type-2 vomeronasal receptor paralogs and promoting ligand binding specificity.
捕食性物种依靠一系列综合特征来捕食猎物，这些特征包括也用于非捕食行为的感官特性。因此，将感官特性的进化与特定选择压力联系起来，需要深入了解产生这些复杂表型的潜在遗传学和分子机制。然而，对于由大基因家族编码的蛋白质组成的复杂感官系统，这种关系仍知之甚少。响尾蛇的化学感应库包括数百种2型犁鼻器受体和嗅觉受体，它们是基因组中发现的两个最大的基因家族。为了研究这种化学感受器多样性的生物学重要性，我们评估了东部菱斑响尾蛇（Crotalus adamanteus）的基因表达，并鉴定了性别和年龄偏向性基因。我们发现犁鼻器上皮中2型犁鼻器受体表达仅限于幼年蛇，这表明该组织的感官编程可能与早期生命发育相关。在嗅觉上皮中，我们发现了细微的表达偏向，这更能指示生活史而非发育过程。我们还发现了性连锁基因剂量补偿和转录因子表达中性状整合的转录证据。我们将在东部菱斑响尾蛇中的分子特征叠加到更新的嗅觉受体和2型犁鼻器受体系统发育树上，为这些受体的未来研究提供了遗传路线图。最后，我们研究了跨越四足动物兴起的表达量最高的2型犁鼻器受体基因的更深层次宏观进化背景，并估计了预测蛋白质结构中单个氨基酸残基的正选择强度。我们假设该基因可能已经进化为一个保守的信号亚基，以确保一致的G蛋白偶联受体功能，潜在地放松对其他2型犁鼻器受体旁系同源物的信号限制，并促进配体结合特异性。
