Yang Chao, Wang Qingxiong, Sun Kuo, Luo Lei, Yuan Hao, Li Xuejuan, Huang Yuan, Xiao Hong
Shaanxi Key Laboratory of Qinling Ecological Security, Shaanxi Institute of Zoology, Xi'an, 710032, China.
College of Life Sciences, Shaanxi Normal University, Xi'an, 710062, China.
BMC Genomics. 2025 Jan 24;26(1):67. doi: 10.1186/s12864-025-11257-x.
The relict gull (Larus relictus, Charadriiformes, Laridae) classified as vulnerable in the IUCN Red List is defined as a first-class national protected bird in China. However, our knowledge of the evolutionary history of L. relictus is limited. Here, we performed whole-genome resequencing of L. relictus (n = 14) and L. brunnicephalus (n = 3) to explore the genetic relationships and population structures and understand their adaptive evolution.
The whole genome resequencing generated 667.55 Gb clean reads with an average sequencing depth of ~ 29×. The genomic variant analysis identified 13,717,267 heterozygous SNPs in the samples obtained from 17 individuals. Population genetic diversity analysis revealed that low nucleotide diversity (0.00029) and no obvious population structure in L. relictus. Demographic history revealed that from 180 to 5 kya (thousand years ago), the effective population size (Ne) of L. relictus exhibited declines (24,000 to 5,000), with a very low range population size (2,200 to 5,000). In contrast, from 100 to 80 kya, L. brunnicephalus peaked in ancestral Ne, followed by distinct declines at ~ 70 kya (100,000 to 16,000). The findings identified several genes associated with the correlated changed life-history traits of L. relictus, including BMP4 involved in beak adaptation; HAND2, NEUROG1, COL11A2, and EDNRB involved in the evolution of the palate, soft palate, and tongue; PIGR and PLCB2 involved in an enhanced response to bitter taste by sensing chemical secretions released by staple food substrate insects to activate protective mechanisms. Furthermore, thirty-four genes related to sperm development and activity, including KLHL10 and TEKT3, were identified in the expanded gene family. In addition, MED1, CNOT9, NR5A1, and PATZ1 were involved in enhanced male hormone secretion and a high density of candidate genes associated with embryonic development were identified. The findings indicated that the L. relictus population was in a male-biased diffusion mode; the function of the TEKT3 gene showed that males played a dominant role in brooding, which enhanced their attraction to females. Our study revealed that significant enrichment of olfactory signaling pathway genes, including OR14C36, OR14J1, OR14I1, and OR14A16; inner ear development-related, including PTN, PTPN11, GATA2, ATP8B1, and MYO15A; and those related to hypoxic adaptation to high-altitude breeding and iris colour.
Based on the results and the knowledge of this organism biology and habitat use, we infer that less adaptive evolutionary pressure on vision in L. relictus were related with their feeding behaviour and adaptation. In summary, this comprehensive analysis provides insights into the evolutionary features of L. relictus and a new perspective for scientific research on L. relictus to effectively determine its future survival viability.
遗鸥（Larus relictus，鸻形目，鸥科）在世界自然保护联盟红色名录中被列为易危物种，在中国被定为国家一级保护鸟类。然而，我们对遗鸥进化历史的了解有限。在此，我们对遗鸥（n = 14）和棕头鸥（n = 3）进行了全基因组重测序，以探索它们的遗传关系和种群结构，并了解它们的适应性进化。
全基因组重测序产生了667.55 Gb的clean reads，平均测序深度约为29×。基因组变异分析在从17个个体获得的样本中鉴定出13,717,267个杂合单核苷酸多态性（SNP）。种群遗传多样性分析显示，遗鸥的核苷酸多样性较低（0.00029），且没有明显的种群结构。种群历史分析表明，从180至5千年前（kya），遗鸥的有效种群大小（Ne）呈下降趋势（从24,000降至5,000），种群数量范围非常低（2,200至5,000）。相比之下，从100至80 kya，棕头鸥的祖先Ne达到峰值，随后在约70 kya（100,000至16,000）明显下降。研究结果确定了几个与遗鸥相关生活史特征变化相关的基因，包括参与喙适应的BMP4；参与腭、软腭和舌进化的HAND2、NEUROG1、COL11A2和EDNRB；通过感知主食底物昆虫释放的化学分泌物来激活保护机制，从而增强对苦味反应的PIGR和PLCB2。此外，在扩展基因家族中鉴定出34个与精子发育和活性相关的基因，包括KLHL10和TEKT3。此外，MED1、CNOT9、NR5A1和PATZ1参与增强雄性激素分泌，并鉴定出与胚胎发育相关的高密度候选基因。研究结果表明，遗鸥种群处于雄性偏向的扩散模式；TEKT3基因的功能表明雄性在育雏中起主导作用，这增强了它们对雌性的吸引力。我们的研究揭示了嗅觉信号通路基因（包括OR14C36、OR14J1、OR14I1和OR14A16）、内耳发育相关基因（包括PTN、PTPN11、GATA2、ATP8B和MYO15A）以及与高海拔繁殖的低氧适应和虹膜颜色相关基因的显著富集。
基于这些结果以及对该生物生物学和栖息地利用的了解，我们推断遗鸥视觉上较低的适应性进化压力与其觅食行为和适应性有关。总之, 这一全面分析为遗鸥的进化特征提供了见解，并为遗鸥的科学研究提供了一个新的视角，以有效确定其未来的生存能力。
