Kirsch Roy, Okamura Yu, García-Lozano Marleny, Weiss Benjamin, Keller Jean, Vogel Heiko, Fukumori Kayoko, Fukatsu Takema, Konstantinov Alexander S, Montagna Matteo, Moseyko Alexey G, Riley Edward G, Slipinski Adam, Vencl Fredric V, Windsor Donald M, Salem Hassan, Kaltenpoth Martin, Pauchet Yannick
Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745 Jena, Germany.
Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745 Jena, Germany; Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo 113-0033, Japan.
Curr Biol. 2025 Feb 3;35(3):640-654.e7. doi: 10.1016/j.cub.2024.12.028. Epub 2025 Jan 17.
Beetles that feed on the nutritionally depauperate and recalcitrant tissues provided by the leaves, stems, and roots of living plants comprise one-quarter of herbivorous insect species. Among the key adaptations for herbivory are plant cell wall-degrading enzymes (PCWDEs) that break down the fastidious polymers in the cell wall and grant access to the nutritious cell content. While largely absent from the non-herbivorous ancestors of beetles, such PCWDEs were occasionally acquired via horizontal gene transfer (HGT) or by the uptake of digestive symbionts. However, the macroevolutionary dynamics of PCWDEs and their impact on evolutionary transitions in herbivorous insects remained poorly understood. Through genomic and transcriptomic analyses of 74 leaf beetle species and 50 symbionts, we show that multiple independent events of microbe-to-beetle HGT and specialized symbioses drove convergent evolutionary innovations in approximately 21,000 and 13,500 leaf beetle species, respectively. Enzymatic assays indicate that these events significantly expanded the beetles' digestive repertoires and thereby contributed to their adaptation and diversification. Our results exemplify how recurring HGT and symbiont acquisition catalyzed digestive and nutritional adaptations to herbivory and thereby contributed to the evolutionary success of a megadiverse insect taxon.
以活植物的叶、茎和根所提供的营养匮乏且难以分解的组织为食的甲虫，占食草昆虫种类的四分之一。食草的关键适应性特征之一是植物细胞壁降解酶（PCWDEs），它能分解细胞壁中难以处理的聚合物，从而获取营养丰富的细胞内容物。虽然在甲虫的非食草祖先中基本不存在，但这种植物细胞壁降解酶偶尔会通过水平基因转移（HGT）或摄取消化共生体而获得。然而，植物细胞壁降解酶的宏观进化动态及其对食草昆虫进化转变的影响仍知之甚少。通过对74种叶甲物种和50种共生体进行基因组和转录组分析，我们发现微生物到甲虫的多次独立水平基因转移事件和特殊共生关系分别在约21000种和13500种叶甲物种中推动了趋同进化创新。酶活性测定表明，这些事件显著扩展了甲虫的消化能力，从而促进了它们的适应和多样化。我们的研究结果例证了反复发生的水平基因转移和共生体获取如何催化了对食草的消化和营养适应，进而促成了一个超级多样化昆虫类群的进化成功。
