Weng Yi-Ming, Martinez Jose I, Markee Amanda, Plotkin David, Sondhi Yash, Mongue Andrew J, Frandsen Paul B, Kawahara Akito Y
McGuire Center for Lepidoptera & Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL, USA.
Florida Department of Agriculture and Consumer Services, Gainesville, FL, USA.
Genome Biol Evol. 2025 Sep 2;17(9). doi: 10.1093/gbe/evaf156.
Butterflies and moths (Lepidoptera) are a megadiverse lineage of approximately 160,000 described species. Their evolutionary success is thought to be closely linked to the radiation of flowering plants and represents a classic example of co-evolution. However, mechanisms by which these insects evolved to feed on such diverse plant hosts remain largely unknown. Previous studies found emergent gene families of odorant receptors and peptidases in the ancestor of Lepidoptera, suggesting these genetic innovations may be linked to Lepidoptera diversification. Here, we examined 431 genomes and identified lineage-specific gene families within Lepidoptera and 3 key nested clades. We found 54, 88, 77, and 4 functionally annotated gene families specific to Lepidoptera, Glossata, Ditrysia, and Apoditrysia, respectively. These gene families are involved in chemosensation, digestion, detoxification, immunity, and other functions. There was a marked increase in gene families presumably associated with chemosensation and immunity in Glossata and Ditrysia, clades which encompass more than 98% of Lepidoptera species diversity. We also identified horizontal gene transfer (HGT) events involving two putative digestion-related gene families (Catalytic LigB subunit of aromatic ring-opening dioxygenase and Glycosyl hydrolases family 32) and a detoxification gene family (Cysteine synthase-like), likely acquired in the common ancestors of Lepidoptera and Ditrysia, respectively. These HGT events likely played a pivotal role in facilitating dietary transitions from algae, diatoms, and aquatic plant debris to fungi and early terrestrial plants, ultimately enabling Lepidoptera to adapt to and diversify on angiosperm hosts.
蝴蝶和飞蛾（鳞翅目）是一个拥有约16万种已描述物种的超级多样化谱系。它们在进化上的成功被认为与开花植物的辐射密切相关，是共同进化的一个经典例子。然而，这些昆虫进化为以如此多样的植物宿主为食的机制在很大程度上仍然未知。先前的研究在鳞翅目祖先中发现了气味受体和肽酶的新兴基因家族，表明这些基因创新可能与鳞翅目的多样化有关。在这里，我们研究了431个基因组，并确定了鳞翅目及其3个关键嵌套分支中的谱系特异性基因家族。我们分别发现了54个、88个、77个和4个功能注释的基因家族，它们分别特异性存在于鳞翅目、有喙亚目、双孔亚目和真蝶总科中。这些基因家族涉及化学感应、消化、解毒、免疫和其他功能。在有喙亚目和双孔亚目中，可能与化学感应和免疫相关的基因家族显著增加，这两个分支包含了超过98%的鳞翅目物种多样性。我们还确定了水平基因转移（HGT）事件，涉及两个假定的与消化相关的基因家族（芳香环开裂双加氧酶的催化LigB亚基和糖基水解酶家族32）和一个解毒基因家族（类半胱氨酸合酶），它们可能分别在鳞翅目和双孔亚目的共同祖先中获得。这些HGT事件可能在促进从藻类、硅藻和水生植物碎片到真菌和早期陆生植物的饮食转变中发挥了关键作用，最终使鳞翅目能够适应被子植物宿主并实现多样化。
