Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, 02138, USA.
Museum of Comparative Zoology, Harvard University, Cambridge, MA, 02138, USA.
New Phytol. 2023 Dec;240(5):2050-2057. doi: 10.1111/nph.19266. Epub 2023 Oct 5.
Endophytic feeding behaviors, including stem borings and galling, have been observed in the fossil record from as early as the Devonian and involve the consumption of a variety of plant (and fungal) tissues. Historically, the exploitation of internal stem tissues through galling has been well documented as emerging during the Pennsylvanian (c. 323-299 million years ago (Ma)), replaced during the Permian by galling of foliar tissues. However, leaf mining, a foliar endophytic behavior that today is exhibited exclusively by members of the four hyperdiverse holometabolous insect orders, has been more sparsely documented, with confirmed examples dating back only to the Early Triassic (c. 252-250 Ma). Here, we describe a trace fossil on seed-fern foliage from the Rhode Island Formation of Massachusetts, USA, representing the earliest indication of a general, endophytic type of feeding damage and dating from the Middle Pennsylvanian (c. 312 Ma). Although lacking the full features of Mesozoic leaf mines, this specimen provides evidence of how endophytic mining behavior may have originated. It sheds light on the evolutionary transition to true foliar endophagy, contributes to our understanding of the behaviors of early holometabolous insects, and enhances our knowledge of macroevolutionary patterns of plant-insect interactions.
内生取食行为，包括茎内取食和虫瘿，在早泥盆世的化石记录中就已被观察到，涉及多种植物（和真菌）组织的消耗。历史上，通过虫瘿对内部茎组织的利用在宾夕法尼亚纪（约 3.23 亿至 2.99 亿年前）得到了很好的记录，在二叠纪时期，叶组织的虫瘿取代了茎组织的虫瘿。然而，叶内取食，一种今天仅由四个高度多样化的完全变态昆虫目成员表现出的叶内取食行为，记录得较少，确认的例子只能追溯到早三叠世（约 2.52 亿至 2.5 亿年前）。在这里，我们描述了来自美国马萨诸塞州罗得岛组的种子蕨叶上的一个痕迹化石，这代表了最早的一般性内生取食损伤的迹象，其年代为宾夕法尼亚纪中期（约 3.12 亿年前）。虽然缺乏中生代叶内取食痕迹的全部特征，但这个标本提供了关于内生取食行为如何起源的证据。它揭示了内生取食行为向真正的叶内取食的进化转变，有助于我们理解早期完全变态昆虫的行为，并增进我们对植物-昆虫相互作用的宏观进化模式的了解。
