Phylogeny, Evolution and Classification of Gall Wasps: The Plot Thickens

Gall wasps (Cynipidae) represent the most spectacular radiation of gall-inducing insects. In addition to true gall formers, gall wasps also include phytophagous inquilines, which live inside the galls induced by gall wasps or other insects. Here we present the first comprehensive molecular and total-evidence analyses of higher-level gall wasp relationships. We studied more than 100 taxa representing a rich selection of outgroups and the majority of described cynipid genera outside the diverse oak gall wasps (Cynipini), which were more sparsely sampled. About 5 kb of nucleotide data from one mitochondrial (COI) and four nuclear (28S, LWRh, EF1alpha F1, and EF1alpha F2) markers were analyzed separately and in combination with morphological and life-history data. According to previous morphology-based studies, gall wasps evolved in the Northern Hemisphere and were initially herb gallers. Inquilines originated once from gall inducers that lost the ability to initiate galls. Our results, albeit not conclusive, suggest a different scenario. The first gall wasps were more likely associated with woody host plants, and there must have been multiple origins of gall inducers, inquilines or both. One possibility is that gall inducers arose independently from inquilines in several lineages. Except for these surprising results, our analyses are largely consistent with previous studies. They confirm that gall wasps are conservative in their host-plant preferences, and that herb-galling lineages have radiated repeatedly onto the same set of unrelated host plants. We propose a revised classification of the family into twelve tribes, which are strongly supported as monophyletic across independent datasets. Four are new: Aulacideini, Phanacidini, Diastrophini and Ceroptresini. We present a key to the tribes and discuss their morphological and biological diversity. Until the relationships among the tribes are resolved, the origin and early evolution of gall wasps will remain elusive.瘿蜂科（Cynipidae）的瘿蜂是诱导虫瘿昆虫中物种辐射演化最为显著的类群。除真正的虫瘿诱导者外，瘿蜂科还包含植食性寄居类群——它们栖息于瘿蜂或其他昆虫诱导形成的虫瘿内部。本研究首次针对瘿蜂科的高阶系统发育关系，开展了全面的分子与整合证据分析。本研究涵盖100余个类群，包含大量外类群以及多数已描述的非多样栎瘿蜂族（Cynipini）瘿蜂属类群，而栎瘿蜂族类群的采样相对稀疏。我们选取了1个线粒体分子标记（COI）与4个核分子标记（28S、LWRh、EF1α F1、EF1α F2），获得了约5 kb的核苷酸序列数据，并分别与联合形态学、生活史数据开展分析。依据既往基于形态学的研究结论，瘿蜂起源于北半球，最初为草本植物虫瘿诱导者，而寄居类群仅单次起源于丧失虫瘿诱导能力的瘿蜂诱导者。尽管本研究结果尚不具备定论性，但却指向了一套截然不同的演化假说：原始瘿蜂更可能与木本寄主植物相关联，且虫瘿诱导者、寄居类群或二者均存在多次独立起源事件，其中一种可能性为多个演化支中的虫瘿诱导者均独立起源于寄居类群。除上述令人意外的结论外，本研究的分析结果整体与既往研究相符，证实了瘿蜂对寄主植物的选择具有保守性，且草本虫瘿诱导类群曾多次独立辐射演化至同一组非近缘寄主植物上。我们提出了瘿蜂科的修订分类系统，将其划分为12个族，各候选族均得到独立数据集的强烈单系支持，其中4个族为新定义类群：Aulacideini、Phanacidini、Diastrophini及Ceroptresini。本研究同时提供了各属族的分类检索表，并讨论了其形态学与生物学多样性。在明确各属族间的系统发育关系之前，瘿蜂的起源与早期演化历程仍将难以厘清。