Host Niches and Defensive Extended Phenotypes Structure Parasitoid Wasp Communities

Oak galls are spectacular extended phenotypes of gallwasp genes in host oak tissues and have evolved complex morphologies that serve, in part, to exclude parasitoid natural enemies.Parasitoids and their insect herbivore hosts have coevolved to produce diverse communities comprising about a third of all animal species. The factors structuring these communities, however, remain poorly understood. An emerging theme in community ecology is the need to consider the effects of host traits, shaped by both natural selection and phylogenetic history, on associated communities of natural enemies. Here we examine the impact of host traits and phylogenetic relatedness on 48 ecologically closed and species-rich communities of parasitoids attacking gall-inducing wasps on oaks. Gallwasps induce the development of spectacular and structurally complex galls whose species- and generation-specific morphologies are the extended phenotypes of gallwasp genes. All the associated natural enemies attack their concealed hosts through gall tissues, and several structural gall traits have been shown to enhance defence against parasitoid attack. Here we explore the significance of these and other host traits in predicting variation in parasitoid community structure across gallwasp species. In particular, we test the ��Enemy Hypothesis,�� which predicts that galls with similar morphology will exclude similar sets of parasitoids and therefore have similar parasitoid communities. Having controlled for phylogenetic patterning in host traits and communities, we found significant correlations between parasitoid community structure and several gall structural traits (toughness, hairiness, stickiness), supporting the Enemy Hypothesis. Parasitoid community structure was also consistently predicted by components of the hosts' spatiotemporal niche, particularly host oak taxonomy and gall location (e.g., leaf versus bud versus seed). The combined explanatory power of structural and spatiotemporal traits on community structure can be high, reaching 62% in one analysis. The observed patterns derive mainly from partial niche specialisation of highly generalist parasitoids with broad host ranges (>20 hosts), rather than strict separation of enemies with narrower host ranges, and so may contribute to maintenance of the richness of generalist parasitoids in gallwasp communities. Though evolutionary escape from parasitoids might most effectively be achieved via changes in host oak taxon, extreme conservatism in this trait for gallwasps suggests that selection is more likely to have acted on gall morphology and location. Any escape from parasitoids associated with evolutionary shifts in these traits has probably only been transient, however, due to subsequent recruitment of parasitoid species already attacking other host galls with similar trait combinations.

栎瘿（oak galls）是寄生在宿主栎树组织中的瘿蜂（gallwasp）基因所表达的显著延伸表型，其演化出复杂的形态结构，部分功能便是抵御寄生性天敌（parasitoid）的侵袭。寄生性天敌与其植食性昆虫宿主协同演化，形成了占所有动物物种约三分之一的多样群落。然而，塑造这类群落的核心机制仍未得到充分阐释。群落生态学领域的新兴研究范式指出，需同时考量由自然选择与系统发育历史共同塑造的宿主性状，对其关联的天敌群落所产生的影响。本研究针对48个生态封闭、物种丰富的寄生蜂群落展开分析，这些群落均以栎树上的造瘿蜂为宿主，借此检验宿主性状与系统发育亲缘关系对这类群落的影响。瘿蜂可诱导宿主栎树形成形态壮观、结构复杂的瘿，这类具有物种与世代特异性的形态结构，正是瘿蜂基因的延伸表型。所有与之关联的天敌均需通过瘿组织侵袭其隐蔽的宿主，且已有研究证实，多项瘿的结构性状可提升宿主对寄生蜂侵袭的防御能力。本研究旨在探究上述及其他宿主性状，对不同瘿蜂物种间寄生蜂群落结构差异的预测效力。我们尤其针对“天敌假说（Enemy Hypothesis）”展开检验：该假说预测，形态相似的瘿会排斥相似类群的寄生蜂，因此其对应的寄生蜂群落结构也会趋于一致。在控制宿主性状与群落的系统发育格局后，我们发现寄生蜂群落结构与多项瘿的结构性状（硬度、被毛程度、粘性）之间存在显著相关性，这一结果支持了天敌假说。寄生蜂群落结构同样可通过宿主的时空生态位特征得到稳定预测，其中尤以宿主栎树的分类学属性与瘿的着生位置（如着生于叶片、芽体或种子）最为显著。结构性状与时空生态位特征的组合对群落结构的解释力可达较高水平，在某一分析中其解释度高达62%。本研究观测到的格局主要源于寄主范围极广（宿主种类超过20种）的广食性寄生蜂的部分生态位特化，而非寄主范围较窄的天敌的严格生态位分离，因此这一结果或有助于维持瘿蜂群落中广食性寄生蜂的物种丰富度。尽管通过改变宿主栎树的分类学类群，或许能最有效地实现对寄生蜂的演化逃逸，但瘿蜂在该性状上存在极强的保守性，这表明自然选择更倾向于作用于瘿的形态与着生位置。然而，通过上述性状的演化改变实现的寄生蜂逃逸，大概率仅为短暂现象——因为后续会有已适应其他具有相似性状组合的宿主瘿的寄生蜂物种，重新入侵该类群。