Of islands on islands: Natural habitat fragmentation drives microallopatric differentiation in the context of distinct biological assemblages

An important evolutionary hypothesis posits that much of the biodiversity we see today was generated by the interplay of colonization, extinction, adaptation, and speciation during episodes of natural habitat fragmentation. To interrogate the generality of this hypothesis, we leverage the natural experiment provided by arthropod communities in kīpuka—patches of Hawaiian wet forest isolated by lava flows. With DNA metabarcoding, we provide the first simultaneous exploration of ecological and evolutionary characteristics in the kīpuka system. At both species- and haplotype-equivalent scales, we find that diversity scales with kīpuka area, and that kīpuka accelerate the distance decay of similarity relative to continuous forest. Open lava, kīpuka edges, and the centers of the smallest kīpuka host lower inter- and intra-specific richness, are more biologically homogeneous, and have higher proportions of non-native OTUs than kīpuka centers for the order we could test (Araneae). Our work shows how natural habitat fragmentation stimulates, in tandem, ecological shifts in community composition and genetic differentiation. The strong signatures of both ecological and evolutionary processes highlight the importance of studying both processes simultaneously if we are to understand how biological communities respond to change.

Methods
See "Materials and methods" of the manuscript.

一项重要的进化假说提出，当前所见的绝大多数生物多样性，均源自自然生境破碎化事件中，定殖、灭绝、适应与物种形成之间的相互作用。为验证该假说的普适性，我们依托由熔岩流分隔的夏威夷湿林斑块（即基普卡，kīpuka）内的节肢动物群落所构成的自然实验开展研究。本研究借助DNA元条形码（DNA metabarcoding）技术，首次对基普卡系统中的生态与进化特征开展同步探究。在物种与单倍型等效尺度下，我们发现多样性随基普卡面积呈正比关系，且相较于连续森林，基普卡会加快相似性的距离衰减效应。在我们可开展检测的蜘蛛目（Araneae）类群中，裸露熔岩、基普卡边缘以及最小基普卡的中心区域，其种间与种内丰富度均低于基普卡中心区域，生物学同质性更强，且非本土操作分类单元（OTU, Operational Taxonomic Unit）的占比更高。本研究揭示了自然生境破碎化如何同时推动群落组成的生态转变与遗传分化。生态与进化过程均留下了显著信号，这表明若要理解生物群落如何响应环境变化，同步探究这两类过程至关重要。
方法
详见论文的「材料与方法」部分。