Of Islands on Islands: Natural Habitat Fragmentation Drives Microallopatric Differentiation in the Context of Distinct Biological Assemblages

Abstract

An important evolutionary hypothesis posits that much of the biodiversity we see today arose during episodes of natural habitat fragmentation through the interplay of colonization, extinction, adaptation, and speciation. 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-equivalent (3% radius OTUs) and haplotype-equivalent (zOTUs) scales, we find that richness increases with kīpuka area, and that kīpuka exhibit faster distance decay of similarity compared to continuous forest. Kīpuka also differ in OTU and zOTU composition from continuous forest, notably hosting higher proportions of non-native OTUs for an arthropod order in which we can comprehensively classify native/non-native OTUs (Araneae). These findings reveal that natural habitat fragmentation drives parallel changes at species and haplotype scales in the kīpuka system. By integrating ecological and evolutionary perspectives, our study underscores the importance of studying both processes simultaneously if we are to understand, better predict, and more intelligently manage the responses of biological communities to environmental change.