A holobiont view of island biogeography: unraveling patterns driving the nascent diversification of a Hawaiian spider and its microbial associates

Abstract

The diversification of a host lineage can be influenced by both the external environment and its assemblage of microbes. Here, we use a young lineage of spiders, distributed along a chronologically arranged series of volcanic mountains, to determine the parallels between the evolutionary histories of the host spiders and their associated microbial communities, together forming the "holobiont". Using the stick spider Ariamnes waikula (Araneae, Theridiidae) on the island of Hawaii, and outgroup taxa on older islands, we tested whether each component of the holobiont (the spider hosts, the intracellular endosymbionts, and the gut microbial communities) showed correlated signatures of diversity due to sequential colonization from older to younger volcanoes. In order to investigate this, we generated ddRAD data for the host spiders and 16S rRNA gene amplicon data from their microbiota. We expected sequential colonizations to result in a (phylo)genetic structuring of the host spiders and in a diversity gradient in microbial communities. Results showed that the host A. waikula is indeed structured by geographic isolation, suggesting sequential colonization from older to younger volcanoes. Similarly, the endosymbiont communities were markedly different between Ariamnes species on different islands, but more homogeneous among A. waikula populations on the island of Hawaii. Conversely, the gut microbiota was largely conserved across all populations and species, which we suspect are generally environmentally derived. Our results highlight that the different components of the holobiont have responded in distinct ways to the dynamic environment of the volcanic archipelago, showing the necessity of understanding the interplay between components to better characterize holobiont evolution.