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 organism 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 evolutionary history of a host and its associated microbial communities, altogether forming the “holobiont”. Using the stick spider Ariamnes waikula (Araneae, Theridiidae) on the island of Hawai’i, and outgroup taxa on older islands, we tested whether the host spiders and their microbial constituents have responded in similar ways to the dynamic abiotic environment of the volcanic archipelago. The expectation was that each component of the holobiont (the spider hosts, intracellular endosymbionts, and gut microbiota) should show a similar pattern of 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. Results showed that the host A. waikula is strongly structured by isolation, suggesting sequential colonization from older to younger volcanoes. Similarly, the endosymbiont communities were markedly different between Ariamnes species on different islands, but more homogenized among A. waikula populations. In contrast, the gut microbiota was largely conserved across all populations and species, and probably mostly environmentally derived. Our results highlight the different evolutionary trajectories of the distinct components of the holobiont, showing the necessity of understanding the interplay between components in order to assess any role of the microbial communities in host diversification.

Differing Dietary Nutrients and Diet-Associated Bacteria Has Limited Impact on Spider Gut Microbiota Composition

“…Considering their complicated dietary regimens and diverse gut microbiota, spiders provide a suitable model to explore the degree to which diet or diet-acquired microbes impact the gut bacterial community. Many studies on microorganisms within spiders have focused on endosymbionts and their reproductive effects on their hosts [20][21][22], while other studies have identified and compared the gut microbiomes in different spider species [23][24][25][26]; analyzed the heritability of microbial communities within spiders [27]; and demonstrated that the gut microbiota of the spider Ariamnes waikula (Araneae, Theridiidae), which is found in the Hawaiian islands, to be fairly conserved for over 2 million years [28]. Although the existence of a common core microbiome in spiders remains elusive, gut bacteria in genera Acinetobacter, Pseudomonas, Bacillus are dominant and widely distributed in more than 40 spiders [23][24][25], while gut bacteria Staphylococcus, Corynebacterium, and Cutibacterium have varied abundance among the spiders.…”

Differing Dietary Nutrients and Diet-associated Bacteria has Limited Impact on Spider Gut Microbiota Composition

“…Considering their complicated dietary regimens and diverse gut microbiota, spiders provide a good model to explore the degree to which diet or diet-acquired microbes impact the gut bacterial community. A lot of studies on microorganisms within spiders have focused on endosymbionts and their reproductive effects on their hosts [24][25][26], while other studies have identi ed the gut microbiomes in three spider species [27]; analyzed the heritability of microbial communities within spiders [28]; and demonstrated that the gut microbiota of the Ariamnes spider, which is found in the Hawaiian islands, to be fairly conserved for over 2 million years [29].…”