A holobiont view of island biogeography: Unravelling 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 investigate how their associated microbial communities have changed as the spiders colonized new locations. Using the stick spider Ariamnes waikula (Araneae, Theridiidae) on the island of Hawaiʻi, and outgroup taxa on older islands, we tested whether each component of the “holobiont” (spider hosts, intracellular endosymbionts and gut microbial communities) showed correlated signatures of diversity due to sequential colonization from older to younger volcanoes. 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. The results showed that the host A. waikula is indeed structured by geographical 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 Hawaiʻi. Conversely, the gut microbiota, which we suspect is generally environmentally derived, was largely conserved across all populations and species. Our results show that different components of the holobiont respond in distinct ways to the dynamic environment of the volcanic archipelago. This highlights the necessity of understanding the interplay between different components of the holobiont, to properly characterize its evolution.

Limited Evidence for Microbial Transmission in the Phylosymbiosis between Hawaiian Spiders and Their Microbiota

“…Using previously published data on Hawaiian Ariamnes spiders and their associated microbiota ( 17 ), we confirmed that the evolutionary history of the 63 sampled Ariamnes spiders reconstructed using double digest restriction site-associated DNA (ddRAD) markers presented a clustering by geographic area ( Fig. 1a ).…”

“…Irrespective of how a host acquires its microbiota, microbiotas of closely related host species are often more similar than those of distantly related species, such that host dendrograms constructed from the similarities of whole microbiota communities tend to mirror the host phylogeny ( 13 , 14 ). This pattern, referred to as phylosymbiosis, has for example been documented for the gut microbiotas of primates ( 15 , 16 ) and arthropods ( 17 ) and in the roots of plants ( 18 ). However, how and why this pattern emerges has been intensively debated ( 12 , 19 ).…”

“…Here, we used HOME to investigate the modes of inheritance of the bacterial microbiota of a lineage of Hawaiian spiders in the genus Ariamnes that exhibit a significant pattern of phylosymbiosis ( 17 ). Our goal was to examine whether this empirical pattern of phylosymbiosis (at the whole-microbiota community level) is explained by vertically transmitted microbes (at the level of individual microbial lineages).…”

“…Ariamnes spiders are nonmodel organisms, and whether their associated microbes are vertically transmitted is unknown. In general, spider-associated bacteria can be either unspecific and transient ( 5 ) or intimate and maternally transmitted symbionts ( 36 ), as is commonly the case for endosymbiotic intracellular bacteria that colonize most spider tissues, including the midgut ( 17 , 36 ). Previous work has shown that Hawaiian Ariamnes spiders have a diverse and relatively stable gut microbiota composed mainly of Proteobacteria and Firmicutes , and each spider is colonized by at least one endosymbiont from the genera Wolbachia , Rickettsia , and Rickettsiella ( 17 ).…”

“…In general, spider-associated bacteria can be either unspecific and transient ( 5 ) or intimate and maternally transmitted symbionts ( 36 ), as is commonly the case for endosymbiotic intracellular bacteria that colonize most spider tissues, including the midgut ( 17 , 36 ). Previous work has shown that Hawaiian Ariamnes spiders have a diverse and relatively stable gut microbiota composed mainly of Proteobacteria and Firmicutes , and each spider is colonized by at least one endosymbiont from the genera Wolbachia , Rickettsia , and Rickettsiella ( 17 ). Because the different species of Hawaiian Ariamnes are highly specialized (similar habitat and very narrow and conserved diet relative to other spiders) and are closely related within an island, we thus expected (i) their niche conservatism to favor microbial vertical transmission, at least for the endosymbionts, and (ii) their geographical clustering to influence host switch dynamics.…”