A holobiont view of island biogeography: Unravelling patterns driving the nascent diversification of a Hawaiian spider and its microbial associates
In their recent paper in Molecular Ecology, Armstrong and Perez-Lamarque et al investigated the evolution of the holobiont. The holobiont is the assemblage of species associated with a particular host organism. In the case of this study, the holobiont refers to the stick spider (Ariamnes), its microbiome and its endosymbionts. Taking advantage of the successive colonization of islands in a volcanic archipelego, Armstrong and Perez-Lamarque et al contrasted the evolutionary history of the host species to the different components of the holobiont on different islands in Hawai’i.
We sent some questions to the authors of this work and here’s what Benoît Perez-Lamarque, Rosemary Gillespie and Henrik Krehenwinkel had to say.
What led to your interest in this topic / what was the motivation for this study?
Gut microbiota play multiple roles in the functioning of animal organisms. In addition, host-associated microbiota composition can be relatively conserved over time and the concept of the “holobiont” has been proposed to describe the ecological unit formed by the host and its associated microbial communities. Yet, it remains unclear how the different components of the holobiont (the hosts and the microbial communities) evolve. This is what spurred our interest. Taking advantages of the chronologically arranged series of volcanic mountains of the Hawaiian archipelago, we were able to tackle this question and could investigate how the different components of the holobiont have changed as the host spiders colonized new locations.
Can you describe the significance of this research for the general scientific community in one sentence?
The evolution of Hawaiian spider hosts and their associated microbes are differently impacted by the dynamic environment of the volcanic archipelago.
Can you describe the significance of this research for your scientific community in one sentence.
The host and its associated microbiota may not act as a single and homogeneous unit of selection over evolutionary timescales.
What difficulties did you run into along the way?
All the different components of the holobiont are not as easy to study. For instance, for the host spiders, we used double digest RAD sequencing (ddRAD) to obtain genome-wide single nucleotide polymorphism data. With such data, we could precisely reconstruct the evolutionary histories of the different spider populations in the last couple of million years and tracked the finest changes in their genetic diversity. In contrast, characterizing the composition of the microbial components is much more challenging. We used metabarcoding of a short region of the 16S rRNA gene to identify the bacteria present. However, over such short evolutionary timescales, this DNA region is too conserved to accumulate many differences between isolated populations. Therefore, we had high-resolution data for the spider hosts but comparably low-resolution data for the bacterial communities. To ensure that the observed patterns were not artefactually driven by such differences of resolutions, we complemented our analyses with a range of simulations to assess the robustness of our findings.
What is the biggest or most surprising innovation highlighted in this study?
We find that the different components of the holobiont (the host spiders, the intracellular endosymbionts, and gut microbial communities) respond in distinct ways to the dynamic environment of the Hawaiian archipelago. While the host spiders have experienced sequential colonizations from older to younger volcanoes, resulting in a strong (phylo)genetic structuring across the archipelago’s chronosequence, the gut microbiota was largely conserved in all populations irrespectively of the archipelago’s chronosequence. More intermediately, we found different endosymbiont genera colonizing the spiders on each island. This suggests that this holobiont does not necessarily evolve as a single unit over long timescales.
In the conclusion to your study, you point out how different components of the holobiont likely contribute differently to selection/colonization history in this system. If you had unlimited resources, what would you do to strengthen this conclusion?
We indeed suspect that the different components of the holobiont probably did not act as a single and homogeneous unit of selection during the colonization of the Hawaiian archipelago. First, it would be ideal to perform an even broader sampling, targeting more Ariamnes populations and species from older islands, to better characterize the long-term changes of the different holobiont components. Using sequencing technics with better resolution (as detailed below) would also improve our characterization of the microbial component(s) of the holobiont. Second, to properly test for selection, we should perform transplant experiments of the bacterial communities between spider populations/species and measure whether or not it impacts holobiont fitness. We would expect to find a significant impact of the transplant for the endosymbionts, but no or low impact for the gut bacterial communities of these spiders.
The geological history of Hawai’i provides a powerful system to build understanding of the evolution of holobiont. Are you aware of other systems where similar studies could be performed? (I appreciate that this is related to the previous question!).
Many other archipelagos, with similar island chronosequences, like the Canary Islands or the Society Islands, are also ideal for testing hypotheses on the evolution of holobionts. Within the Hawaiian archipelago again, we could replicate our work on other holobiont systems. For instance, among arthropods, plant feeders might rely more importantly on their microbiota for their nutrition, and this might likely translate into different patterns of holobiont evolution.
Moving forward, what are the next steps in this area of research?
As previously said, one main limitation is the low resolution of the 16S rRNA metabarcoding. This prevented us to look at the evolutionary history of the individual bacterial lineages. Using a new model, we have recently tackled this issue of low resolution (https://doi.org/10.1128/msystems.01104-21) and we reported little evidence of microbial vertical transmission in these holobionts. Yet, the next step would be to move from classical metabarcoding to metabarcoding with longer sequencing reads (e.g. the whole 16S rRNA gene) or even metagenomics. It would provide more resolution for looking at bacterial evolution and would also bring more information on the functioning of these bacterial communities (e.g. are gut microbiota contributing to the digestion of these Hawaiian spiders in natural environments?).
Armstrong, E. E.*, Perez-Lamarque, B.*, Bi, K., Chen, C., Becking, L. E., Lim, J. Y., Linderoth, T., Krehenwinkel, H., & Gillespie, R. G. (2022). A holobiont view of island biogeography: Unravelling patterns driving the nascent diversification of a Hawaiian spider and its microbial associates. Molecular Ecology, 31, 1299– 1316.
*Authors contributed equally