Abstract

Microbial symbiosis and speciation profoundly shape the composition of life’s biodiversity. Despite the enormous contributions of these two fields to the foundations of modern biology, there is a vast and exciting frontier ahead for research, literature, and conferences to address the neglected prospects of merging their study. Here, we survey and synthesize exemplar cases of how endosymbionts and microbial communities affect animal hybridization and vice versa. We conclude that though the number of case studies remain nascent, the wide-ranging types of animals, microbes, and isolation barriers impacted by hybridization will likely prove general and a major new phase of study that includes the microbiome as part of the functional whole contributing to reproductive isolation. Though microorganisms were proposed to impact animal speciation a century ago, the weight of the evidence supporting this view has now reached a tipping point.

Highlights

  • Microbiomes, inclusive of intracellular and extracellular microorganisms, are often distinguishable across host body sites within species [14,15,16,17,18,19,20]

  • We set out to answer the following questions: How does hybridization affect the microbiome? Can hybrid maladies be facilitated by changes in the microbiome? And how do hybrid organisms differ from their parentals? The exemplars presented here offer a steppingstone to studies that comprehensively interrogate (i) the distinguishable nature of microbiomes across host species; (ii) the characterization and causes of microbial differences between hybrids and their parental species; and (iii) the microbial and host components of animal reproductive isolation and speciation

  • Moving forward, there are still several questions outstanding including: What types of hybrid reproductive isolation are most frequently impacted by microorganisms? Does natural selection in parental holobionts often lead to divergence in the host genome or microbiome and ensuing hybrid maladies? How have well-characterized systems of hybrid maladies overlooked the influences of microbial communities that previously went unmeasured in experiments? How do bacteriophages and viruses impact microbial community changes in hybrids?

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Summary

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Citation: Miller AK, Westlake CS, Cross KL, Leigh BA, Bordenstein SR (2021) The microbiome impacts host hybridization and speciation. PLoS Biol 19(10): e3001417. https://doi.org/10.1371/ journal.pbio.3001417 Funding: This work was supported by the Vanderbilt Innovation Center to S.R.B., a Searle Undergraduate Research Program (SyBBURE) Fellowship to A.K.M., an NIH Ruth Kirschstein Postdoctoral Fellowship F32 AI140694-03 to B.A. L., and an NSF Postdoctoral Research Fellowship in Biology Grant No 2010695 to K.L.C. We thank Mahip Kalra for assistance with figure editing. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Living and evolving in a microbial world
PLOS BIOLOGY
Lessons learned from case studies
Findings
Concluding remarks
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