Ecological and evolutionary mechanisms underlying patterns of phylosymbiosis in host-associated microbial communities

Abstract

Phylosymbiosis, where similarities in host-associated microbial communities recapitulate the phylogeny of their hosts, is a newly recognized yet pervasive pattern in the field of host–microbe interactions. While phylosymbiosis has been documented across many systems, we still have a poor understanding of the mechanisms that underlie this emergent pattern. Host selection of the microbiome is a widely cited mechanism, yet other basic ecological and evolutionary processes (dispersal, drift and diversification) may also be at play. This paper discusses the roles that each of these processes and their interactions may play in yielding phylosymbiotic signals across hosts. Finally, this paper will identify open questions and methods that are required to better understand the relative contributions of these basic processes to phylosymbiosis. Given that phylosymbiosis has been shown to relate to functional components of host fitness, understanding the processes that contribute to these patterns will be important for our understanding of the ecology and evolution of host–microbe interactions. This article is part of the theme issue ‘Conceptual challenges in microbial community ecology’.

Niche Specialization and Functional Overlap of Bamboo Leaf and Root Microbiota

“…Finally, environment conditions may obscure phylosymbiotic signals (Brooks et al, 2016). In addition, eco-evolutionary processes (selection, dispersal, drift, and diversification) (Cordovez et al, 2019;Kohl, 2020), and priority effect (Carlström et al, 2019) may also underlie the phylosymbiosis apart from host selection.…”

“…These two sites were 37.5 km apart and their climate conditions and environment surroundings quite resemble [both are subtropical monsoon climate with four distinct seasons, mean annual precipitation is 1,485 mm (ABEP) vs. 1,420 mm (ZAFU), and the mean annual temperature is 15 • C (ABEP) vs. 15.6 • C (ZAFU)] (Song et al, 2016), giving rise to the concordance of leaf microbiota from different bamboo genus. It is also possible that priority effect may play a role, which means that the first microbial colonizers of bamboo organs altered the inner physiology environment by activating the host immune system or though the production of bioactive compounds that inhibit the growth of other microbial species (Kohl, 2020). Nevertheless, more relevant experiments are needed to verify the detailed mechanisms underlying the relationship between bamboos and microbiota.…”

“…Phylosymbiosis is observed at one moment in time and space, which does not necessarily imply coevolution of hosts and their microbiota, but coevolution may be one mechanism contributing to observations of phylosymbiosis ( O’Brien et al, 2020 ). Ecological and evolutionary mechanisms (selection, dispersal, drift, and diversification) underlying patterns of phylosymbiosis in host-associated microbial communities have been discussed ( Kohl, 2020 ). Host selection or filtering of microbial communities is largely likely to be a dominant contributor to phylosymbiosis, yet, dispersal, drift, diversification, and interactions between these processes may also work ( Kohl, 2020 ).…”

“…Ecological and evolutionary mechanisms (selection, dispersal, drift, and diversification) underlying patterns of phylosymbiosis in host-associated microbial communities have been discussed ( Kohl, 2020 ). Host selection or filtering of microbial communities is largely likely to be a dominant contributor to phylosymbiosis, yet, dispersal, drift, diversification, and interactions between these processes may also work ( Kohl, 2020 ).…”

Patterns of microbiome variation among infrapopulations of permanent bloodsucking parasites

“…In general, both stochastic (e.g., dispersal, or ecological drift) and deterministic (e.g., host immunological regulation, or microbe-microbe interactions) processes operate across multiple spatial scales to shape the composition of animal microbiomes (Adair and Douglas 2017;Kohl 2020). In particular, among the many determinants shaping microbiome composition, host species identity has been repeatedly identified as a key factor determining the composition of animal microbiomes (Brooks et al 2016;Mazel et al 2018;Nishida and Ochman 2018;Lutz et al 2019;Knowles et al 2019;Lim and Bordenstein 2020;Song et al 2020).…”