The biogeography of host‐associated bacterial microbiomes: Revisiting classic biodiversity patterns

Abstract

Background The question of which ecological and evolutionary processes structure the distribution of biodiversity has intrigued scientists for centuries, and historically, inferences have been gained predominantly by studying animals and plants. Although substantial progress has been made towards understanding the multitude of factors that shape host‐associated microbial communities (i.e., microbiomes), it remains largely unknown whether large‐scale geographical patterns in diversity observed for macroorganisms also apply for their microbiomes and whether microbiomes are shaped by the same processes that appear key for determining biogeographical patterns in their hosts. The geographical distribution of microbiome diversity We discuss challenges and potential approaches for studying microbiome biogeography, with the goal of inspiring future lines of research that can stimulate the development of new ecological and evolutionary theory in the microbiome field. The theory and examples presented here focus specifically on bacterial microbiomes, and we give an overview of host‐associated bacterial microbiome research beginning to examine some of the classic biodiversity patterns central to the fields of ecology and evolution. Potential impacts of microbiome variation for host ecology and evolution Microbiome diversity patterns are particularly important to consider because microbes are crucial for many aspects of the biology of their hosts. We discuss how more comprehensive knowledge of the geographical variation of microbiome diversity at the host individual and population levels might be crucial for understanding host ecology and evolution.

Host population crashes disrupt the diversity of associated marine microbiomes

“…The relationship between population density and microbiome diversity has recently been highlighted as an outstanding question in host-microbiome biogeography (Härer & Rennison, 2023). Differences in density that arise out of disturbance-induced population changes may explain the observed beta-diversity differences across disturbances due to reduced physical interactions between hosts.…”

“…For example, vertically acquired microbes may be more likely to persist long term in non‐disturbed populations, as the likelihood of being lost due to drift is reduced as more ‘replacement’ microbes of the same type are present in nearby D. antarctica . Nevertheless, the role of vertical transmission may be diminished due to increased exposure of external microbial communities to the environment (Härer & Rennison, 2023), alongside the associated wave‐induced biofilm and blade erosion. Out‐planted cultivated macroalgae also exhibit low levels of nursery‐microbe persistence, with greater acquisition of environmental microbes, suggesting horizontal transmission is a major factor in shaping macroalgal microbiomes (K. M. Davis et al, 2023).…”

The effects of host ecology and phylogeny on gut microbiota (non)parallelism across birds and mammals

“…For example, the broad diet categorization does not account for temporal and spatial variation in diet, which can strongly affect host-associated microbial communities ( 25 , 45 , 46 ). Besides, there is a plethora of technical (source material), host-associated (host morphology, physiology, and genetics) or environmental factors (abiotic conditions, geographic distribution) that can affect microbial community composition ( 5 , 12 , 47 , 48 ) and the resulting (non)parallelism estimates. An important next step would be to more rigorously test how parallel changes in specific host-associated or environmental factors, such as changes in salinity or temperature that have been shown to affect the composition of host-associated microbial communities ( 49 , 50 ), might affect microbiota (non)parallelism.…”

“…Diverse microbial communities form associations with multicellular hosts, and these associations seem to be ubiquitous across the animal kingdom ( 1 ). Microbes appear to play a crucial role in their hosts’ ecology and evolution ( 2 – 5 ). Gut microbiota are thought to be particularly important as they impact their host’s physiology in multiple ways, including nutrient metabolism ( 6 ).…”

Geographic Location Affects the Bacterial Community Composition and Diversity More than Species Identity for Tropical Tree Species

“…It is evident that the plant compartment shapes plant microorganisms, a fact that cannot be disputed [ 18 , 19 ]. Moreover, geographic variability is widely believed to play a fundamental role in structuring microbial communities [ 20 , 21 , 22 ]. Due to significant evolutionary associations between hosts and groups of bacteria, as well as selective filtering by hosts, bacteria have host specificity [ 23 , 24 ].…”