Andreas Härer

Microbial communities are critical to the functioning of ecosystems and shape the ecology and evolution of host organisms. However, we have a limited understanding of how host‐associated and free‐living microbes differ in their structure and biogeography. Here, we test whether host‐associated (fish gut) and free‐living (lake bacterioplankton) microbes exhibit different metacommunity structure, spatial turnover, and consistency with neutral expectations using two independent lake systems. We characterized microbial communities in lake water (Vancouver Island and Sierra Nevada) and guts in two fish species (stickleback and brook trout) using 16S amplicon sequencing. We compared alpha and beta diversity within lakes, quantified spatial turnover (distance‐decay), and tested for departure from neutral abundance‐occurrence expectations between bacterioplankton and fish gut microbiomes. Fish microbiomes had lower alpha diversity compared to bacterioplankton, but higher beta diversity within lakes. Bacterioplankton were more similar across lakes yet showed stronger patterns of spatial turnover with distance than fish gut microbiomes. A neutral model explained a substantial proportion of abundance‐occurrence relationships in bacterioplankton communities but performed poorly for fish‐associated microbes. Our study indicates that host‐associated and free‐living microbes have disparate patterns of metacommunity structure and spatial turnover consistent with differences in the strength of neutral ecological processes. Fish microbiomes were less diverse at the local scale but more variable across space and time than bacterioplankton communities, suggestive of potentially strong local selection and/or reduced microbial exchange among hosts compared to environmental communities. Importantly, we observed highly consistent patterns across both lake systems despite differences in host species, sampling design, and region, demonstrating that differences in the distribution of host and environmental microbes are potentially widespread. This study demonstrates how host association fundamentally alters the diversity and spatial distribution of microbes, emphasizing the need to incorporate hosts into broader frameworks of microbial biogeography.

Microbial communities are critical to the functioning of ecosystems and shape the ecology and evolution of host organisms. However, we have a limited understanding of how host-associated and free-living microbes differ in their structure and biogeography. Here, we test whether host-associated (fish gut) and free-living (lake bacterioplankton) microbes exhibit different metacommunity structure, spatial turnover, and consistency with neutral expectations using two independent lake systems. We characterized microbial communities in lake water (Vancouver Island and Sierra Nevada) and guts in two fish species (stickleback and brook trout) using 16S amplicon sequencing. We compared alpha and beta diversity within lakes, quantified spatial turnover (distance-decay), and tested for departure from neutral abundance-occurrence expectations between bacterioplankton and fish gut microbiomes. Fish microbiomes had lower alpha diversity compared to bacterioplankton, but higher beta diversity within lakes. Bacterioplankton were more similar across lakes yet showed stronger patterns of spatial turnover with distance than fish gut microbiomes. A neutral model explained a substantial proportion of abundance-occurrence relationships in bacterioplankton communities but performed poorly for fish-associated microbes. Our study indicates that host-associated and free-living microbes have disparate patterns of metacommunity structure and spatial turnover consistent with differences in the strength of neutral ecological processes. Fish microbiomes were less diverse at the local scale but more variable across space and time than bacterioplankton communities, suggestive of potentially strong local selection and/or reduced microbial exchange among hosts compared to environmental communities. Importantly, we observed highly consistent patterns across both lake systems despite differences in host species, sampling design, and region, demonstrating that differences in the distribution of host and environmental microbes are potentially widespread. This study demonstrates how host association fundamentally alters the diversity and spatial distribution of microbes, emphasizing the need to incorporate hosts into broader frameworks of microbial biogeography.

Background: Despite the growing recognition of the importance of gut microbiota in host ecology and evolution, our understanding of the relative contributions of host-associated and environmental factors shaping gut microbiota composition within and across wild populations remains limited. Here, we investigate how host morphology, sex, genetic divergence, and environmental characteristics influence the gut microbiota of threespine stickleback fish populations from 20 lakes on Vancouver Island, Canada. Results: Our findings reveal substantial variation in gut microbiota composition and diversity among populations, with host traits exerting a relatively stronger influence on bacterial alpha diversity than environmental characteristics. Previous studies have suggested a link between stickleback body shape and niche specialization, and our results indicate that aspects of host morphology may be associated with gut microbiota divergence among populations, though whether this is related to trophic ecology remains to be explored. Within and across populations, we only observed a weakly defined core microbiota and limited sharing of amplicon sequence variants (ASVs) among hosts, indicating that gut microbiota composition is individualized. Additionally, we detected sex-dependent differences in microbial diversity, opening avenues for future research into the mechanisms driving this variation. Conclusions: In sum, our study emphasizes the need to consider both host-associated and environmental factors in shaping gut microbiota dynamics and highlights the complex interplay between host organisms, their associated microbial communities, and the environment in natural settings. Ultimately, these insights add to our understanding of the eco-evolutionary implications of host-microbiota interactions while underscoring the need for further investigation into the underlying mechanisms.

Research on microbial biogeography has revealed key patterns like the diversity–area relationship and distance–decay of similarity. However, how habitat size affects bacterial diversity in freshwater environments remains largely unclear. Here, we characterize bacterial communities in the littoral zones of 10 mountain lakes in the Sierra Nevada, CA, ranging in surface area from 0.92 to 71.72 ha. Despite significant habitat size effects on community composition, dominant bacterial phyla were shared across lakes. We found no evidence for diversity–area relationships, either in single samples (alpha diversity) or cumulative lake-level samples (within-lake gamma diversity), when accounting for environmental variation. Moreover, within-lake beta diversity showed little spatial structuring, with similar bacterial community composition across samples regardless of geographic distance. Gamma diversity did not reach saturation with our sample size, and lake size had no effect on the predicted sample size necessary to reach gamma diversity saturation. Our findings offer new insights into diversity–area dynamics and spatial structuring by investigating alpha, beta, and gamma diversity in freshwater environments. Notably, individual water samples captured much of the bacterial community, with strong correlations between alpha and gamma diversity. These results advance our understanding of microbial biogeography and inform sampling designs for characterizing bacterial diversity in freshwater ecosystems.

Background: Despite the growing recognition of the importance of gut microbiota in host ecology and evolution, our understanding of the relative contributions of host-associated and environmental factors shaping gut microbiota composition within and across wild populations remains limited. Here, we investigate how host morphology, sex, genetic divergence, and environmental characteristics influence the gut microbiota of threespine stickleback fish populations from 20 lakes on Vancouver Island, Canada. Results: Our findings reveal substantial variation in gut microbiota composition and diversity among populations, with host traits exerting a stronger influence on bacterial alpha diversity than environmental characteristics. Host morphology, which is indicative of trophic ecology, was linked to gut microbiota divergence among populations, suggesting that dietary specialization may play a role in shaping the stickleback gut microbiota. Within and across populations, we only observed a weakly defined core microbiota and limited sharing of ASVs among hosts, indicating that gut microbiota composition is individualized. Additionally, we detected sex-dependent differences in microbial diversity, opening avenues for future research into the mechanisms driving this variation. Conclusions: In sum, our study emphasizes the need to consider both host-associated and environmental factors in shaping gut microbiota dynamics and highlights the complex interplay between host organisms, their associated microbial communities, and the environment in natural settings. Ultimately, these insights enhance our understanding of host-microbiota interactions and their eco-evolutionary implications.

The vertebrate gut microbiota is a critical determinant of organismal function, yet whether and how gut microbial communities affect host fitness under natural conditions remains largely unclear. We characterised associations between a fitness proxy—individual growth rate—and bacterial gut microbiota diversity and composition in threespine stickleback fish introduced to large semi‐natural ponds. We detected a 63% higher richness of bacterial taxa (α‐diversity) in the guts of high‐fitness fish compared to low‐fitness fish, which might be driven by stronger bacterial dispersal among high‐fitness fish according to the fit of a neutral community model. Further, microbial communities of high‐fitness fish were more similar to one another (i.e., exhibited lower β‐diversity) than those of low‐fitness fish. The lower β‐diversity found to be associated with higher host fitness is consistent with the Anna Karenina principle—that there are fewer ways to have a functional microbiota than a dysfunctional microbiota. Our study links differences in α‐ and β‐diversity to a fitness‐related trait in a vertebrate species reared under naturalistic conditions and our findings provide a basis for functional tests of the fitness consequences of host‐microbiota interactions.

Host–microbiota interactions play a critical role in the hosts’ biology, and thus, it is crucial to elucidate the mechanisms that shape gut microbial communities. We leveraged threespine stickleback fish ( Gasterosteus aculeatus ) as a model system to investigate the contribution of host and environmental factors to gut microbiota variation. These fish offer a unique opportunity for experiments in naturalistic conditions; we reared benthic and limnetic ecotypes from three different lakes in experimental ponds, allowing us to assess the relative effects of shared environment (pond), geographic origin (lake-of-origin), trophic ecology and genetics (ecotype) and biological sex on gut microbiota α- and β-diversity. Host ecotype had the strongest influence on α-diversity, with benthic fish exhibiting higher diversity than limnetic fish, followed by the rearing environment. β-diversity was primarily shaped by rearing environment, followed by host ecotype, indicating that environmental factors play a crucial role in determining gut microbiota composition. Furthermore, numerous bacterial orders were differentially abundant across ponds, underlining the substantial contribution of environmental factors to gut microbiota variation. Our study illustrates the complex interplay between environmental and host ecological or genetic factors in shaping the stickleback gut microbiota and highlights the value of experiments conducted under naturalistic conditions for understanding gut microbiota dynamics.

Selection pressures differ along environmental gradients, and traits tightly linked to fitness (e.g., the visual system) are expected to track such variation. Along gradients, adaptation to local conditions might be due to heritable and nonheritable environmentally induced variation. Disentangling these sources of phenotypic variation requires studying closely related populations in nature and in the laboratory. The Nicaraguan lakes represent an environmental gradient in photic conditions from clear crater lakes to very turbid great lakes. From two old, turbid great lakes, Midas cichlid fish (Amphilophus cf. citrinellus) independently colonized seven isolated crater lakes of varying light conditions, resulting in a small adaptive radiation. We estimated variation in visual sensitivities along this photic gradient by measuring cone opsin gene expression among lake populations. Visual sensitivities observed in all seven derived crater lake populations shifted predictably in direction and magnitude, repeatedly mirroring changes in photic conditions. Comparing wild-caught and laboratory-reared fish revealed that 48% of this phenotypic variation is genetically determined and evolved rapidly. Decreasing intrapopulation variation as environments become spectrally narrower suggests that different selective landscapes operate along the gradient. We conclude that the power to predict phenotypic evolution along gradients depends on both the magnitude of environmental change and the selective landscape shape.

The gut microbiota plays a crucial role in the biological function of their hosts since bacteria provide nutrient processing, protection against pathogens, and modulation of the immune system. Thus, as organisms adapt to different ecological niches, their gut microbial communities are thought to change in response to novel environmental conditions. Quantifying the direction and magnitude of gut microbiota changes associated with ecological niche offers valuable insights into the predictability of gut microbial community change accompanying shifts in host ecology. We used multivariate vector analysis to assess the (non)parallelism of gut microbiota community composition associated with host occupancy of a similar niche. We studied gut microbiota (non)parallelism across an extensive data set of 53 mammalian and 50 avian host species. Our results suggest that parallel shifts in host trophic ecology are associated with greater gut microbiota parallelism, whereas we could not find evidence for a clear effect of host phylogeny. Furthermore, parallelism was generally stronger when estimated from inferred metagenome function compared with gut microbiota taxonomic composition, suggesting that functional redundancy among bacterial lineages might obscure the signature of adaptive gut microbiota changes. Notably, a substantial proportion of the variation in gut microbiota (non)parallelism was not explained by host trophic ecology or phylogeny. Thus, we encourage future microbiota studies to use quantitative analyses along with additional ecological and host-associated data to obtain a comprehensive understanding of the factors shaping the direction and magnitude of gut microbiota changes associated with ecological divergence. IMPORTANCE: What are the roles of determinism and contingency in evolution? The paleontologist and evolutionary biologist Stephen J. Gould raised this question in his famous thought experiment of “replaying life’s tape.” Settings where independent lineages have repeatedly adapted to similar ecological niches (i.e., parallel evolution) are well suited to address this question. Here, we quantified whether repeated ecological shifts across 53 mammalian and 50 avian host species are associated with parallel gut microbiota changes. Our results indicate that parallel shifts in host diet are associated with greater gut microbiota parallelism (i.e., more deterministic). While further research will be necessary to obtain a comprehensive picture of the circumstances under which deterministic gut microbiota changes might be expected, our study can be instrumental in motivating the use of more quantitative methods in microbiota research. This, in turn, can help us better understand microbiota dynamics during adaptive evolution of their hosts.

The gut microbiota is crucial for many aspects of their hosts’ biology, and it has been characterized for many species across the animal kingdom. Yet, we still don’t have a good understanding of whether non-lethal sampling can accurately capture the diversity of gut-associated bacterial communities, as estimated from lethal sampling of intestinal tissue. We further lack knowledge on whether non-lethal sampling methods are suitable for detecting gut microbiota shifts associated with changes in environmental factors (e.g., diet). We addressed these questions in threespine stickleback fish, a model system for evolutionary ecology, by comparing bacterial communities from intestinal tissue and feces. Despite some differences in community composition between the two sample types and considerable temporal variation among fecal samples, bacterial communities appear to largely overlap. Further, we detected consistent and significant changes of fecal bacterial communities associated with an experimental diet manipulation. This suggests that fecal sampling can represent an adequate non-lethal method to characterize the gut microbiota of threespine stickleback, but additional studies will be necessary before drawing general conclusions regarding the validity of fecal sampling for gut microbiota studies. To this end, we give recommendations to improve the characterization of the gut microbiota via fecal sampling. Fecal sampling allows studying temporal gut microbiota shifts associated with environmental change at the individual level, which increases opportunities for future experimental gut microbiota research.