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Rennison, D. J.

Publications and source records attributed to Rennison, D. J..

7 recordsLinked to original sources

Consistent, scale-dependent differences in the biogeography of host-associated and free-living microbiomes across systems

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.

ecology↗

Host traits and environmental variation shape gut microbiota diversity in wild threespine stickleback

BackgroundDespite 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. ResultsOur 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. ConclusionsIn 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.

ecology↗

A positive association between gut microbiota diversity and vertebrate host performance in a field experiment

The vertebrate gut microbiota is a critical determinant of organismal function, yet it remains unclear if and how gut microbial communities affect host fitness under natural conditions. Here, we investigate associations between growth rate (a fitness proxy) and gut microbiota diversity and composition in a field experiment with threespine stickleback fish (Gasterosteus aculeatus). We detected on average 63% more bacterial taxa in the guts of high-fitness fish compared to low-fitness fish (i.e., higher -diversity), suggesting that higher diversity promotes host growth. The microbial communities of high-fitness fish had higher similarity (i.e., lower {beta}-diversity) than low-fitness fish, supporting the Anna Karenina principle-- that there are fewer ways to have a functional microbiota than a dysfunctional microbiota. Our findings provide a basis for functional tests of the fitness consequences of host-microbiota interactions. Significance statementThe vertebrate gut microbiota is important for many aspects of their hosts biology--such as nutrient metabolism and defense against pathogens--that could ultimately affect host fitness. However, studies investigating the effects of gut microbiota composition on vertebrate host fitness under natural conditions remain exceedingly rare. We tested for associations between gut microbiota diversity and growth rate (a fitness proxy) in threespine stickleback fish reared in large outdoor ponds. We found evidence that a more diverse gut microbiota was predictive of higher growth rate and therefore increased host fitness. Notably, high-fitness fish had higher gut microbiota similarity to one another than did low-fitness fish, providing experimental evidence for the Anna Karenina principle--that there are fewer ways to have a functional microbiota than a dysfunctional microbiota--as it relates to host fitness.

evolutionary biology↗

Validity of fecal sampling for characterizing temporal variation in threespine stickleback's gut microbiota

Diverse microbial communities associated with the guts of their hosts are crucial for many aspects of their hosts physiology, ecology, and evolution. The gut microbiota has been characterized for a broad range of species across the animal kingdom. Yet, for many host species we still dont have a good understanding of whether non-lethal sampling (e.g., fecal matter) can accurately capture the diversity of gut-associated bacterial communities, as estimated from lethal sampling of intestinal tissue. We further lack knowledge on whether such non-lethal sampling methods are suitable for studying temporal gut microbiota dynamics. Here, we addressed these questions in threespine stickleback fish, a model system in evolutionary ecology, by comparing bacterial communities based on 16S rRNA gene sequencing from intestinal tissue and feces. Despite some differences in community composition between the two sample types, we show that bacterial communities of feces and intestinal tissue largely overlap. Further, we were able to detect consistent and significant changes of fecal bacterial communities associated with an experimental diet shift. These results suggest that fecal sampling represents an adequate non-lethal method to characterize the gut microbiota of threespine stickleback. This allows for studying temporal gut microbiota dynamics at the individual level, which increases opportunities for future experimental gut microbiota research.

evolutionary biology↗

Quantifying (non)parallelism of gut microbial community change using multivariate vector analysis

Parallel evolution of phenotypic traits is regarded as strong evidence for natural selection and has been studied extensively in a variety of taxa. However, we have limited knowledge of whether parallel evolution of host organisms is accompanied by parallel changes of their associated microbial communities (i.e., microbiotas), which are crucial for their hosts ecology and evolution. Determining the extent of microbiota parallelism in nature can improve our ability to identify the factors that are associated with (putatively adaptive) shifts in microbial communities. While it has been emphasized that (non)parallel evolution is better considered as a quantitative continuum rather than a binary phenomenon, quantitative approaches have rarely been used to study microbiota parallelism. We advocate using multivariate vector analysis (i.e., phenotypic change vector analysis) to quantify direction and magnitude of microbiota changes and discuss the applicability of this approach for studying parallelism. We exemplify its use by reanalyzing gut microbiota data from multiple fish species that exhibit parallel shifts in trophic ecology. This approach provides an analytical framework for quantitative comparisons across host lineages, thereby providing the potential to advance our capacity to predict microbiota changes. Hence, we emphasize that the development and application of quantitative measures, such as multivariate vector analysis, should be further explored in microbiota research in order to better understand the role of microbiota dynamics during their hosts adaptive evolution, particularly in settings of parallel evolution.

evolutionary biology↗

Genetic evidence for environment-dependent hybrid incompatibilities in threespine stickleback

Hybrid incompatibilities occur when interactions between opposite-ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are intrinsic, meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis are scarce. In this article, we compiled genetic data for F2 hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatus L.) that were born and raised in either the field (semi-natural experimental ponds) or the laboratory (aquaria). We tested for differences in excess heterozygosity between these two environments at ancestry informative loci--a genetic signature of selection against incompatibilities. We found that excess ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Previous results from F1 hybrids in the field suggest that pond-specific (single-locus) heterosis is unlikely to explain this finding. Our study suggests that, in stickleback, a coarse signal of environment-dependent hybrid incompatibilities is reliably detectable and that extrinsic incompatibilities have evolved before intrinsic incompatibilities.

evolutionary biology↗

Parallel shifts of visual sensitivity and body colouration in replicate populations of extremophile fish.

Visual sensitivity and body pigmentation are often shaped by both natural selection from the environment and sexual selection from mate choice. One way of quantifying the impact of the environment is by measuring how traits have changed after colonization of a novel habitat. To do this, we studied Poecilia mexicana populations that have repeatedly adapted to extreme sulphidic (H2S containing) environments. We measured visual sensitivity using opsin gene expression, as well as body pigmentation and water transmission for populations in four independent drainages. Both visual sensitivity and body pigmentation showed significant parallel shifts towards greater medium wavelength sensitivity and reflectance in sulphidic populations. The light spectrum was only subtly different between environments and overall, we found no significant correlations between the light environment and visual sensitivity or body pigmentation. Altogether we found that sulphidic habitats select for differences in visual sensitivity and pigmentation; our data suggest that this effect is unlikely to be driven purely by the waters spectral properties and may instead be from other correlated ecological changes.

evolutionary biology↗