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Host genetics can shape microbiome composition, but to what extent it does, remains unclear. Like any other complex trait, this important question can be addressed by estimating the heritability (h²) of the microbiome—the proportion of variance in the abundance in each taxon that is attributable to host genetic variation. However, unlike most complex traits, microbiome heritability is typically based on relative abundance data, where taxon-specific abundances are expressed as the proportion of the total microbial abundance in a sample.

We derived an analytical approximation for the heritability that one obtains when using such relative, and not absolute, abundances, based on an underlying quantitative genetic model for absolute abundances. Based on this, we uncovered three problems that can arise when using relative abundances to estimate microbiome heritability: (1) the interdependency between taxa can lead to imprecise heritability estimates. This problem is most apparent for dominant taxa. (2) Large sample size leads to high false discovery rates. With enough statistical power, the result is a strong overestimation of the number of heritable taxa in a community. (3) Microbial co-abundances lead to biased heritability estimates.

We discuss several potential solutions for advancing the field, focusing on technical and statistical developments, and conclude that caution must be taken when interpreting heritability estimates and comparing values across studies.

 

Experimental evolution has a long history of uncovering fundamental insights into evolutionary processes, but has largely neglected one underappreciated component--the microbiome. As eukaryotic hosts evolve, the microbiome may also respond to selection. However, the microbial contribution to host evolution remains poorly understood. Here, we re-analyzed genomic data to characterize the metagenomes from ten Evolve and Resequence (E&R) experiments inDrosophila melanogasterto determine how the microbiome changed in response to host selection.

Bacterial diversity was significantly different in 5/10 studies, primarily in traits associated with metabolism or immunity. Duration of selection did not significantly influence bacterial diversity, highlighting the importance of associations with specific host traits.

Our genomic re-analysis suggests the microbiome often responds to host selection; thus, the microbiome may contribute to the response ofDrosophilain E&R experiments. We outline important considerations for incorporating the microbiome into E&R experiments. The E&R approach may provide critical insights into host-microbiome interactions and fundamental insight into the genomic basis of adaptation.

 

ABSTRACT The timing of life history events has important fitness consequences. Since the 1950s, researchers have combined first principles and data to predict the optimal timing of life history transitions. Recently, a striking mystery has emerged. Such transitions can be shaped by a completely different branch of the tree of life: species in the microbiome. Probing these interactions using testable predictions from evolutionary theory could illuminate whether and how host-microbiome integrated life histories can evolve and be maintained. Beyond advancing fundamental science, this research program could yield important applications. In an age of microbiome engineering, understanding the contexts that lead to microbiota signaling shaping ontogeny could offer novel mechanisms for manipulations to increase yield in agriculture by manipulating plant responses to stressful environments, or to reduce pathogen transmission by affecting vector efficiency. We combine theory and evidence to illuminate the essential questions underlying the existence of mi crobiome- d ependent o ntogenetic t iming (MiDOT) to fuel research on this emerging topic. 

Mothers provide their offspring with symbionts. Maternally transmitted, intracellular symbionts must disperse from mother to offspring with other cytoplasmic elements, like mitochondria. Here, we investigated how the intracellular symbiontWolbachiainteracts with mitochondria during maternal transmission. Mitochondria andWolbachiamay interact antagonistically and compete as each population tries to ensure its own evolutionary success. Alternatively, mitochondria andWolbachiamay cooperate as both benefit from ensuring the fitness of the mother. We characterized the relationship between mitochondria andWolbachiatiters in ovaries ofDrosophila melanogaster. We found that mitochondria andWolbachiatiters are positively correlated in common laboratory genotypes ofD. melanogaster. We attempted to perturb this covariation through the introduction ofWolbachiavariants that colonize at different titers. We also attempted to perturb the covariation through manipulating the female reproductive tract to disrupt maternal transmission. Finally, we also attempted to disrupt the covariation by knocking down gene expression for two loci involved in mitochondrial metabolism:NADHdehydrogenase and a mitochondrial transporter. Overall, we find that mitochondria andWolbachiatiters are commonly positively correlated, but this positive covariation is disrupted at high titers ofWolbachia. Our results suggest that mitochondria andWolbachiahave likely evolved mechanisms to stably coexist, but the competitive dynamics change at highWolbachiatiters. We provide future directions to better understand how their interaction influences the maintenance of the symbiosis.

 

In many ant–plant mutualisms, ants establish colonies in hollow thorns, leaf pouches, or other specialized structures on their host plants, which they then defend from herbivores. Resource heterogeneity could affect the maintenance of these mutualisms if it leads to one or both partners altering their investment in the interaction. Such a phenomenon may be especially pertinent to theAcacia–antmutualism found in East African savannas, where termite mounds have a profound effect on the spatial structuring of resources used by both plants and ants. Here, we examined whether the proximity to termite mounds ofAcacia drepanolobiumtrees is associated with variation in the behavior of one of their ant associates,Crematogaster nigriceps. We found that ant colonies near termite mounds had decreased aggressive responses to simulated herbivory as well as increased off‐tree movement. We hypothesize that these changes are the result of resident ant colonies near termite mounds shifting investment from defense of their host plant to foraging for nearby resources.