Population bottlenecks constrain microbiome diversity and host genetic variation impeding fitness

Abstract

It is becoming increasingly clear that microbial symbionts influence key aspects of their host’s fitness, and vice versa. This may fundamentally change our thinking about how microbes and hosts interact in influencing fitness and adaptation to changing environments. Here we explore how reductions in population size commonly experienced by threatened species influence microbiome diversity. Fitness consequences of such reductions are normally interpreted in terms of a loss of genetic variation and increase in inbreeding depression due to a loss of heterozygosity. However, fitness effects might also be mediated through microbiome diversity, e.g. if functionally important microbes are lost. Here we utilise Drosophila melanogaster lines with different histories of population bottlenecks to explore these questions. The lines were phenotyped for egg-to-adult viability and their genomes sequenced to estimate genetic variation. The bacterial 16S rRNA gene was amplified in these lines to investigate microbial diversity. We found that 1) host population bottlenecks constrained microbiome richness and diversity, 2) core microbiomes of hosts with low genetic variation were constituted from subsets of microbiomes found in flies with higher genetic variation, 3) both microbiome diversity and host genetic variation contributed to host population fitness, 4) connectivity and robustness of bacterial networks increased with higher host genetic variation, and 5) reduced microbial diversity is associated with weaker evolutionary responses in stressful environments. These findings suggest that population bottlenecks reduce hologenomic variation (in combined host and microbial genomes). Thus while the current biodiversity crisis focuses on population sizes and genetic variation of eukaryotes, an additional focal point should be the microbial diversity carried by the eukaryotes, which in turn may influence host fitness and adaptability with consequences for the persistence of populations.