Population bottlenecks constrain host microbiome diversity and 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. Consequences of such reductions are normally interpreted in terms of a loss of genetic variation, increased inbreeding and associated inbreeding depression. However, fitness effects of population bottlenecks might also be mediated through microbiome diversity, such as through loss of functionally important microbes. Here we utilise 50 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 was low in the inbred lines regardless of host genetic variation, 5) reduced microbial diversity was associated with weaker evolutionary responses of hosts in stressful environments, and 6) these effects were unrelated to Wolbachia density. These findings suggest that population bottlenecks reduce hologenomic variation (combined host and microbial genetic variation). 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.

Sustained positive consequences of genetic rescue of fitness and behavioural traits in inbred populations of Drosophila melanogaster

“…While some inbred lines showed severe inbreeding depression (δ >> 0), others performed well and a few even outperformed the outbred control lines (δ < 0) (Figure S3). This is in line with several other studies showing large phenotypic variation across replicate lines with the same expected level of inbreeding (Fowler & Whitlock, 1999; Kristensen et al, 2003; Mikkelsen et al, 2010; Ørsted et al, 2019, 2022; Reed et al, 2002; Whitlock & Fowler, 1996; Wright et al, 2008). This illustrates that stochastic processes, such as the experimental bottlenecks performed in this study, can have population‐specific (or line‐specific) outcomes in terms of the severity of inbreeding depression (Bouzat, 2010; Ørsted et al, 2019).…”

“…To manage the detrimental genetic effects associated with population fragmentation, such as inbreeding and loss of genetic variation (Bijlsma & Loeschcke, 2012; Bouzat, 2010; Frankham et al, 2002; Hedrick & Fredrickson, 2010; Hedrick & Kalinowski, 2000; López‐Cortegano et al, 2019; Ørsted et al, 2019, 2022; Reed, 2004), introducing immigrants from other populations, termed ‘genetic rescue’, is increasingly being considered as a management approach (Hoffmann et al, 2021a, 2021b; Ingvarsson, 2001; Tallmon et al, 2004; Weeks et al, 2011; Whiteley et al, 2015; Willi et al, 2022). Several examples have proven that genetic rescue can restore/increase fitness and reduce the extinction risk of small genetically depauperate natural populations (Bouzat et al, 2009; Hedrick & Fredrickson, 2010; Hoffmann et al, 2021a; Hogg et al, 2006; Madsen et al, 1999; Weeks et al, 2017; Westemeier, 1998).…”

Gut microbiota of ring-tailed lemurs (Lemur catta) vary across natural and captive populations and correlate with environmental microbiota

“…Host genotype is also a well-established mediator of microbial community structure. Reduced genetic diversity, evidenced as founder effects or inbreeding depression, plays a variable role across taxa in shaping the gut microbiome [89][90][91][92] and may contribute to differences between captive and wild populations. Although both neutral heterozygosity and genomic functional diversity decrease over time in captive ring-tailed lemurs [93,94], inbreeding effects can be mitigated through managed breeding programs, resulting in the rapid 'rescue' of genetic diversity [94].…”

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

“…Likewise, the random subsampling of host‐associated microbes that are brought into a new environment by a small number of hosts could lead to reduced microbiome diversity (“microbiome founder effect”). Such an effect has been observed in Drosophila , where a reduction in population size led to a loss of host genetic variation and decreased bacterial microbiome diversity, which together might lead to geographical variability in the adaptive capacity of hosts associated with differences in population size (Orsted et al, 2022). More experimental studies manipulating host population size, in addition to studies in natural settings where host lineages recently colonized new environments (accompanied by a reduction in population size), will be necessary to infer how common “microbiome founder effects” are across diverse host lineages.…”