Insular holobionts: persistence and seasonal plasticity of the Balearic wall lizard (Podarcis lilfordi) gut microbiota

Abstract

Integrative studies of animals and associated microbial assemblages (i.e., the holobiont) are rapidly changing our perspectives on organismal ecology and evolution. Islands provide ideal natural systems to understand the biogeographic patterns that shape these symbiotic associations, their resilience and plasticity over temporal and spatial scales, and ultimately their role in the host ecological adaptation. Here we used the Balearic wall lizard Podarcis lilfordi to address the diversification of the holobiont in an insular context by dissecting the drivers of the gut microbiota diversity within and across host allopatric populations. By extensive fecal sampling of individually identified lizards from three closed populations/islets in the South of Mallorca (Na Moltona, Na Guardis and En Curt) along two years and two seasons (spring and autumn), we sorted out the effect of islet, year, season, sex and partly life stage on the microbiota composition. We further related microbiota distances to host genetics and trophic ecology. Overall, the three populations showed a remarkable conservation of the major microbial taxonomic profile, while carrying their unique microbial signature at finer level of taxonomic resolution (Amplicon Sequence Variants (ASVs)). Microbiota distances across populations were compatible with both host genetics (as inferred by microsatellites) and trophic niche distances (as inferred by stable isotopes and fecal content). Within populations, a large proportion of ASVs (30-50%) persisted along the four sampling dates. Microbial diversity was driven by life stage and season, with no annual or sex effect. Seasonal changes within islets were mainly associated with fluctuations in the relative abundances of few bacterial taxa (mostly families Lachnospiraceae and Ruminococcaceae), consistently in both sampled years and without any major compositional turnover. These results support a large resilience of the major compositional aspects of the P. lilfordi gut microbiota over the short-term evolutionary divergence of their host allopatric populations (<10,000 years), but also suggest an undergoing process of parallel diversification of the holobiont. The cyclic seasonal fluctuations in gut microbiota composition hint to an important plasticity of these bacterial communities in response to the host annual physiological/metabolic shifts. The importance of these microbial community dynamics in the host ecology and dietary flexibility remains to be investigated.