Metabolite profiling of the social spider Stegodyphus dumicola along a climate gradient

Animals experience climatic variation in their natural habitats, which may
lead to variation in phenotypic responses among populations through local
adaptation or phenotypic plasticity. In ectotherm arthropods, the
expression of thermoprotective metabolites such as free amino acids,
sugars, and polyols, in response to temperature stress, may facilitate
temperature tolerance by regulating cellular homeostasis. If populations
experience differences in temperatures, individuals may exhibit
population-specific metabolite profiles through differential accumulation
of metabolites that facilitate thermal tolerance. Such thermoprotective
metabolites may originate from the animals themselves or from their
associated microbiome, and hence microbial symbionts may contribute to
shape the thermal niche of their host. The social spider Stegodyphus
dumicola has extremely low genetic diversity, yet it occupies a relatively
broad temperature range occurring across multiple climate zones in
Southern Africa. We investigated whether the metabolome, including
thermoprotective metabolites, differs between populations, and whether
population genetic structure or the spider microbiome may explain
potential differences. To address these questions, we assessed metabolite
profiles, phylogenetic relationships, and microbiomes in three natural
populations along a temperature gradient. The spider microbiomes in three
genetically distinct populations of S. dumicola showed no significant
population-specific pattern, and none of its dominating genera (Borrelia,
Diplorickettsia, and Mycoplasma) are known to facilitate thermal tolerance
in hosts. These results do not support a role of the microbiome in shaping
the thermal niche of S. dumicola. Metabolite profiles of the three spider
populations were significantly different. The variation was driven by
multiple metabolites that can be linked to temperature stress (e.g.
lactate, succinate or xanthine) and thermal tolerance (e.g. polyols,
trehalose, or glycerol): these metabolites had higher relative abundance
in spiders from the hottest geographic region. These distinct metabolite
profiles are consistent with a potential role of the metabolome in
temperature response.