Abstract
BackgroundMicrobiomes can have profound impacts on host biology and evolution, but to date, remain vastly understudied in spiders despite their unique and diverse predatory adaptations. This study evaluates closely related species of spiders and their host-microbe relationships in the context of phylosymbiosis, an eco-evolutionary pattern where the microbial community profile parallels the phylogeny of closely related host species. Using 16S rRNA gene amplicon sequencing, we characterized the microbiomes of five species with known phylogenetic relationships from the family Theridiidae, including multiple closely related widow spiders (L. hesperus, L. mactans, L. geometricus, S. grossa, and P. tepidariorum).ResultsWe compared whole animal and tissue-specific microbiomes (cephalothorax, fat bodies, venom glands, silk glands, and ovary) in the five species to better understand the relationship between spiders and their microbial symbionts. This showed a strong congruence of the microbiome beta-diversity of the whole spiders, cephalothorax, venom glands, and silk glands when compared to their host phylogeny. Our results support phylosymbiosis in these species and across their specialized tissues. The ovary tissue microbial dendrograms also parallel the widow phylogeny, suggesting vertical transfer of species-specific bacterial symbionts. By cross-validating with RNA sequencing data obtained from the venom glands, silk glands and ovaries of L. hesperus, L. geometricus, S. grossa, and P. tepidariorum we confirmed that several microbial symbionts of interest are viably active in the host.ConclusionTogether these results provide evidence that supports the importance of host-microbe interactions and the significant role microbial communities may play in the evolution and adaptation of their hosts.
Highlights
Microbiomes can have profound impacts on host biology and evolution, but to date, remain vastly understudied in spiders despite their unique and diverse predatory adaptations
Host, and tissue specificity of spider microbiota The microbiome of each spider species included in this study (5 species in family Theridiidae) was evaluated from whole spider samples (3 per each species, 15 whole samples) and at a tissue-specific level (3 animal/ tissue sets per species, 5 tissues per set – cephalothorax, venom glands, ovary, silk glands, and fat tissue, 75 tissue samples)
We found evidence that several of the microbial community members observed in P. tepidariorum, S. grossa, L. geometricus and L. hesperus are possibly metabolically active, as transcripts for these symbionts were found in corresponding RNA sequencing datasets (RNA-Seq data was unavailable for L. mactans)
Summary
Microbiomes can have profound impacts on host biology and evolution, but to date, remain vastly understudied in spiders despite their unique and diverse predatory adaptations. This study evaluates closely related species of spiders and their host-microbe relationships in the context of phylosymbiosis, an eco-evolutionary pattern where the microbial community profile parallels the phylogeny of closely related host species. Microbial communities within and across three closely related and environmentally controlled Nasonia species exhibit a phylogenetically distinct pattern that mirrors their hosts’ phylogeny [4]. This evolutionary hostmicrobe relationship provides strong evidence, along with other similar studies, to support a recently proposed hypothesis known as phylosymbiosis [7, 8]. Deer mice inoculated with microbial communities from more distantly related species had lower food digestibility and jewel wasps that received transplants of interspecific microbiota had reduced survival compared to those exposed to their own intraspecific microbiota [8]
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