Abstract
Symbiosis with vitamin-provisioning microbes is essential for the nutrition of animals with somespecialized feeding habits. While coevolution favors the interdependence between symbiotic partners, their associations are not necessarily stable: Recently acquired symbionts can replace ancestral symbionts. In this study, we demonstrate successful replacement by Francisella-like endosymbionts (-LE), a group of B-vitamin-provisioning endosymbionts, across tick communities driven by horizontal transfers. Using a broad collection of Francisella-LE-infected tick species, we determined the diversity of Francisella-LE haplotypes through a multi-locus strain typing approach and further characterized their phylogenetic relationships and their association with biological traits of their tick hosts. The patterns observed showed that Francisella-LE commonly transfer through similar ecological networks and geographic distributions shared among different tick species and, in certain cases, through preferential shuffling across congeneric tick species. Altogether, these findings reveal the importance of geographic, ecological, and phylogenetic proximity in shaping the replacement pattern in which new nutritional symbioses are initiated.
Highlights
Mutualisms with microbes are at the origin of animal lineages feeding on nutritionally incomplete food resources [1,2,3]
On the basis of 16S rRNA, rpoB, groEL, ftsZ, and gyrB gene sequences, we characterized 24 to 32 distinct alleles depending on the gene, leading to the identification of 38 genetically different Francisella-LE haplotypes in the 29 tick species (Table 1)
We found a significant signal of phylogenetic clustering for certain vertebrates on which ticks feed (Fig. 2) : Francisella-LE haplotypes cluster with tick species feeding on birds (D=0.14, p(D0)=0.39), but not with tick species feeding on mammals (D=0.78, p(D0)=0.10) or on reptiles (D=0.99, p(D0)=0.06)
Summary
Mutualisms with microbes are at the origin of animal lineages feeding on nutritionally incomplete food resources [1,2,3]. Microbes can synthesize essential amino acids and vitamins that animals cannot, and have vital roles in compensating for nutritional deficiencies Through this mechanism, symbiont acquisition enabled the emergence and expansion of many animal lineages, such as aphids, bed bugs, and leeches, which would otherwise not exist [1, 3, 4]. Sap-feeding insects display a complex mosaic of nutritional symbiont combinations, reflecting repeated symbiont acquisitions, replacements, and losses [4] These novel symbioses typically originate either following horizontal transfer from one host species to another or from uptake of novel symbionts from the environment, and primarily depend on the symbiont’s ability to successfully shift hosts across species boundaries [4, 5]. It remains unclear how invasive symbionts are primarily acquired by novel host species
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