Biology subjects

Henry, L. M.

Publications and source records attributed to Henry, L. M..

7 recordsLinked to original sources

bioRxiv2025

Phenotypic divergence is driven by mobile genetic elements in a heritable insect symbiont

AO_SCPLOWBSTRACTC_SCPLOWHeritable microbes profoundly influence insect biology, yet the traits they confer often evolve rapidly and differ among closely related symbiont strains. Despite their importance, we lack a clear understanding of how novel traits arise in symbiosis and how this diversity influences host ecology in natural populations. The aphid facultative symbiont Regiella insecticola is ideally suited to this question because of its strong lineage-specific variation in host benefits. By generating 20 high-quality genomes, we found that Regiellas evolution is driven largely by gene gains mediated by mobile genetic elements. We identified a plasmid (pRILSR1) that encodes a type IV secretion system and a highly expressed predicted effector that has been convergently acquired by Regiella strains from pea aphids. Notably, only pRILSR1-bearing strains confer protection against the specialist fungal pathogen Pandora neoaphidis, indicating that gains and losses of the plasmid underlie the evolution of this key defensive phenotype. Using a multi-year field study, we further show that the pRILSR1 plasmid is strongly associated with Regiella found in pea aphid populations adapted to specific host plants, driving variation in symbiont-mediated defense across populations. Together, our results show that mobile genetic elements generate key adaptive traits in microbial symbionts and, in doing so, drive phenotypic divergence among host populations.

evolutionary biology↗

bioRxiv2025

Phage toxin variants are linked to protection specificity in a defensive symbiont

Insects often depend on symbiotic bacteria for protection, yet the mechanisms by which these microbes target specific natural enemies remain poorly understood. In aphids, different strains of the facultative symbiont Hamiltonella defensa provide highly specific protection against particular species of parasitoid wasps. To uncover the genetic basis of this specificity, we analyzed 26 Hamiltonella genomes and their toxin-encoding APSE bacteriophages with distinct protective phenotypes. Our analyses revealed that Hamiltonella strains share a conserved core genome but differ significantly in accessory gene content, reflecting their distinct evolutionary origins. Strikingly, we show that variation in toxin types is the key distinguishing feature of APSE phages in Hamiltonella strains that protect against different parasitoid species. These toxin repertoires include several novel candidates, such as variants with MAC/perforin domains and leucine-rich repeat (LRR) proteins previously unreported in insect defensive symbionts. We also reveal cases of multiple co-integrated APSE phages carrying different toxins within a single genomic locus. These findings implicate phage-borne toxins as primary determinants of enemy-specific defense and point to phage-driven toxin diversification as a major force shaping the functional evolution of this symbiosis. This work highlights how mobile genetic elements influence the ecological roles and diversification of protective symbionts.

evolutionary biology↗

bioRxiv2023

Evidence of phylosymbiosis in Formica ants

Insects share intimate relationships with microbes that play important roles in their biology. Yet our understanding of how host-bound microbial communities assemble and perpetuate over evolutionary time is limited. Ants host a wide range of microbes with diverse functions and are an emerging model for studying the evolution of insect microbiomes. Here, we ask whether phylogenetically related ant species have formed distinct and stable microbiomes. To answer this question, we investigated the microbial communities associated with queens of 14 Formica species from five clades, using deep coverage 16S rRNA amplicon sequencing. We reveal that Formica species and clades harbour highly defined microbial communities that are dominated by four bacteria genera: Wolbachia, Lactobacillus, Liliensternia, and Spiroplasma. Our analysis reveals that the composition of Formica microbiomes mirrors the phylogeny of the host, i.e. phylosymbiosis, in that related hosts harbour more similar microbial communities. Our analysis also revealed significant correlations between microbe co-occurrences, which suggests that synergistic and antagonistic interactions may contribute to the phylosymbiotic signal. Additional factors potentially contributing to the phylosymbiotic signal are discussed, including host phylogenetic relatedness, host-microbe genetic compatibility, modes of transmission, and similarities in host ecologies (e.g., diets). Overall, our results support the growing body of evidence that microbial community composition closely depends on the phylogeny of their hosts, despite bacteria having diverse modes of transmission and localisation within the host.

evolutionary biology↗

bioRxiv2022

Variation in density, immune gene suppression, and co-infection outcomes among strains of the aphid endosymbiont Regiella insecticola

AO_SCPLOWBSTRACTC_SCPLOWMany insects harbor heritable beneficial microbes that influence host phenotypes. Across systems, divergent symbiont strains have been shown to establish at different densities within hosts. This genetic variation is important evolutionarily because within-host density has been linked to the costs and benefits of the symbiosis for both partners. Studying the factors shaping within-host density is therefore important to our broader understanding of host-microbe coevolution. Here we focused on different strains of Regiella insecticola, a facultative symbiont of aphids. We first demonstrated that different strains of Regiella consistently establish in pea aphids at drastically different densities. We then found that variation in density is correlated with the expression levels of two key insect immune system genes (phenoloxidase and hemocytin), with immune gene suppression correlating with higher Regiella density. We then performed an experiment where we established co-infections of a higher- and lower-density Regiella strain, and we showed that the higher-density strain is better able to persist in co-infections than the lower-density strain. Together, our results point to a potential mechanism for strain-level variation in symbiont density in this system, and further suggest that symbiont fitness may be increased by establishing at higher density within hosts. Our work highlights the importance of within-host dynamics shaping symbiont evolution.

evolutionary biology↗

bioRxiv2022

The hologenome of Osedax frankpressi reveals the genetic interplay for the symbiotic digestion of vertebrate bone

The marine annelid Osedax has evolved a unique heterotrophic symbiosis that allows it to feed exclusively on sunken bones. Yet, the genetic and physiological principles sustaining this symbiosis are poorly understood. Here we show that Osedax frankpressi has a small, AT-rich genome shaped by extensive gene loss. While the Oceanospirillales endosymbiont of Osedax is enriched in genes for carbohydrate and nitrogen metabolism, O. frankpressi has undergone genetic changes to accommodate bone digestion, including the expansion of matrix metalloproteases, and a loss of pathways to synthesize amino acids that are abundant in collagen. Unlike other symbioses, however, innate immunity genes required to acquire and control the endosymbionts are reduced in O. frankpressi. These findings reveal Osedax has evolved an alternative genomic toolkit to bacterial symbiosis where host-symbiont co-dependence has favoured genome simplicity in the host to exploit the nutritionally unbalanced diet of bones. TeaserGenome reduction and adaptations for collagen digestion underpin the symbiosis of Osedax worms to exploit decaying bones.

genomics↗

bioRxiv2022

Local adaptation to hosts and parasitoids shape Hamiltonella defensa genotypes across aphid species

Facultative symbionts are common in insects and are known to provide important adaptations that can drive rapid host evolution. Yet we still have a limited understanding of what shapes their distributions, such as why particular symbiont strains are common in some host species yet absent in other. To address this question, we genotyped the defensive symbiont Hamiltonella defensa in 26 aphid species that commonly carry this microbe. We found that Hamiltonella strains were strongly associated with specific aphid species and that strains found in one host species rarely occurred in others. To explain these associations, we reciprocally transferred the Hamiltonella strains of 3 aphid species, Acyrthosiphon pisum, Macrosiphoniella artemisiae and Macrosiphum euphorbiae, in the other host species, and assessed the impact of Hamiltonella strain on: the stability of the symbiosis, aphid fecundity, and parasitoid resistance. We demonstrate that the Hamiltonella associations found in nature are locally adapted both to the aphid host itself, and its ecology, in that aphids tend to carry Hamiltonella strains that provide strong protection against their dominant parasitoid species. Our results suggest that Hamiltonella strains function as a horizontal gene pool that aphids draw from to rapidly adapt to pressures from different natural enemies.

evolutionary biology↗

bioRxiv2020

Parallel evolution in the integration of a co-obligate aphid symbiosis

Insects evolve dependencies - often extreme - on microbes for nutrition. These include cases where insects harbour multiple endosymbionts that function collectively as a metabolic unit. How do these metabolic co-dependencies originate, and is there a predictable sequence of events leading to the integration of new symbionts? While dependency on multiple nutrient-provisioning symbionts has evolved numerous times across sap-feeding insects, there is only one known case of metabolic co-dependency in aphids, between Buchnera aphidicola and Serratia symbiotica in the Lachninae subfamily. Here we identify three additional independent transitions to the same co-obligate symbiosis in different aphids. A comparison of recent and ancient associations allows us to investigate intermediate stages of metabolic and physical integration between the typically facultative symbiont, Serratia, and the ancient obligate symbiont Buchnera. We find that these uniquely replicated evolutionary events support the idea that co-obligate associations initiate in a predictable manner, through parallel evolutionary processes. Specifically, we show (i) how the repeated losses of the riboflavin pathway in Buchnera leads to dependency on Serratia, (ii) evidence of a stepwise process of symbiont integration, whereby dependency evolves first, then essential amino acid pathways are lost (at ~30-60MYA), which coincides with increased physical integration of the companion symbiont; and (iii) dependency can evolve prior to specialised structures (e.g. bacteriocytes), and in one case with no direct nutritional basis. More generally, our results suggest the energetic costs of synthesising nutrients may provide a unified explanation for the sequence of gene loses that occur during the evolution of co-obligate symbiosis.

evolutionary biology↗