Biology subjects

Pons, I.

Publications and source records attributed to Pons, I..

5 recordsLinked to original sources

bioRxiv2025

Fidelity in co-diversified symbiosis

Obligate co-dependence can arise in symbiosis, yielding heritable partnerships. These interactions are considered to be highly specific, but partner fidelity is difficult to quantify owing to the experimental constraints of symbiont exchange between host species. Here, we overcome this challenge by leveraging the unique transmission dynamics of Stammera capleta, the obligate digestive symbiont of tortoise beetles (Chrysomelidae: Cassidinae). Despite its extracellular localization, S. capleta possesses a drastically reduced genome ([~]0.25 Mb) and is vertically transmitted through egg-associated spheres. Manipulating these spheres allowed us to experimentally exchange S. capleta between beetle species to determine their impact on host development. We show that non-native S. capleta can successfully colonize the symbiotic organs of a novel host, but that the interaction outcome correlates with genetic relatedness to the native symbiont. Genetically distant species trigger a more pronounced transcriptional response and can only partially rescue host development. While more closely related symbionts proliferate similarly to the native one and induce a comparable host response, they fail to propagate to the next generation, underscoring how transmission fidelity, host-symbiont compatibility, and local adaptation can further specificity within a Paleocene-aged partnership.

evolutionary biology↗

bioRxiv2023

Paleocene origin of a streamlined digestive symbiosis in leaf beetles

Timing the acquisition of a beneficial microbe relative to the evolutionary history of its host can shed light on the adaptive impact of a partnership. Here, we investigated the onset and molecular evolution of an obligate symbiosis between Cassidinae leaf beetles and Candidatus Stammera capleta, a {gamma}-proteobacterium. Residing extracellularly within foregut symbiotic organs, Stammera upgrades the digestive physiology of its host by supplementing plant cell wall-degrading enzymes. We observe that Stammera is a shared symbiont across tortoise and hispine beetles that collectively comprise the Cassidinae subfamily, despite differences in their folivorous habits. In contrast to its transcriptional profile during vertical transmission, Stammera elevates the expression of genes encoding digestive enzymes while in the foregut symbiotic organs, matching the nutritional requirements of its host. Symbiont acquisition during the Paleocene ([~]62 Mya) did not coincide with the origin of Cassidinae beetles, despite the widespread distribution of Stammera across the subfamily. Early-diverging lineages lack the symbiont and the specialized organs that house it. Reconstructing the ancestral state of host-beneficial factors revealed that Stammera encoded three digestive enzymes at the onset of symbiosis, including polygalacturonase - a pectinase that is universally shared. While non-symbiotic cassidines encode polygalacturonase endogenously, their repertoire of plant cell wall-degrading enzymes is more limited compared to symbiotic beetles supplemented with digestive enzymes from Stammera. Highlighting the potential impact of a symbiotic condition and an upgraded metabolic potential, Stammera-harboring beetles exploit a greater variety of plants and are more speciose compared to non-symbiotic members of the Cassidinae.

evolutionary biology↗

bioRxiv2023

Extracellular symbiont colonizes insect during embryo development

Insects typically acquire their beneficial microbes early in development. Endosymbionts housed intracellularly are commonly integrated during oogenesis or embryogenesis, whereas extracellular microbes are only known to be acquired after hatching by immature instars such as larvae or nymphs. Here, however, we report on an extracellular symbiont that colonises its host during embryo development. Tortoise leaf beetles (Chrysomelidae: Cassidinae) host their digestive bacterial symbiont Stammera extracellularly within foregut symbiotic organs, and in ovary-associated glands to ensure its vertical transmission. We outline the initial stages of symbiont colonization and observe that while the foregut symbiotic organs develop three days prior to larval emergence, they remain empty until the final 24 hours of embryo development. Infection by Stammera occurs during that timeframe, and prior to hatching. By experimentally manipulating symbiont availability to embryos in the egg, we describe a 12-hour developmental window governing colonization by Stammera. Symbiotic organs form normally in aposymbiotic larvae, demonstrating that these Stammera-bearing structures develop autonomously. In adults, the foregut symbiotic organs are already colonized following metamorphosis and host a stable Stammera population to facilitate folivory. The ovary-associated glands, however, initially lack Stammera. Symbiont abundance subsequently increases within these transmission organs, thereby ensuring sufficient titers at the onset of oviposition [~]29 days following metamorphosis. Collectively, our findings reveal that Stammera colonization precedes larval emergence, where its proliferation is eventually decoupled in adult beetles to match the nutritional and reproductive requirements of its host.

evolutionary biology↗

bioRxiv2021

Ubiquity of the Symbiont Serratia symbiotica in the Aphid Natural Environment: Distribution, Diversity and Evolution at a Multitrophic Level

Bacterial symbioses are significant drivers of insect evolutionary ecology. However, despite recent findings that these associations can emerge from environmentally derived bacterial precursors, there is still little information on how these potential progenitors of insect symbionts circulates in the trophic systems. The aphid symbiont Serratia symbiotica represents a valuable model for deciphering evolutionary scenarios of bacterial acquisition by insects, as its diversity includes intracellular host-dependent strains as well as gut-associated strains that have retained some ability to live independently of their hosts and circulate in plant phloem sap. These strains represent a potential reservoir for the emergence of new and more intimate symbioses. Here, we conducted a field study to examine the distribution and diversity of S. symbiotica found in aphid populations, as well as in different compartments of their surrounding environment. A total of 250 aphid colonies, 203 associated insects, and 161 plant samples associated with aphid colonies were screened for S. symbiotica. Twenty percent of aphids were infected with S. symbiotica, and the symbiont includes a wide diversity of strains with varied tissue tropism corresponding to different lifestyle. We also showed that the prevalence of S. symbiotica is influenced by seasonal temperatures. For the first time, we found that S. symbiotica was present in non aphid species and in host plants, and that the prevalence of the bacterium in these samples was higher when associated aphid colonies were infected. Furthermore, phylogenetic analyses suggest the existence of horizontal transfers between the different trophic levels examined. These results provide a completely new picture of the ubiquity of an insect symbiont in nature. They suggest that ecological interactions promote the dissemination of strains that are still free-living and poorly specialized, and for which plants are a proabable reservoir for the acquisition of new bacterial partners in insects.

evolutionary biology↗

bioRxiv2018

New Insights into the Nature of Symbiotic Associations in Aphids: Initial Steps Involved in Aphid Gut Infection by Serratia symbiotica Bacteria

Symbiotic microorganisms are widespread in nature and can play a major role in the ecology and evolution of animals. The aphid-Serratia symbiotica bacterium interaction provides a valuable model to study mechanisms behind these symbiotic associations. The recent discovery of cultivable S. symbiotica strains having the possibility of free-living lifestyle allowed us to simulate their environmental acquisition by aphids to examine the mechanisms involved in this infection pathway. Here, after oral ingestion, we analyzed the infection dynamic of cultivable S. symbiotica strains during the hosts lifetime using qPCR and fluorescence techniques and determined the immediate fitness consequences of these bacteria on their new host. We further examined the transmission behavior and phylogenetic position of cultivable strains. Usually, S. symbiotica are considered as maternally-transmitted bacteria living within aphid body cavity and bringing some benefits to their hosts despite their costs. Otherwise, our study revealed that cultivable S. symbiotica are predisposed to establish a symbiotic association with new aphid host, settling in its gut. We showed that cultivable S. symbiotica colonized the entire aphid digestive tract following infection, after which the bacterium multiplied exponentially during aphid development. Our results further revealed that gut colonization by the bacteria induce a fitness cost to their hosts. Nevertheless, it appeared that they also offer an immediate protection against parasitoids. Interestingly, cultivable S. symbiotica seem to be extracellularly transmitted, possibly through the honeydew. These findings provide new insights into the nature of symbiosis in aphids and the mechanisms underpinning these interactions.\n\nImportanceFor the first time, our study provides experimental data that highlight a new kind of symbiotic associations in aphids. By successfully isolating microbial symbiont from aphids and by cultivating it in vitro in our laboratory, we established artificial association by simulating new bacterial acquisitions involved in aphid gut infection. Our results showed the early stages involved in this route of infection. Until now, Serratia symbiotica is considered as a maternally-transmitted aphid endosymbiont. Nevertheless, here, we showed that our cultivable strains having an intermediate status between a strict free-living bacterium and a facultative endosymbiont, occupy and replicate in aphid gut and seem to be transmitted over generations through an environmental transmission mechanism. Moreover, they are both parasites and mutualists given the context, as many of the endosymbionts in aphids. Our findings give new perception of associations involved in aphids symbiosis.

evolutionary biology↗