Search bioRxiv⌕ Search

Biology subjects

Clamens, A.-L.

Publications and source records attributed to Clamens, A.-L..

7 recordsLinked to original sources

Coevolution and synchronized evolutionary rates in aphid dual endosymbiosis

Many insects rely on obligate bacterial endosymbionts for essential nutrients. However, long-term endosymbiosis drives genome erosion, frequently resulting in the acquisition of additional symbionts that complement or replace ancestral partners. In aphids, the primary nutritional symbiont Buchnera aphidicola can be supplemented by a co-obligate symbiont, most commonly Serratia symbiotica. The long-term evolutionary trajectory of this newly acquired symbiont and its impact on Buchnera remain unknown. Here, we assembled host mitochondrial and endosymbiont genomes from thirteen aphid species belonging to a clade in which Serratia has functioned as a co-obligate symbiont for approximately 25 million years. Phylogenomic analyses reveal that Serratia has undergone extensive genome reduction followed by strict codivergence with aphids and Buchnera. Bayesian molecular dating shows that substitution rates in Serratia and Buchnera are tightly correlated and fall within the range previously reported for Buchnera. Genome-wide analyses indicate pervasive purifying selection in both symbionts. Homologous host-provisioning genes retained in both symbionts did not exhibit elevated evolutionary rates. However, unlike other functional categories, their dN/dS values were not correlated between symbionts, suggesting that they no longer evolve under shared selective regimes, consistent with progressive metabolic specialization. Intraspecific patterns of polymorphism and phylogenies mirror macroevolutionary patterns across the clade. Fluorescence in situ hybridization shows that Serratia and Buchnera occupy distinct bacteriocytes, suggesting that similar demographic processes may contribute to their parallel evolution. Our findings demonstrate that, once integrated into an obligate partnership, newly acquired nutritional symbionts can converge on the long-term evolutionary dynamics of ancient obligate symbionts while undergoing functional specialization.

evolutionary biology↗

Asexual lineages of a cosmopolitan pest aphid are associated with different climatic niches

Asexual lineages often exhibit broader distributions and can thrive in extreme habitats compared to their sexual counterparts. Two hypotheses have been proposed to explain this phenomenon. The general-purpose genotype model posits that selection favours a few versatile asexual genotypes with wide environmental tolerance, enabling their long-term persistence across diverse conditions. Conversely, the frozen niche variation model suggests that selection favours specialised genotypes with minimal niche overlap among them and their sexual relatives, potentially leading to competition-driven exclusion of both sexual and asexual relatives. To investigate these hypotheses, we examined ecological niche differentiation among six globally distributed obligate asexual lineages of the cosmopolitan aphid pest, Brachycaudus helichrysi. We initially investigated the presence of different endosymbionts across clones, as endosymbionts play a major role in aphid niche differentiation. Subsequently, we conducted multivariate analyses to explore climatic niche divergence among clones. We provide evidence for climatic niche specialisation in asexual lineages, which is not related to variations in endosymbiont associations. Therefore, despite their apparent global distribution, B. helichrysi clones exhibit characteristics of specialised genotypes, which aligns with the frozen niche variation hypothesis. This study represents the first comprehensive evidence of climatic adaptation in aphid superclones, providing novel insights into their global distribution.

ecology↗

Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages

Aphids are a large family of phloem-sap feeders. They typically rely on a single bacterial endosymbiont, Buchnera aphidicola, to supply them with essential nutrients lacking in their diet. This association with Buchnera was described in model aphid species from the Aphidinae subfamily and has been assumed to be representative of most aphids. However, in two lineages, Buchnera has lost some essential symbiotic functions and is now complemented by additional symbionts. Though these cases break our view of aphids harbouring a single obligate endosymbiont, we know little about the extent, nature, and evolution of these associations across aphid subfamilies. Here, using metagenomics on 25 aphid species from nine subfamilies, re-assembly and re-annotation of 20 aphid symbionts previously sequenced, and 16S rRNA amplicon sequencing on 223 aphid samples (147 species from 12 subfamilies), we show that dual symbioses have evolved anew at least six times. We also show that these secondary co-obligate symbionts have typically evolved from facultative symbiotic taxa. Genome-based metabolic inference confirms interdependencies between Buchnera and its partners for the production of essential nutrients but shows contributions vary across pairs of co-obligate associates. Fluorescent in situ hybridisation microscopy shows a common bacteriocyte localisation of two newly acquired symbionts. Lastly, patterns of Buchnera genome evolution reveal that small losses affecting a few key genes can be the onset of these dual systems, while large gene losses can occur without any co-obligate symbiont acquisition. Hence, the Buchnera-aphid association, often thought of as exclusive, seems more flexible, with a few metabolic losses having recurrently promoted the establishment of a new co-obligate symbiotic partner.

genomics↗

Genomic balancing selection is key to the invasive success of the fall armyworm

A successful biological invasion involves survival in a newly occupied environment. If a population bottleneck occurs during an invasion, the resulting depletion of genetic variants could cause increased inbreeding depression and decreased adaptive potential, which may result in a fitness reduction. How invasive populations survive in the newly occupied environment despite reduced heterozygosity and how, in many cases, they maintain moderate levels of heterozygosity are still contentious issues1. The Fall armyworm (FAW; Lepidoptera: Spodoptera frugiperda), a polyphagous pest, is native to the Western hemisphere. Its invasion in the Old World was first reported from West Africa in early 2016, and in less than four years, it swept sub-Saharan Africa and Asia, finally reaching Australia. We used population genomics approaches to investigate the factors that may explain the invasive success of the FAW. Here we show that genomic balancing selection played a key role in invasive success by restoring heterozygosity before the global invasion. We observe a drastic loss of mitochondrial polymorphism in invasive populations, whereas nuclear heterozygosity exhibits a mild reduction. The population from Benin in West Africa has the lowest length of linkage disequilibrium amongst all invasive and native populations despite its reduced population size. This result indicates that balancing selection increased heterozygosity by facilitating the admixture of invasive populations from distinct origins and that, once heterozygosity was sufficiently high, FAW started spreading globally in the Old World. As comparable heterozygosity levels between invasive and native populations are commonly observed1, we postulate that the restoration of heterozygosity through balancing selection could be widespread among successful cases of biological invasions.

evolutionary biology↗

Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids' di-symbiotic systems

Many insects with a nutrient-restricted diet depend on obligate mutualistic bacteria for the provisioning of essential nutrients lacking from their food source, namely essential amino acids and B vitamins. Most aphids (Hemiptera: Aphididae), whose diet consists of phloem, rely on the bacterial endosymbiont Buchnera for the supply of the aforementioned compounds. However, in some aphid lineages Buchnera have lost the capability of producing these nutrients and thus the symbiotic consortium has accommodated an extra bacterial partner to supplement Buchneras deficiencies. In this work, we explore the di-symbiotic nutritional endosymbiosis of a group of Cinara aphids which has been found to harbour both Buchnera and an Erwinia-related symbiont. Using fluorescence in situ hybridisation, we have located this symbiont to the bacteriome where it inhabits its own bacteriocytes. Through whole-genome sequencing of the endosymbionts of 9 species of Erwinia-associated Cinara aphids, we have found that Ewrinia genomes are highly syntenic and all show significant genome reduction. Additionally, Erwinia symbionts display phylogenetic congruency with Buchnera, suggesting long-term co-divergence. Most significantly, we found that not only is Erwinia capable of complementing Buchneras auxotrophies, but that the genes involved in the biosynthesis of two B vitamins have actually been horizontally acquired from a Sodalis-related bacterium. Finally, this B-vitamin biosynthetic genes have been further transferred to a new Hamiltonella co-obligate symbiont in a specific Cinara lineage, thus displaying a tri-symbiotic system. These results highlight the important role horizontal gene transfer plays in the establishment of new obligate nutritional symbionts.

genomics↗

A Freeloader?: The Highly Eroded Yet Big-Genomed Serratia symbiotica symbiont of Cinara strobi

Genome reduction is pervasive among maternally-inherited bacterial endosymbionts. This genome reduction can eventually lead to serious deterioration of essential metabolic pathways, thus rendering an obligate endosymbiont unable to provide essential nutrients to its host. This loss of essential pathways can lead to either symbiont complementation (sharing of the nutrient production with a novel co-obligate symbiont) or symbiont replacement (complete takeover of nutrient production by the novel symbiont). However, the process by which these two evolutionary events happen remains somewhat enigmatic by the lack of examples of intermediate stages of this process. Cinara aphids (Hemiptera: Aphididae) typically harbour two obligate bacterial symbionts: Buchnera and Serratia symbiotica. However, the latter has been replaced by different bacterial taxa in specific lineages, and thus species within this aphid lineage could provide important clues into the process of symbiont replacement. In the present study, using 16S rRNA high-throughput amplicon sequencing, we determined that the aphid Cinara strobi harbours not two, but three fixed bacterial symbionts: Buchnera aphidicola, a Sodalis sp., and S. symbiotica. Through genome assembly and genome-based metabolic inference, we have found that only the first two symbionts (Buchnera and Sodalis) actually contribute to the hosts supply of essential nutrients while S. symbiotica has become unable to contribute towards this task. We found that S. symbiotica has a rather large and highly eroded genome which codes only for a few proteins and displays extensive pseudogenisation. Thus, we propose an ongoing symbiont replacement within C. strobi, in which a once competent\" S. symbiotica does no longer contribute towards the beneficial association. These results suggest that in dual symbiotic systems, when a substitute co-symbiont is available, genome deterioration can precede genome reduction and a symbiont can be maintained despite the apparent lack of benefit to its host.

genomics↗

Buchnera has changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts

Symbiotic associations with bacteria have facilitated important evolutionary transitions in insects and resulted in long-term obligate interactions. Recent evidence suggests that these associations are not always evolutionarily stable and that symbiont replacement and/or supplementation of an obligate symbiosis by an additional bacterium has occurred during the history of many insect groups. Yet, the factors favoring one symbiont over another in this evolutionary dynamic are not well understood; progress has been hindered by our incomplete understanding of the distribution of symbionts across phylogenetic and ecological contexts. While many aphids are engaged into an obligate symbiosis with a single Gammaproteobacterium, Buchnera aphidicola, in species of the Lachninae subfamily, this relationship has evolved into a \"menage a trois\", in which Buchnera is complemented by a cosymbiont, usually Serratia symbiotica. Using deep sequencing of 16S rRNA bacterial genes from 128 species of Cinara (the most diverse Lachninae genus), we reveal a highly dynamic dual symbiotic system in this aphid lineage. Most species host both Serratia and Buchnera but, in several clades, endosymbionts related to Sodalis, Erwinia or an unnamed member of the Enterobacteriaceae have replaced Serratia. Endosymbiont genome sequences from four aphid species+confirm that these coresident symbionts fulfill essential metabolic functions not ensured by Buchnera. We further demonstrate through comparative phylogenetic analyses that co-symbiont replacement is not associated with the adaptation of aphids to new ecological conditions. We propose that symbiont succession was driven by factors intrinsic to the phenomenon of endosymbiosis, such as rapid genome deterioration or competitive interactions between bacteria with similar metabolic capabilities.

evolutionary biology↗