Asexual lineages often exhibit broad distributions and can thrive in extreme habitats compared to their sexual counterparts. Several hypotheses can be proposed to explain this pattern. Asexual ...lineages could be versatile genotypes with wide environmental tolerance, enabling their dispersal and persistence across large geographic areas. Alternatively, asexual genotypes could be ecological specialists that thrive in specific environments and outcompete relative colonizing distantly related with similar conditions in the process. Several aphid species feature widespread obligate asexual lineages, commonly known as ‘superclones'. Yet it is often unknown whether these clones are widespread ecological generalists or successful specialists. To explore these hypotheses, we examined climatic niche differentiation among six globally distributed obligate asexual lineages of the cosmopolitan aphid pest, Brachycaudus helichrysi. To ensure that we were investigating the aphid genotype niche and not a by‐product of their association with endosymbionts mediating thermal tolerance, we first verified that clones hosted similar endosymbiont communities. Subsequently, we conducted multivariate analyses on clone occurrence data on a worldwide scale. Our results revealed that, despite their global distribution, B. helichrysi superclones occupy different climatic niches. This study represents the first evidence that aphid superclone distribution can be mediated by distinctive ranges of climatic tolerance.
Endosymbiotic bacteria are important drivers of insect evolutionary ecology, acting both as partners that contribute to host adaptation and as subtle parasites that manipulate host reproduction. ...Among them, the genus Arsenophonus is emerging as one of the most widespread lineages. Its biology is, however, entirely unknown in most cases, and it is therefore unclear how infections spread through insect populations. Here we examine the incidence and evolutionary history of Arsenophonus in aphid populations from 86 species, characterizing the processes that shape their diversity. We identify aphids as harbouring an important diversity of Arsenophonus strains. Present in 7% of the sampled species, incidence was especially high in the Aphis genus with more than 31% of the infected species. Phylogenetic investigations revealed that these Arseno‐phonus strains do not cluster within an aphid‐specific clade but rather exhibit distinct evolutionary origins showing that they undergo repeated horizontal transfers (HT) between distantly related host species. Their diversity pattern strongly suggests that ecological interactions, such as plant mediation and parasitism, are major drivers for Arsenophonus dispersal, dictating global incidence across insect communities. Notably, plants hosting aphids may be important ecological arenas for global exchange of Arsenophonus, serving as reservoirs for HT.
It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent ...phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant-insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by > 750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale cophylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on an average, wasps had sequences from 77% of 6 genes (5.6 kb), figs had sequences from 60% of 5 genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based cophylogenetic analyses further support the codiversification hypothesis. Biogeographic analyses indicate that the present-day distribution of fig and pollinator lineages is consistent with a Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant-insect interactions of coordinated dispersal and long-term codiversification.
Ancestral character states computed from the combination of phylogenetic trees with extrinsic traits are used to decipher evolutionary scenarios in various research fields such as phylogeography, ...epidemiology, and ecology. Despite the existence of powerful methods and software in ancestral character state inference, difficulties may arise when interpreting the outputs of such inferences. The growing complexity of data (trees, annotations), the diversity of optimization criteria for computing trees and ancestral character states, the combinatorial explosion of potential evolutionary scenarios if some ancestral characters states do not stand out clearly from others, requires the design of new methods to explore associations of phylogenetic trees with extrinsic traits, to ease the visualization and interpretation of evolutionary scenarios.
We developed PastView, a user-friendly interface that includes numerical and graphical features to help users to import and/or compute ancestral character states from discrete variables and extract ancestral scenarios as sets of successive transitions of character states from the tree root to its leaves. PastView provides summarized views such as transition maps and integrates comparative tools to highlight agreements or discrepancies between methods of ancestral annotations inference.
The main contribution of PastView is to assemble known numerical and graphical methods into a multi-maps graphical user interface dedicated to the computing, searching and viewing of evolutionary scenarios based on phylogenetic trees and ancestral character states. PastView is available publicly as a standalone software on www.pastview.org .
Aphids harbour an obligatory symbiont, Buchnera aphidicola, providing essential amino acids not supplied by their diet. These bacteria are transmitted vertically and phylogenic analyses suggest that ...they have 'cospeciated' with their hosts. We investigated this cospeciation phenomenon at a fine taxonomic level, within the aphid genus Brachycaudus. We used DNA-based methods of species delimitation in both organisms, to avoid biases in the definition of aphid and Buchnera species and to infer association patterns without the presumption of a specific interaction. Our results call into question certain 'taxonomic' species of Brachycaudus and suggest that B. aphidicola has diversified into independently evolving entities, each specific to a 'phylogenetic' Brachycaudus species. We also found that Buchnera and their hosts simultaneously diversified, in parallel. These results validate the use of Buchnera DNA data for inferring the evolutionary history of their host. The Buchnera genome evolves rapidly, making it the perfect tool for resolving ambiguities in aphid taxonomy. This study also highlights the usefulness of species delimitation methods in cospeciation studies involving species difficult to conceptualize-as is the case for bacteria-and in cases in which the taxonomy of the interacting organisms has not been determined independently and species definition depends on host association.
Most metazoans are involved in durable relationships with microbes which can take several forms, from mutualism to parasitism. The advances of NGS technologies and bioinformatics tools have opened ...opportunities to shed light on the diversity of microbial communities and to give some insights into the functions they perform in a broad array of hosts. The pea aphid is a model system for the study of insect-bacteria symbiosis. It is organized in a complex of biotypes, each adapted to specific host plants. It harbors both an obligatory symbiont supplying key nutrients and several facultative symbionts bringing additional functions to the host, such as protection against biotic and abiotic stresses. However, little is known on how the symbiont genomic diversity is structured at different scales: across host biotypes, among individuals of the same biotype, or within individual aphids, which limits our understanding on how these multi-partner symbioses evolve and interact.
We present a framework well adapted to the study of genomic diversity and evolutionary dynamics of the pea aphid holobiont from metagenomic read sets, based on mapping to reference genomes and whole genome variant calling. Our results revealed that the pea aphid microbiota is dominated by a few heritable bacterial symbionts reported in earlier works, with no discovery of new microbial associates. However, we detected a large and heterogeneous genotypic diversity associated with the different symbionts of the pea aphid. Partitioning analysis showed that this fine resolution diversity is distributed across the three considered scales. Phylogenetic analyses highlighted frequent horizontal transfers of facultative symbionts between host lineages, indicative of flexible associations between the pea aphid and its microbiota. However, the evolutionary dynamics of symbiotic associations strongly varied depending on the symbiont, reflecting different histories and possible constraints. In addition, at the intra-host scale, we showed that different symbiont strains may coexist inside the same aphid host.
We present a methodological framework for the detailed analysis of NGS data from microbial communities of moderate complexity and gave major insights into the extent of diversity in pea aphid-symbiont associations and the range of evolutionary trajectories they could take.
Aim: Scenarios of aphid evolution suggest that adaptation to host plants plays a major role in aphid diversification. It is therefore commonly assumed that host association has also shaped the ...biogeographical patterns of aphids; particularly, it has been hypothesized that the intercontinental disjunctions observed in the Holarctic for many aphid groups resulted from the disappearance or migration of their hosts. We explored this hypothesis for the conifer-feeding genus Cinara, one of the most diverse and widely distributed aphid genera in the Holarctic. Location: Holarctic. Methods: Six DNA fragments from 361 specimens representing 92 species were used to reconstruct the phylogeny of Cinara species. We used speciesdelimitation methods to identify putative species, and estimated times of divergence using Bayesian relaxed clocks and fossil calibrations. We investigated rates of diversification, biogeographical and host-association history using maximum likelihood and Bayesian approaches. Results: Cinara originated in Asia c. 50 Ma following a host switch to conifers from an angiosperm-feeding ancestor. The steady diversification observed since then suggests that this host switch did not cause adaptive radiation in Cinara, as previously assumed. Switches between conifer host genera could have facilitated the expansion of Cinara in the Holarctic, but the intercontinental disjunctions observed today are most likely the result of vicariance mediated by climatic or geological barriers. Main conclusions: This study shows that biogeographical and diversification patterns in Cinara have not only been shaped by host-plant adaptation processes, but also by the climatic and geological changes that occurred through the Cenozoic.
Aphids constitute a diverse group of plant-feeding insects and are among the most important crop pests in temperate regions. Their morphological identification is time-consuming and requires specific ...knowledge, training and skills that may take years to acquire. We assessed the advantages and limits of DNA barcoding with the standard COI barcode fragment for the identification of European aphids. We constructed a large reference dataset of barcodes from 1020 specimens belonging to 274 species and 87 genera sampled throughout Europe and set up a database-driven website allowing species identification from query sequences.
In this unbiased sampling of the taxonomic diversity of European aphids, intraspecific divergence ranged from 0.0% to 3.9%, with a mean value of 0.29%, whereas mean congeneric divergence was 6.4%, ranging from 0.0% to 15%. Neighbor-joining analysis generated a tree in which most species clustered in distinct genetic units. Most of the species with undifferentiated or overlapping barcodes belonged to the genus Aphis or, to a lesser extent, the genera Brachycaudus, Dysaphis and Macrosiphum. The taxa involved were always morphologically similar or closely related and belonged to species groups known to present taxonomic difficulties.
These data confirm that COI barcoding is a useful identification tool for aphids. Barcode identification is straightforward and reliable for 80% of species, including some difficult to distinguish on the basis of morphological characters alone. Unsurprisingly, barcodes often failed to distinguish between species from groups for which classical taxonomy has also reached its limits, leading to endless revisions and discussions about species and subspecies definitions. In such cases, the development of an effective procedure for the accurate identification of aphid specimens continues to pose a difficult challenge.
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