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Moreau, C. S.

Publications and source records attributed to Moreau, C. S..

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Multiple Shifts from Peptide-Based to Metabolite-Based Venoms in Ants

Venom systems are key evolutionary innovations that have contributed to the ecological success of numerous animal lineages. In ants (Formicidae), venom exhibits an exceptional diversity in both chemical composition and delivery mechanisms. Here, we combine a synthesis of current knowledge on the evolution of ant venoms with new phylogenetic comparative analyses, integrating chemical, morphological, and phylogenetic data at the genus level. Comparative analyses across Formicidae support the hypothesis that peptide-rich venoms represent the ancestral condition in ants, as they are widely distributed across basal and derived lineages. Despite this ancestral state, we identify seven independent evolutionary transitions toward non-peptidic venom, occurring in major clades including Dolichoderinae, Formicinae, Stenammini, Solenopsidini, Crematogaster, Pheidole, and fungus-growing ants. Ancestral state reconstruction and tests of correlated evolution across 114 genera show that these seven shifts away from peptide-based venom were almost irreversible and tightly coupled with the loss of stinging capacity and a dietary shift away from predation. These transitions are consistently associated with profound morphological modifications of the venom apparatus, such as reduction or complete loss of the sting, or its transformation into non-injecting structures. Chemically, these systems are dominated by alkaloids, iridoids, formic acid, esters, and terpenoids. These repeated transitions reflect major ecological and evolutionary shifts. Lineages that rely less on individual predation and more on collective foraging or plant-based diets tend to exhibit reduced reliance on injectable peptide toxins. Instead, they favor metabolite-based venoms that can be co-opted from existing biochemical pathways and deployed in diverse ecological contexts. Conversely, peptide-rich venoms are retained in lineages subjected to strong selective pressures for rapid prey immobilization or defense against vertebrate predators. Overall, ants represent a unique model for understanding venom evolution, illustrating how shifts in chemistry, morphology, and ecological strategy can drive repeated and convergent innovations. Future integrative studies combining genomics, metabolomics, and functional assays will be essential to unravel the mechanisms underlying these transitions and their role in the extraordinary diversification of ants.

evolutionary biology↗

UCE phylogenomics inform the systematics and geographic range evolution of the harvester ant genus Pogonomyrmex

The harvester ant genus Pogonomyrmex is common in arid regions of North America, South America, and Hispaniola. Here, we use ultraconserved elements (UCEs) to infer the most comprehensive phylogeny of the genus to date. Our inferred topology largely supports previously hypothesized Pogonomyrmex evolutionary relationships and species groups. Our divergence dating analysis substantially pushes back the age of both Pogonomyrmex and the Pogonomyrmecini tribe, suggesting an early Eocene origin for Pogonomyrmex. We infer that Pogonomyrmex likely originated within the Pacific dominion ecoregion of Northern South America. Pogonomyrmex (excluding the Pogonomyrmex mayri clade) likely adapted to cooler and drier climates in the middle Eocene. The genus spread to North America in the late Eocene, likely aided by the ephemeral volcanic islands of the Panama Arc. A smaller group of Pogonomyrmex dispersed to Mesoamerica and North America in the Oligocene and to Hispaniola in the Miocene, most likely out of Mesoamerica. Our results suggest that adaptations to arid environments allowed Pogonomyrmex to spread and diversify in regions of the Americas that were actively becoming cooler and drier due to orogeny and other geologic processes.

zoology↗

Evaluating UCE data adequacy and integrating uncertainty in a comprehensive phylogeny of ants

While some relationships in phylogenomic studies have remained stable since the era of Sanger sequencing, many challenging nodes elude resolution, even with genome-scale data. As early studies grappled with random error and insufficient information, incongruence or lack of resolution in phylogenomics is generally associated with inadequate modeling of biological phenomena combined with analytical issues leading to systematic biases. Few phylogenomic studies, however, explore the potential for random error or establish an expectation of what level of resolution should be expected from a given empirical dataset. In presenting incongruent results, phylogeneticists face a choice of providing a diverse array of results from different approaches or a single preferred tree, with few attempting to integrate uncertainties across methods. Recent phylogenetic work has uncovered many well-supported and often novel relationships, as well as more contentious findings, across the phylogeny of ants. Ants are the most species-rich lineage of social insects and among the most ecologically important terrestrial animals. As a result, they have attracted much research, including regarding systematics. To date, however, there has been no comprehensive genus-level phylogeny of the ants inferred using genomic data combined with an effort to evaluate signal and incongruence throughout. Here we provide deeper insight into and quantify uncertainty across the ant tree of life. We accomplish this with the most taxonomically comprehensive Ultraconserved Elements dataset to date, including 277 (81%) of recognized ant genera from all 16 extant subfamilies, representing over 98% of described species-level diversity. We use simulations to establish expectations for resolution, identify branches with less-than-expected concordance, and dissect the effects of data and model selection on recalcitrant nodes. We also construct a consensus tree integrating uncertainty from multiple analyses. Simulations show that hundreds of loci are needed to resolve recalcitrant nodes on our genus-level ant phylogeny, even under a best-case scenario of known model parameters and without systematic bias. This demonstrates that random error continues to play a role in phylogenomics. Our analyses provide a comprehensive picture of support and incongruence across the ant phylogeny, and our consensus topology is congruent with a recent phylogenomic study on the subfamily-level, while rendering a more realistic picture of uncertainty and significantly expanding generic sampling. We use this topology for divergence dating and find that assumptions about root age have significant impact on the dates inferred. Our results suggest that improved understanding of ant phylogeny will require both more data and better phylogenetic models. We also provide a workflow to identify under-supported nodes in concatenation analyses, outline a pragmatic way to reconcile conflicting results in phylogenomics, and introduce a user-friendly locus selection tool for divergence dating.

evolutionary biology↗

Adaptive trade-offs between vertebrate defense and insect predation drive ant venom evolution

Stinging ants have diversified into various ecological niches, and several evolutionary drivers may have contributed to shape the composition of their venom. To comprehend the drivers underlying venom variation in ants, we selected 15 Neotropical species and recorded a range of traits, including ecology, morphology, and venom bioactivity. Principal component analysis of both morphological and venom bioactivity traits revealed that stinging ants display two functional strategies. Additionally, phylogenetic comparative analysis indicated that venom function (predatory, defensive, or both) and mandible morphology significantly correlate with venom bioactivity and amount, while pain-inducing activity trades off with insect paralysis. Further analysis of the venom biochemistry of the 15 species revealed switches between cytotoxic and neurotoxic venom compositions in some species. This study highlights the fact that ant venoms are not homogenous, and for some species, there are major shifts in venom composition associated with the diversification of venom ecological functions. SignificanceVenoms are under severe evolutionary pressures, exerted either on the innovation of toxins or the reduction of the metabolic cost of production (1). To reduce the metabolic costs associated with venom secretion, some venomous animals can regulate venom expenditure by metering the amount of venom injected and by switching between offensive and defensive compositions (2-2). Many ants use venom for subduing a wide range of arthropod prey, as well as for defensive purposes against invertebrates and vertebrates, but are unable to adapt venom composition to stimuli (5, 6). Consequently, the expression of venom genes directly affects the ability of ants to interact with the biotic environment, and the venom composition may be fine-tuned to the ecology of each species. A previous study showed that defensive traits in ants exhibit an evolutionary trade-off in which the presence of a sting is negatively correlated with several other defensive traits, further supporting that trade-offs in defensive traits significantly constrain trait evolution and influence species diversification in ants (7). However, the sting is not used for the same purpose depending on the ant species. Our study supports an evolutionary trade-off between the ability of venom to deter vertebrates and to paralyze insects which are correlated with different life history strategies among Formicidae.

ecology↗

Comparative phylogenomic analyses of SNP versus full locus datasets: insights and recommendations for researchers

PremiseIn phylogenomic analyses, no consensus exists on whether using single nucleotide polymorphisms (SNPs) or including flanking regions (full locus) is best, nor how strictly missing data should be filtered. Moreover, empirical evidence on whether SNP-only trees are suitable for downstream phylogenetic comparative methods such as divergence time estimation and ancestral state reconstructions is lacking. MethodsUsing GBS data from 22 taxa of Glycine, we addressed the effects of SNP vs. locus usage and filtering stringency on phylogenomic inference and phylogenetic comparative methods. We compared branch length, node support, and divergence time estimation across eight datasets with varying amounts of missing data and total size. ResultsOur results reveal five aspects of phylogenomic data usage: 1. tree topology is largely congruent regardless of data type or filtering parameters; 2. filtering missing data too strictly reduces the confidence in some relationships; 3. absolute branch lengths vary by two orders of magnitude between datasets; 4. data type and branch length variation have little effect on divergence time estimation; 5. phylograms significantly alter the estimation of ancestral states. DiscussionWhen conducting phylogenomic analyses we recommend not to filter datasets too strictly to minimize the risk of misleading topologies, low support, and inaccurate divergence times.

evolutionary biology↗

Assessing biosynthetic gene cluster diversity in a multipartite nutritional symbiosis between herbivorous turtle ants and conserved gut symbionts

In insect-microbe nutritional symbioses the symbiont supplements the low nutrient diet of the host by producing amino acids and vitamins, and degrading lignin or polysaccharides. In multipartite mutualisms composed of multiple symbionts from different taxonomical orders, it has been suggested that in addition to the genes involved in the nutritional symbiosis the symbionts maintain genes responsible for the production of metabolites putatively playing a role in the maintenance and interaction of the bacterial communities living in close proximity. To test this hypothesis we investigated the diversity of biosynthetic gene clusters (BGCs) in the genomes and metagenomes of obligate gut symbionts associated with the herbivorous turtle ants (genus: Cephalotes). We studied 17 Cephalotes species collected across several geographical areas to reveal that (i) mining bacterial metagenomes and genomes provides complementary results demonstrating the robustness of this approach with metagenomic data, (ii) symbiotic gut bacteria have a high diversity of BGCs which is correlated with host geography but not host phylogeny, (iii) the majority of the BGCs comes from the bacteria involved in the nutritional symbiosis supporting conserved metabolic functions for colonization, communication and competition in the gut environment, (iv) phylogenetic analysis of arylpolyene, polyketide (PK), and siderophore shows high similarity between BGCs of a single symbiont across different ant host species, while non-ribosomal peptide (NRP) shows high similarity between BGCs from different bacterial orders within a single host species suggesting multiple mechanisms for genome evolution of these obligate mutualistic gut bacteria.

evolutionary biology↗

Evidences for convergent evolution of host parasitic manipulation in response to environmental conditions

Environmental conditions exert strong selection on animal behavior. We tested the hypothesis that the altered behavior of hosts due to parasitic manipulation is also subject to selection imposed by changes in environmental conditions over time. Our model system is ants manipulated by parasitic fungi to bite onto vegetation. We analyzed the correlation between forest type (tropical vs. temperate) and biting substrate (leaf vs. twigs), the time required for the fungi to reach reproductive maturity, and the phylogenetic relationship among specimens from tropical and temperate forests in different parts of the globe. We show that the fungal development in temperate forest is longer than the period of time leaves are present and the ants are manipulated to bite twigs. When biting twigs, 90% of the we examined dead ants had their legs wrapped around twigs, which appears to provide better attachment to the plant. Ancestral state character reconstruction suggests that the leaf biting is the ancestral trait and that twig biting is a convergent trait in temperate regions of the globe. These three lines of evidence suggest that changes in environmental conditions have shaped the manipulative behavior of the host by its parasite.

evolutionary biology↗

Mutualistic acacia-ants show that specialized bacteria are not required for the evolution of herbivory

Acacia-ant mutualists in the genus Pseudomyrmex nest obligately in acacia plants and, through stable isotope analysis, we show that they are among the strictest of herbivores, feeding exclusively from their hosts. The diets of herbivorous insects such as these are often enriched by obligate bacterial endosymbionts through nitrogen recycling and even gaseous di-nitrogen fixation. We, therefore, examine the bacterial communities associated with mutualistic acacia-ants, comparing them with related non-mutualists in order to determine whether they host bacterial partners likely to contribute to the enrichment of their diets. However, despite their low trophic position, we find no evidence for bacteria-assisted nutrition in either adults or larvae. These acacia-ants do not host any species- or clade-specific bacteria, though several lineages of acetic acid bacteria present across social insects do differ in abundance between mutualists and non-mutualists, likely in response to the sugar-rich diets of their hosts. In addition, two novel lineages of Actinomycetales inhabit both mutualistic and non-mutualistic Pseudomyrmex and differ in abundance between the juveniles of these groups, potentially serving as defensive symbionts. Metagenomic sequencing of these taxa reveal substantial capacity for the production of defensive chemicals. Overall, we find little evidence for nutrition-associated bacteria in these strictly herbivorous ants, showing that bacteria are not as essential to animal nutrition as is often hypothesized.

ecology↗