Biology subjects

LeBoeuf, A. C.

Publications and source records attributed to LeBoeuf, A. C..

10 recordsLinked to original sources

bioRxiv2026

Genome assemblies and annotations of the poneroid ants Platythyrea mocquerysi (Ponerinae) and Stigmatomma oregonense (Amblyoponinae)

We present draft genome assemblies for two poneroid ant species with distinctive life history traits: Platythyrea mocquerysi Emery, 1899 (Ponerinae) and Stigmatomma oregonense Wheeler, 1915 (Amblyoponinae). Platythyrea mocquerysi is a Malagasy ant in which larvae produce secretions from a ventral tubercle that are consumed by adults, representing an unusual form of larva-to-adult trophallaxis. Stigmatomma oregonense, a North American "dracula ant," feeds non-lethally on larval haemolymph. Using PacBio HiFi long-read sequencing, we assembled the P. mocquerysi genome (187 Mb, 307 scaffolds, N50 = 5.26 Mb, BUSCO 99.2% complete) and the S. oregonense genome (262 Mb, 1,189 scaffolds, N50 = 0.84 Mb, BUSCO 98.3% complete). These genomes encode 10,860 and 12,354 protein-coding genes, respectively. Repeat content is higher in S. oregonense than in P. mocquerysi, 54.3% against a lower bound of 15.7%. Most of the difference is in unclassified repeats, which we show to be diverged transposable elements. Comparative analysis with two additional poneroid genomes from closely related species reveals that genome size variation across poneroid ants is largely explained by transposable element dynamics, with notable expansions in several gene families including carboxylesterases, serine proteases, and lipid metabolism genes in Amblyoponinae. These genomes provide essential resources for investigating the molecular basis of unconventional brood management strategies in ants.

genomics↗

bioRxiv2026

Genomic insights into bacterial isolates dominating honeypot ant crop microbiomes reveal metabolically distinct Fructilactobacillus sp.

Honeypot ants engage in a convergently-evolved phenotype called repletism, where specialized workers expand their crops and gasters to store vast amounts of food internally. They then store that food for months to support colonies during times of food scarcity. This fascinating phenotype is not well-understood and very little is known about the microbial interactions happening within the fructose-rich replete crop. Previous research using amplicon sequencing showed that Fructilactobacillus makes up nearly 100% of the crop microbiomes of Myrmecocystus mexicanus repletes. This striking result and successful isolation of those strains led to the present investigation into the phylogenetic diversity of these strains and any clues to the nature of the symbiotic relationship between them and the ant host. We find that the isolates from these repletes represented two evolutionary lineages, both most closely related to F. fructivorans. One of those lineages was also found to be phylogenetically and metabolically distinct from all other Fructilactobacillus reference genomes used in this study. This discovery in a genus of bacteria that are highly relevant for fermented human foods and will also lay the groundwork for future understanding of the convergent evolutionary mechanisms of repletism in ants. 3. Impact statementThese analyses add to the literature by identifying a new microbe within a genus that is relevant to food systems. In addition, the host phenotype is convergently evolved and likely microbe-mediated (or at least highly exposed). Understanding this system allows for the testing of ideas of coevolutionary hypotheses with natural replicates. We expect interest to come from food safety and probiotics researchers, evolutionary biologists that think about the impacts of microbes, microbial ecologists interested in novel systems, and those interested in bacteria that may display unique metabolic possibilities. This output allows for the clear future examination of this system with many clear hypotheses. Our analysis allows for the creation of a new and unique model system of host-microbe symbiosis. 4. Data summaryNew genomes assembled in this work can be found under BioProject ID PRJNA1449409. https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA1449409. Reference bacterial genomes were obtained from NCBI at the following accession numbers: SAMN20557570, SAMN28081009, SAMN28081010, SAMN02597458, SAMN43111088, SAMN28081011, SAMN28535231, SAMN04505734, SAMN28081013, SAMN33452149, SAMN37926504, SAMN02849426, SAMN02470196, SAMN02369432, SAMN02797779, SAMN02797782, SAMN02797768, SAMN09762388, SAMN12785275, SAMEA117660288. The honeypot ant genome was obtained from SAMN37666067. Raw proteomics files will be uploaded to ProteomeXchange with a unique identifier upon manuscript acceptance.

genomics↗

bioRxiv2025

The origins and molecular evolution of sperm

Sperm is a nearly universal cell type among animals, yet its evolutionary origins remain unclear. Using comparative proteomics and phylogenomics across 32 species, we reconstruct the 700+ million year evolutionary history of sperm to define the Last Universal Common Sperm (LUCS), a conserved core of 301 gene families enriched in motility and energy metabolism. We found that most of the LUCS toolkit was developed in filozoan unicellular ancestors approximately 400 Ma before animals, revealing sperm as a reconfigured legacy from our unicellular past rather than an invention of multicellularity. Sperm shows a within-cell evolutionary gradient, both spatial and temporal, where ancient proteins dominate the tail, while younger innovations concentrate in the head. The oldest sperm components are disproportionately associated with human infertility, establishing an empirical bridge between evolutionary depth and clinical relevance. Together, our findings reveal how evolutionary history is inscribed within a single cell and can guide clinical insights.

evolutionary biology↗

bioRxiv2025

A stochastic ratchet during genome streamlining can commit insect endosymbionts to a parasitic or mutualistic fate

Many arthropods, including insects, harbor endosymbiotic bacteria. As bacteria transitioned to live inside host cells, free-living bacterial ancestors of endosymbionts reduced their genomes in a process known as streamlining. Contemporary endosymbioses represent at least two distinct life strategies: endosymbionts either become unilaterally dependent on host-derived resources (uni-obligate) or enter bidirectionally obligate mutualistic relationships (bi-obligate endosymbiosis). It is an open question whether these paths taken by free-living bacteria can be sequential, or alternatively, if commitment takes place early, making these strategies mutually exclusive. In this study, we quantified metabolic capacity of different endosymbionts to contextualize genome streamlining in terms of organismal function. We show that uni-obligate endosymbionts of insects have lost substantial parts of their metabolic capacity that are present both in free-living bacteria and bi-obligate endosymbionts. On the contrary, genomes of uni-obligate endosymbionts contain more genes which can be attributed to scavenging host resources. In sum, we challenge the existing notion that bi-obligate endosymbionts have emerged from uni-obligate ones, and rather, propose a stochastic ratchet model: in early stages of endosymbiosis, bacteria get locked into either a more mutualistic or more parasitic relationship with the host depending on the first losses during streamlining.

systems biology↗

bioRxiv2024

Plasticity and evolution of metabolic division of labour within families

Fluids produced by parents for dependent young, such as milk or regurgitate, carry molecules that assist offspring with growth, immunity and digestion, allowing the metabolic burden of development to be shared between parents and offspring. We tested whether this division of metabolic labour changes plastically and evolves when offspring are experimentally deprived of their parents metabolic assistance. In the burying beetle Nicrophorus vespilloides parents deposit oral fluids on their carrion nest during pre-hatching care, and facultatively transfer fluids to larvae through oral trophallaxis as post-hatching care. We analysed the oral fluid proteomes of replicate experimental populations that had been evolving for 50 generations with or without post-hatching care, and which were then allowed to raise larvae with or without post-hatching care for one experimental generation. We found that parents and larvae plastically and evolutionarily adjusted the proteins in their oral fluids when we prevented post-hatching care. When reared in the absence of post-hatching care, larvae that evolved without post-hatching care were also more capable of consuming carrion proteins than larvae that had evolved with post-hatching care, and had higher survival. Our results suggest that metabolic division of labour within families is plastically modulated, and that the extent of socially modulated plasticity can evolve rapidly when social conditions change.

evolutionary biology↗

bioRxiv2022

Ruling the unruly: Larval passiveness enabled size inequality between ant queens and workers

Building differences between genetically equivalent units is a fundamental challenge for every (super)organism with reproductive division of labor. In ants, reproductive or worker fate is typically determined during the larval stage. However, the methods by which adults feed their larvae, thus controlling their development, vary widely across ant species. Similarly, the body size gap between queen and worker is highly heterogeneous, ranging from species with similar-sized individuals to species with queens over 300 times larger than their smallest workers. To investigate the role of alloparental feeding control in caste dimorphism and the evolution of social complexity, we assembled data for queen:worker dimorphism, alloparental care, and larval morphology for a phylogenetically comprehensive sample of several hundred species, along with ecological and life-history traits. Using comparative phylogenetic methods, we analyzed the macroevolution of ant larvae and queen:worker dimorphism on a large scale. Our findings indicate that both extended alloparental feeding care and dimorphism are associated with the evolution of passive larval morphologies. Furthermore, greater queen:worker dimorphism co-evolved with several traits indicative of social complexity, including larger colony sizes, distinct worker subcastes, and the loss of full reproductive potential in workers. In sum, change in larval feeding habits were promoted by dietary shifts from prey to foods necessitating individualized distribution. These innovations granted adults greater capacity to manipulate larval nutrition, and consequently, caste size inequality, with significant implications for social complexity. Significance statementAnts are among the rare organisms to have extended reproductive division labor beyond the cells of a multicellular organism. However, the degree of specialization between reproductive and worker castes varies considerably between ant lineages. In this study, we demonstrate that strong caste dimorphism in ants co-evolved with complex eusociality traits, and this strong caste dimorphism was achieved by asserting adult control over larvae development. We conclude that this enhanced control over larval caste fate was a critical junction in the major evolutionary transition of ants toward caste specialization. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=125 SRC="FIGDIR/small/519655v2_ufig1.gif" ALT="Figure 1"> View larger version (21K): org.highwire.dtl.DTLVardef@9347dborg.highwire.dtl.DTLVardef@1528464org.highwire.dtl.DTLVardef@71c2f0org.highwire.dtl.DTLVardef@b52a2d_HPS_FORMAT_FIGEXP M_FIG C_FIG

evolutionary biology↗

bioRxiv2022

Ecological change and conflict reduction led to the evolution of a transformative social behavior in ants

Behavioral innovations can be ecologically transformative for lineages that perform them and for their associated communities. Many ecologically dominant, superorganismal, and speciose ant lineages use a mouth-to-mouth fluid exchange behavior - trophallaxis - to share both exogenously sourced and endogenously produced materials across their colonies, while lineages that are less abundant, less cooperative and less speciose tend not to perform this behavior. How and why this behavior evolved and fixed in only some ant lineages remains unclear and whether this trait enables ants ecological dominance is not yet understood. Here we show that trophallaxis evolved in two major events ~110 Ma in lineages that today encompass 36% of ants, and in numerous smaller and more recent events. We found that trophallaxis evolved early only in ant lineages that had reduced intra-colonial conflict by losing workers ability to reproduce. Our causal models indicate that this signature behavior of superorganismal ants required social cooperation and ecological opportunism, and likely contributed to the large colony sizes and speciation patterns of the ants that use it and dominate our landscapes today. We hypothesize that the early evolution of trophallaxis was brought about by a major shift in terrestrial ecosystems through the origin and diversification of flowering plants and the consequent opportunistic inclusion of nectar and sap-sucker honeydew in the ant diet.

evolutionary biology↗

bioRxiv2022

Ants dynamically adjust liquid foraging strategies in response to biophysical constraints

Ant foragers need to provide food to the rest of the colony, which often requires transport over long distances. Foraging for liquid is especially challenging because it is difficult to transport and share. Many social insects store liquid food inside the crop to transport it to the nest, and then regurgitate this fluid to distribute it to nestmates through a behaviour called trophallaxis. Some ants instead transport fluids with a riskier behaviour called pseudotrophallaxis - holding a drop of liquid between the mandibles through surface tension. Ants can then share this droplet with nestmates without ingestion or regurgitation. Here, we hypothesised that ants optimise their liquid-collection approach depending on viscosity. Working with a ponerine ant that uses both trophallaxis and pseudotrophallaxis, we investigated why each liquid-collection behaviour might be favoured under different conditions by measuring biophysical properties, collection time, and reaction to food quality for typical and viscosity-altered sucrose solutions. We found that ants can collect more liquid food per unit time by mandibular grabbing than by drinking. At high viscosities, which in nature correspond to high sugar concentrations, ants switched their liquid collection method to mandibular grabbing in response to viscosity, and not to sweetness. Our results demonstrate that ants change their transport and sharing methods according to viscosity - a proxy for sugar concentration in nature - increasing the mass of sugar returned to the nest per trip.

animal behavior and cognition↗

bioRxiv2021

Dynamic variation in a socially exchanged fluid indicates a role in the regulation of ant colony development and maturation

Socially exchanged fluids, like seminal fluid and milk, allow individuals to molecularly influence conspecifics. Many social insects have a social circulatory system, where food and endogenously produced molecules are transferred mouth-to-mouth (stomodeal trophallaxis), connecting all the individuals in the society. To understand how these endogenous molecules relate to colony life, we used quantitative proteomics to investigate the trophallactic fluid within colonies of the carpenter ant Camponotus floridanus. We show that different stages of the colony life cycle circulate different types of proteins: young colonies prioritize direct carbohydrate processing; mature colonies prioritize accumulation and transmission of stored resources. Further, colonies circulate proteins implicated in oxidative stress, ageing, and social insect caste determination, potentially acting as superorganismal hormones. Brood-caring individuals that are also closer to the queen in the social network (nurses) showed higher abundance of oxidative stress-related proteins. Thus, trophallaxis behavior provides a mechanism for distributed metabolism in social insect societies.

evolutionary biology↗

bioRxiv2018

Molecular evolution of juvenile hormone esterase-like proteins in a socially exchanged fluid

Socially exchanged fluids are a direct means for organisms to influence conspecifics. When orally feeding larval offspring via trophallaxis, Camponotus floridanus ant workers were shown to transfer Juvenile Hormone (JH), a key developmental regulator, as well as paralogs of JH esterase (JHE), an enzyme that hydrolyzes JH. We combine proteomic, phylogenetic and selection analyses to investigate the evolution of this esterase subfamily. We show that Camponotus JHE-like proteins have sustained multiple duplications, positive selection, and changed localization to become abundantly and selectively present in trophallactic fluid. To assess their potential role in larval development, we fed workers a JHE-specific inhibitor to introduce it into the trophallactic network. This increased the proportion larvae reared to metamorphosis by these workers, similar to supplementation with JH. Together these findings suggest that JHE-like proteins have evolved new roles in inter-individual regulation of larval development in Camponotus.

evolutionary biology↗