Taxon cycle predictions supported by model-based inference in Indo-Pacific trap-jaw ants (Hymenoptera: Formicidae: Odontomachus).

Nonequilibrium dynamics and non-neutral processes, such as trait-dependent dispersal, are often missing from quantitative island biogeography models despite their potential explanatory value. One of the most influential nonequilibrium models is the taxon cycle, but it has been difficult to test its validity as a general biogeographical framework. Here, we test predictions of the taxon cycle model using six expected phylogenetic patterns and a time-calibrated phylogeny of Indo-Pacific Odontomachus (Hymenoptera: Formicidae: Ponerinae), one of the ant genera that E.O. Wilson used when first proposing the hypothesis. We used model-based inference and a newly developed trait-dependent dispersal model to jointly estimate ancestral biogeography, ecology (habitat preferences for forest interiors, vs. "marginal" habitats, such as savannahs, shorelines, disturbed areas) and the linkage between ecology and dispersal rates. We found strong evidence that habitat shifts from forest interior to open and disturbed habitats increased macroevolutionary dispersal rate. In addition, lineages occupying open and disturbed habitats can give rise to both island endemics re-occupying only forest interiors and taxa that re-expand geographical ranges. The phylogenetic predictions outlined in this study can be used in future work to evaluate the relative weights of neutral (e.g., geographical distance and area) and non-neutral (e.g., trait-dependent dispersal) processes in historical biogeography and community ecology.

Performance, morphology and control of power-amplified mandibles in the trap-jaw ant Myrmoteras (Hymenoptera: Formicidae).

Trap-jaw ants are characterized by high-speed mandibles used for prey capture and defense. Power-amplified mandibles have independently evolved at least four times among ants, with each lineage using different structures as a latch, spring and trigger. We examined two species from the genus Myrmoteras (subfamily Formicinae), whose morphology is unique among trap-jaw ant lineages, and describe the performance characteristics, spring-loading mechanism and neuronal control of Myrmoteras strikes. Like other trap-jaw ants, Myrmoteras latch their jaws open while the large closer muscle loads potential energy in a spring. The latch differs from other lineages and is likely formed by the co-contraction of the mandible opener and closer muscles. The cuticle of the posterior margin of the head serves as a spring, and is deformed by approximately 6% prior to a strike. The mandibles are likely unlatched by a subgroup of closer muscle fibers with particularly short sarcomeres. These fast fibers are controlled by two large motor neurons whose dendrites overlap with terminals of large sensory neurons originating from labral trigger hairs. Upon stimulation of the trigger hairs, the mandibles shut in as little as 0.5 ms and at peak velocities that are comparable with other trap-jaw ants, but with much slower acceleration. The estimated power output of the mandible strike (21 kW kg-1) confirms that Myrmoteras jaws are indeed power amplified. However, the power output of Myrmoteras mandibles is significantly lower than distantly related trap-jaw ants using different spring-loading mechanisms, indicating a relationship between power-amplification mechanism and performance.

Molecular phylogenetics and diversification of trap-jaw ants in the genera Anochetus and Odontomachus (Hymenoptera: Formicidae).

Ants in the genera Anochetus and Odontomachus belong to one of the largest clades in the subfamily Ponerinae, and are one of four lineages of ants possessing spring-loaded "trap-jaws." Here we present results from the first global species-level molecular phylogenetic analysis of these trap-jaw ants, reconstructed from one mitochondrial, one ribosomal RNA, and three nuclear protein-coding genes. Bayesian and likelihood analyses strongly support reciprocal monophyly for the genera Anochetus and Odontomachus. Additionally, we found strong support for seven trap-jaw ant clades (four in Anochetus and three in Odontomachus) mostly concordant with geographic distribution. Ambiguity remains concerning the closest living non-trap-jaw ant relative of the Anochetus+Odontomachus clade, but Bayes factor hypothesis testing strongly suggests that trap-jaw ants evolved from a short mandible ancestor. Ponerine trap-jaw ants originated in the early Eocene (52.5Mya) in either South America or Southeast Asia, where they have radiated rapidly in the last 30million years, and subsequently dispersed multiple times to Africa and Australia. These results will guide future taxonomic work on the group and act as a phylogenetic framework to study the macroevolution of extreme ant mouthpart specialization.

Muscle fatigue in the latch-mediated spring actuated mandibles of trap-jaw ants.

Muscle fatigue can reduce performance potentially affecting an organism's fitness. However, some aspects of fatigue could be overcome by employing a latch-mediated spring actuated system (LaMSA) where muscle activity is decoupled from movement. We estimated the effects of muscle fatigue on different aspects of mandible performance in six species of ants, two whose mandibles are directly actuated by muscles and four that have LaMSA "trap-jaw" mandibles. We found evidence that the LaMSA system of trap-jaw ants may prevent some aspects of performance from declining with repeated use, including duration, acceleration and peak velocity. However, inter-strike interval increased with repeated strikes suggesting that muscle fatigue still comes into play during the spring loading phase. In contrast, one species with directly actuated mandibles showed a decline in bite force over time. These results have implications for design principles aimed at minimizing the effects of fatigue on performance in spring and motor actuated systems.

Relaxed selection underlies genome erosion in socially parasitic ant species.

Inquiline ants are highly specialized and obligate social parasites that infiltrate and exploit colonies of closely related species. They have evolved many times convergently, are often evolutionarily young lineages, and are almost invariably rare. Focusing on the leaf-cutting ant genus Acromyrmex, we compared genomes of three inquiline social parasites with their free-living, closely-related hosts. The social parasite genomes show distinct signatures of erosion compared to the host lineages, as a consequence of relaxed selective constraints on traits associated with cooperative ant colony life and of inquilines having very small effective population sizes. We find parallel gene losses, particularly in olfactory receptors, consistent with inquiline species having highly reduced social behavioral repertoires. Many of the genomic changes that we uncover resemble those observed in the genomes of obligate non-social parasites and intracellular endosymbionts that branched off into highly specialized, host-dependent niches.

Snap-jaw morphology is specialized for high-speed power amplification in the Dracula ant, Mystrium camillae.

What is the limit of animal speed and what mechanisms produce the fastest movements? More than natural history trivia, the answer provides key insight into the form-function relationship of musculoskeletal movement and can determine the outcome of predator-prey interactions. The fastest known animal movements belong to arthropods, including trap-jaw ants, mantis shrimp and froghoppers, that have incorporated latches and springs into their appendage systems to overcome the limits of muscle power. In contrast to these examples of power amplification, where separate structures act as latch and spring to accelerate an appendage, some animals use a 'snap-jaw' mechanism that incorporates the latch and spring on the accelerating appendage itself. We examined the kinematics and functional morphology of the Dracula ant, Mystrium camillae, who use a snap-jaw mechanism to quickly slide their mandibles across each other similar to a finger snap. Kinematic analysis of high-speed video revealed that snap-jaw ant mandibles complete their strike in as little as 23 µsec and reach peak velocities of 90 m s-1, making them the fastest known animal appendage. Finite-element analysis demonstrated that snap-jaw mandibles were less stiff than biting non-power-amplified mandibles, consistent with their use as a flexible spring. These results extend our understanding of animal speed and demonstrate how small changes in morphology can result in dramatic differences in performance.

Mandible-Powered Escape Jumps in Trap-Jaw Ants Increase Survival Rates during Predator-Prey Encounters.

Animals use a variety of escape mechanisms to increase the probability of surviving predatory attacks. Antipredator defenses can be elaborate, making their evolutionary origin unclear. Trap-jaw ants are known for their rapid and powerful predatory mandible strikes, and some species have been observed to direct those strikes at the substrate, thereby launching themselves into the air away from a potential threat. This potential escape mechanism has never been examined in a natural context. We studied the use of mandible-powered jumping in Odontomachus brunneus during their interactions with a common ant predator: pit-building antlions. We observed that while trap-jaw ant workers escaped from antlion pits by running in about half of interactions, in 15% of interactions they escaped by mandible-powered jumping. To test whether escape jumps improved individual survival, we experimentally prevented workers from jumping and measured their escape rate. Workers with unrestrained mandibles escaped from antlion pits significantly more frequently than workers with restrained mandibles. Our results indicate that some trap-jaw ant species can use mandible-powered jumps to escape from common predators. These results also provide a charismatic example of evolutionary co-option, where a trait that evolved for one function (predation) has been co-opted for another (defense).

Ler interdomain linker is essential for anti-silencing activity in enteropathogenic Escherichia coli.

Enteropathogenic Escherichia coli (EPEC) expresses a type III secretion system (T3SS) required for pathogenesis. Regulation of the genes encoding the T3SS is complex; two major regulators control transcription, the silencer H-NS, and the related H-NS-like protein Ler. Our laboratory is interested in understanding the molecular differences that distinguish the anti-silencer Ler from H-NS, and how Ler differentially regulates EPEC virulence genes. Here, we demonstrate that mutated Ler proteins either containing H-NS alpha-helices 1 and 2, missing from Ler, or truncated for the 11 aa C-terminal extension compared with the related H-NS protein, did not appreciably alter Ler function. In contrast, mutating the proline at position 92 of Ler, in the conserved C-terminal DNA binding motif, eliminated Ler activity. Inserting 11 H-NS-specific amino acids, 11 alanines or 6 alanines into the Ler linker severely impaired the ability of Ler to increase LEE5 transcription. To extend our analysis, we constructed six chimeric proteins containing the N terminus, linker region or C terminus of Ler in different combinations with the complementary domains of H-NS, and monitored their in vivo activities. Replacing the Ler linker domain with that of H-NS, or replacing the Ler C-terminal, DNA binding domain with that of H-NS eliminated the ability of Ler to increase transcription at the LEE5 promoter. Thus, the linker and C-terminal domains of Ler and H-NS are not functionally equivalent. Conversely, replacing the H-NS linker region with that of Ler caused increased transcription at LEE5 in a strain deleted for hns. In summary, the interdomain linker specific to Ler is necessary for anti-silencing activity in EPEC.