The evolution and functional morphology of trap-jaw ants

Key innovations are traits that allow organisms to interact with their environment in novel ways and are thought to facilitate adaptive radiation. By providing access to previously untapped resources, key innovations allow organisms to move into new ecological niches and can promote morphological diversification and speciation. I am interested in the evolution of form and function of one particular morphological innovation in the diversification of “trap-jaw” ants: power-amplified mandibles used for prey capture, nest defense, and individual escape from predators. Insects are the most diverse and numerically abundant animal group on the planet. One feature that contributed to their evolutionary success was the diversification their mouthparts. From an ancestral mandibulate condition (still found in many extant taxa), insect mouthparts have diversified into many specialized forms such as the piercing-sucking mouthparts of true bugs and various parasites, the sponging mouthparts of flies, and the extendible proboscis of butterflies and moths. This diversity has allowed insects to occupy a variety of dietary niches, including predation, herbivory, liquid feeding, and parasitism. An understanding of the relationship between structure and function of insect mouthparts is, therefore, critical for understanding their ecological success. My dissertation consists of four chapters and investigates the evolution and functional morphology the highly specialized mouthparts of trap-jaw ants. In Chapter 1, I review the current literature on trap-jaw ant taxonomy, phylogenetics, and biomechanics. The trap-jaw morphology has independently evolved at least four times in the ant family Formicidae, and, in this chapter, I highlight the areas of convergence among the four trap-jaw ant lineages. The most well studied lineage of trap-jaw ants are found in the subfamily Ponerinae, and consist of the sister genera Anochetus and Odontomachus. In Chapter 2, I present my findings from the first comprehensive worldwide phylogeny for these two trap-jaw ant genera. Using molecular sequence from four nuclear and one mitochondrial gene, I establish a phylogenetic framework for approximately half of the currently described species. Specifically, I confirm that the two genera are monophyletic sister groups, and found support for seven monophyletic clades. These trap-jaw ants diversified approximately 30 million years ago predominately in Southeast Asia, with multiple dispersal events to Australasia, the Afrotropics, and South America. Size often determines the output of animal performance systems, and examples of these scaling relationships are common throughout nature. What is unclear is if scaling relationships in musculoskeletal systems are shared within and between species. To answer this question, I examined morphological and performance scaling relationships between different sized trap-jaw ants and within a polymorphic species. I found that among species of Anochetus and Odontomachus, there is a strong and significant negative relationship between speed and body size, with larger and having longer snap durations and lower peak speeds. Contrasting with interspecific scaling relationships, the speed of mandible strikes within the polymorphic species Odontomachus turneri did not show any relationship with body size. Instead the peak kinetic energy of mandibles within and among Odontomachus species scaled with body size, suggesting that there may be stabilizing selection acting on mandible speed, but that strike energy may be determined by body size constraints. In Chapter 4, I examine the biomechanics, morphology and kinematics of the trap-jaw ant, Myrmoteras barbouri. A member of the ant subfamily Formicinae, Myrmoteras trap-jaw ants have received relatively little attention compared to other trap-jaw ant lineages and the mechanism of their spring-loaded mandibles have previously been unstudied. Using high-speed videography, I measured mandible strikes that occur in less than 1 millisecond and peak speeds of 2.6 x 104 rad·s-1. These speeds are faster than can be explained by direct muscle contraction, and confirm that Myrmoteras jaws are spring-loaded. The spring that stores the potential energy required for the strikes is a modification of the occipital margin, which bends during mandible loading. Compared with other trap-jaw ants, Myrmoteras jaws reach similar peak velocities, but accelerate over a much longer period of time, which is likely a reflection of their unique mandible mechanism

Rhode Island State Council on the Arts (1979-1992): Report 02

.csv file with the outcome data for predatory trials in the restraint experimen

Snap-jaw morphology is specialized for high-speed power amplification in the Dracula ant, \u3cem\u3eMystrium camillae\u3c/em\u3e

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 \u27snap-jaw\u27 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

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

Data from: 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)

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

<div><p>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 <i>Odontomachus brunneus</i> 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).</p></div

Frequency of escape behavior by trap-jaw ants in restraint experiment.

<p>Frequency of escape by running or jumping was quantified for each interaction. Ants were unmanipulated (Control), had glue applied to the exterior edge of mandible (Mock), or had their mandibles glued shut (Restrained). Each treatment was replicated 76 times.</p

Summary

Data summarizing the outcomes of trials between unrestrained trap-jaw ants (Odontomachus brunneus) and pitbuilding antlion

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.National Science Foundation [DDIG DEB-1407279, IOS-1354191]; Smithsonian Institution (Peter Buck Fellowship); National Geographic Society [9481-14]; School of Integrative Biology, University of Illinois, Urbana-Champaign12 month embargo; Published online August 30, 2017.This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

Restrained mandibles.

<p>Trap-jaw ant mandibles were glued shut to prevent ants from snapping.</p