Functional innovation promotes diversification of form in the evolution of an ultrafast trap-jaw mechanism in ants.

Evolutionary innovations underlie the rise of diversity and complexity-the 2 long-term trends in the history of life. How does natural selection redesign multiple interacting parts to achieve a new emergent function? We investigated the evolution of a biomechanical innovation, the latch-spring mechanism of trap-jaw ants, to address 2 outstanding evolutionary problems: how form and function change in a system during the evolution of new complex traits, and whether such innovations and the diversity they beget are repeatable in time and space. Using a new phylogenetic reconstruction of 470 species, and X-ray microtomography and high-speed videography of representative taxa, we found the trap-jaw mechanism evolved independently 7 to 10 times in a single ant genus (Strumigenys), resulting in the repeated evolution of diverse forms on different continents. The trap mechanism facilitates a 6 to 7 order of magnitude greater mandible acceleration relative to simpler ancestors, currently the fastest recorded acceleration of a resettable animal movement. We found that most morphological diversification occurred after evolution of latch-spring mechanisms, which evolved via minor realignments of mouthpart structures. This finding, whereby incremental changes in form lead to a change of function, followed by large morphological reorganization around the new function, provides a model for understanding the evolution of complex biomechanical traits, as well as insights into why such innovations often happen repeatedly.

Correction: A novel power-amplified jumping behavior in larval beetles (Coleoptera: Laemophloeidae).

[This corrects the article DOI: 10.1371/journal.pone.0256509.].

The spongiform tissue in Strumigenys ants contains exocrine glands.

The insect cuticle is multifunctional and often includes projections used for support, communication or protection. Ants in the genus Strumigenys exhibit a peculiar honeycomb-like spongiform tissue that covers their petiole, postpetiole and sometimes also the posterior mesosoma and anterior part of the first gastral segment. The tissue is abundantly developed in workers and queens, and much reduced in males. We found this spongiform tissue is associated with a novel exocrine gland that is made up by class-3 secretory cells that are clustered underneath the major pillars of the cuticular extensions, their associated narrow ducts enter these extensions and open at the surface through small pores. The chemical nature and function of the secretion are still unknown. The honeycomb texture may act in the storage and dispersion of the glandular secretions. In addition to the spongiform tissue gland, the posterior region of the petiole and postpetiole also contain intersegmental petiole and postpetiole glands, of which the ducts open through the intersegmental membrane that forms the connection with the next segment. Future work aimed at identifying the chemicals secreted by these glands will shed light onto the function of these unusual structures.

Testing the predictive value of functional traits in diverse ant communities.

Associating morphological features with ecological traits is essential for understanding the connection between organisms and their roles in the environment. If applied successfully, functional trait approaches link form and function in an organism. However, functional trait data not associated with natural history information provide an incomplete picture of an organism's role in the ecosystem. Using data on the relative trophic position of 592 ant (Formicidae) samples comprising 393 species from 11 subfamilies and 19 widely distributed communities, we tested the extent to which commonly used functional proxies (i.e., morphometric traits) predict diet/trophic position as estimated from stable isotopes (δ15N). We chose ants as a group due to their ubiquity and abundance, as well as the wealth of available data on species traits and trophic levels. We measured 12 traits that have previously been identified as functionally significant, and corrected trait values for size and evolutionary history by using phylogenetically corrected trait residuals. Estimated trophic positions varied from 0.9 to 4.8 or roughly 4 trophic levels. Morphological data spanned nearly the entire size range seen in ants from the smallest (e.g., Strumigenys mitis total length 1.1 mm) to the largest species (e.g., Dinoponera australis total length 28.3 mm). We found overall body size, relative eye position, and scape length to be informative for predicting diet/trophic position in these communities, albeit with relatively weak predictive values. Specifically, trophic position was negatively correlated with body size and positively correlated with sensory traits (higher eye position and scape length). Our results suggest that functional trait-based approaches can be informative but should be used with caution unless clear links between form and function have been established.

A novel power-amplified jumping behavior in larval beetles (Coleoptera: Laemophloeidae).

Larval insects use many methods for locomotion. Here we describe a previously unknown jumping behavior in a group of beetle larvae (Coleoptera: Laemophloeidae). We analyze and describe this behavior in Laemophloeus biguttatus and provide information on similar observations for another laemophloeid species, Placonotus testaceus. Laemophloeus biguttatus larvae precede jumps by arching their body while gripping the substrate with their legs over a period of 0.22 ± 0.17s. This is followed by a rapid ventral curling of the body after the larvae releases its grip that launches them into the air. Larvae reached takeoff velocities of 0.47 ± 0.15 m s-1 and traveled 11.2 ± 2.8 mm (1.98 ± 0.8 body lengths) horizontally and 7.9 ± 4.3 mm (1.5 ± 0.9 body lengths) vertically during their jumps. Conservative estimates of power output revealed that some but not all jumps can be explained by direct muscle power alone, suggesting Laemophloeus biguttatus may use a latch-mediated spring actuation mechanism (LaMSA) in which interaction between the larvae's legs and the substrate serves as the latch. MicroCT scans and SEM imaging of larvae did not reveal any notable modifications that would aid in jumping. Although more in-depth experiments could not be performed to test hypotheses on the function of these jumps, we posit that this behavior is used for rapid locomotion which is energetically more efficient than crawling the same distance to disperse from their ephemeral habitat. We also summarize and discuss jumping behaviors among insect larvae for additional context of this behavior in laemophloeid beetles.

Effects of Abdominal Rotation on Jump Performance in the Ant Gigantiops destructor (Hymenoptera, Formicidae).

Jumping is an important form of locomotion, and animals employ a variety of mechanisms to increase jump performance. While jumping is common in insects generally, the ability to jump is rare among ants. An exception is the Neotropical ant Gigantiops destructor (Fabricius 1804) which is well known for jumping to capture prey or escape threats. Notably, this ant begins a jump by rotating its abdomen forward as it takes off from the ground. We tested the hypotheses that abdominal rotation is used to either provide thrust during takeoff or to stabilize rotational momentum during the initial airborne phase of the jump. We used high speed videography to characterize jumping performance of G. destructor workers jumping between two platforms. We then anesthetized the ants and used glue to prevent their abdomens from rotating during subsequent jumps, again characterizing jump performance after restraining the abdomen in this manner. Our results support the hypothesis that abdominal rotation provides additional thrust as the maximum distance, maximum height, and takeoff velocity of jumps were reduced by restricting the movement of the abdomen compared with the jumps of unmanipulated and control treatment ants. In contrast, the rotational stability of the ants while airborne did not appear to be affected. Changes in leg movements of restrained ants while airborne suggest that stability may be retained by using the legs to compensate for changes in the distribution of mass during jumps. This hypothesis warrants investigation in future studies on the jump kinematics of ants or other insects.

Spanish: Efectos de la rotación abdominal en el desempeño del salto de la hormiga Gigantiops destructor (Hymenoptera, Formicidae) El salto es una forma importante de locomoción y muchos animales utilizan diversidad de mecanismos al saltar para mejorar su desempeño. A pesar de que el salto es común en insectos, en general, las hormigas presentan una habilidad limitada. La hormiga neotropical Gigantiops destructor (Fabricius 1804) es una excepción, y utiliza el salto para capturar presas o escapar de potenciales amenazas. Esta especie empieza el salto rotando el abdomen anteriormente al impulsarse desde el suelo. Se evaluaron las hipótesis que la rotación abdominal se usa tanto para la proporción de empuje durante el impulso, así como en la estabilización de la cantidad de movimiento rotacional durante la fase inicial del salto mientras se encuentra en el aire. Se usó videografía de alta velocidad para caracterizar el desempeño del salto entre dos plataformas. Posteriormente, un grupo de hormigas fueron anestesiadas, y con el uso de pegamento, se restringió el movimiento del abdomen para evitar la rotación de éstos en la subsecuente caracterización del desempeño al saltar. Los resultados apoyan la hipótesis que la rotación abdominal proporciona impulso adicional. La distancia máxima, el peso máximo y la velocidad del impulso durante el salto fueron reducidos cuando el abdomen está fijo comparados con los saltos de las hormigas que no sufrieron manipulación y las que se usaron en el tratamiento control. En contraste, no hubo evidencia que la estabilidad de rotación de las hormigas mientras se encontraban en el aire fuera afectada. Las hormigas con abdómenes fijos presentaron cambios en el movimiento de las patas que sugieren que la estabilidad se puede mantener al usar las patas y compensar la distribución de la masa durante el salto. Esta hipótesis justifica futuros estudios evaluando la cinemática del salto en hormigas y otros grupos de insectos. Translated to Spanish by Rafael Achury (rafaelachury@gmail.com).

French: Effet de la rotation abdominal sur les performances du saut chez la fourmi Gigantiops destructor (Hymenoptera, Formicidae) Sauter est une importante forme de locomotion, et les animaux utilisent une diversité de mécanismes pour améliorer les performances de leurs sauts. Meme si sauter est commun chez les insectes en général, la capacité de sauter est rare chez les fourmis. La fourmi néotropicale Gigantiops destructor (Fabricius 1804) est une exception, elle est reconnue pour sauter sur ces proies ou pour s'échapper des menaces. Singulièrement, cette fourmi commence un saut par une rotation de son abdomen vers l'avant au moment de décoller du sol. Nous avons testé l'hypothèse que la rotation abdominale est utilisée pour soit générer une poussée au décollage, soit stabiliser l'élan rotatif pendant la phase aérienne initiale du saut. Nous avons utilisé l'enregistrement vidéo de grande vitesse pour caractériser la performance du saut des ouvrières G. destructor entre deux plateformes. Ensuite, nous avons anesthesié les fourmis et utilisé de la colle pour empêcher leurs abdomens de pivoter durant les prochains sauts, pour de nouveau caractériser la performance du saut suite à la restriction dudit abdomen de cette manière. Nos résultats soutiennent l'hypothèse que la rotation de l'abdomen entraine une poussée supplementaire vu que la distance maximale, la hauteur maximale et la vitesse de décollage des sauts sont réduites par la restriction du mouvement de l'abodmen comparer aux sauts des fourmis non manipulées du groupe témoin. Au contraire, la stabilité rotative des fourmis en phase aérienne ne semble pas être affectée. Les changements dans le mouvement des pattes des fourmis restraintes suggèrent que la stabilité peut être conservée en utilisant les pattes pour compenser les variations de la distribution de la masse pendant le saut. Cette hypothèse garantie, dans de futures études, l'exploration la cinématique du saut chez les fourmis et autres insectes. Translated to French by Jules Chabain (chabain2@illinois.edu).

Portuguese: Efeitos de Rotação Abdominal no Desempenho de Salto na Formiga Gigantiops destructor (Hymenoptera, Formicidae) O salto é uma forma importante de locomoção, e os animais empregam uma variedade de mecanismos para aumentar a performance de salto. Embora o salto seja comum nos insetos em geral, a capacidade de saltar é rara entre as formigas. Uma exceção é a formiga neotropical Gigantiops destructor (Fabricius 1804), conhecido por saltar para capturar presas ou escapar de ameaças. Notavelmente, essa formiga começa um salto girando seu abdômen para a frente enquanto sai do chão. Testamos as hipóteses de que a rotação abdominal é usada para fornecer impulso durante a saída do chão ou para estabilizar o momento de rotação durante a fase inicial do salto no ar. Utilizamos videografia de alta velocidade para caracterizar o desempenho de saltos de formigas operárias de G. destructor saltando entre duas plataformas. Em seguida, anestesiamos as formigas e aplicamos cola para impedir que o abdômen gire durante os saltos subsequentes, caracterizando novamente o desempenho do salto após restringir o abdômen dessa maneira. Nossos resultados suportam a hipótese de que a rotação abdominal fornece impulso adicional, pois a distância máxima, a altura máxima e a velocidade de saída dos saltos foram reduzidas pela restrição do movimento do abdômen, em comparação aos saltos das formigas não manipuladas e de controle. Em contraste, a estabilidade rotacional das formigas no ar não pareceu ser afetada. Alterações nos movimentos das pernas no ar das formigas restringidas sugerem que a estabilidade pode ser mantida usando as pernas para compensar as mudanças na distribuição da massa durante os saltos. Essa hipótese merece investigação em estudos futuros sobre a cinemática do salto de formigas ou outros insetos.Translated to Portuguese by Diego Vaz (dbistonvaz@vims.edu).

Development but not diet alters microbial communities in the Neotropical arboreal trap jaw ant Daceton armigerum: an exploratory study.

To better understand the evolutionary significance of symbiotic interactions in nature, microbiome studies can help to identify the ecological factors that may shape host-associated microbial communities. In this study we explored both 16S and 18S rRNA microbial communities of D. armigerum from both wild caught individuals collected in the Amazon and individuals kept in the laboratory and fed on controlled diets. We also investigated the role of colony, sample type, development and caste on structuring microbial communities. Our bacterial results (16S rRNA) reveal that (1) there are colony level differences between bacterial communities; (2) castes do not structure communities; (3) immature stages (brood) have different bacterial communities than adults; and 4) individuals kept in the laboratory with a restricted diet showed no differences in their bacterial communities from their wild caught nest mates, which could indicate the presence of a stable and persistent resident bacterial community in this host species. The same categories were also tested for microbial eukaryote communities (18S rRNA), and (5) developmental stage has an influence on the diversity recovered; (6) the diversity of taxa recovered has shown this can be an important tool to understand additional aspects of host biology and species interactions.