07/10: Not just cogs in the machine: functional morphology and biomechanics of social insects

07/10 - Not just cogs in the machine: functional morphology and biomechanics of social insects

 

ORGANISERS: Vincent Fourcassié a, Roberto A. Kellerb

a Centre de Recherches sur la Cognition Animale, University Paul Sabatier - Toulouse III, France; b National Museum of Natural History and Science, ULisboa, Portugal

 

CONTACT: vincent.fourcassie@univ-tlse3.fr

 

SUMMARY:

Functional morphology investigates the relationships between the structural components of organisms and the function these components perform. It sheds light on the evolutionary forces that have shaped anatomical adaptations to the environment. Because of the variety of forms encountered in social insects, among as well as within species, social insects provide excellent biological material for research in functional morphology. For example, this approach allows to characterize the morphological specializations that relate to the division of labor between the worker caste and the reproductive caste or within the worker caste in size-polymorphic species. Together with traditional dissections, histology, and SEM images, new 3D imaging methods (X-ray and synchrotron microtomography), in tandem with comparative phylogenetics and geometric morphometrics, offer great opportunities to investigate both the drivers and consequences of evolutionary changes in morphology. At the same time, cheap high speed, high resolution video cameras coupled to automatic tracking software and miniaturized force measurement sensors allow to investigate the kinematics and dynamics of body and appendage movements with unprecedented precision. All these techniques constitute a major asset for the characterization of the functional properties of the external and internal body structures of the individual insects and, in the case of social insects, for the understanding of their role in the division of labor within colonies. In this symposium we will address some of the most recent advances in social insect functional morphology and biomechanics that have been made possible by the use of these tools and techniques.

 

ZOOM LINK:

https://univ-tlse3-fr.zoom.us/j/92949885220

 

PROGRAMME (London time, pm):

 

Time

  Speaker

Title

12:00 

 

Introduction to the symposium

12:05

 Walter Federle

Biomechanics of ant-plant interactions

12:35

 Patrick Schultheiss

Kinematic study of six mangrove ant species (Hymenoptera: Formicidae) reveals different swimming styles and abilities

12:50

 Jordan Drapin

A biomechanical approach of Messor barbarus locomotor pattern

13:05 

 Mathilde Lacombrade

Morphological correlates of dispersal abilities in the yellow-legged hornet

13:20

 

Break

13:35

 Evan Economo

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

14:05 

 Adam Khalife

Multiple ways to miniaturize: ecology and behaviour dictate space allocation inside the thorax of minute ants

14:20

 Lazzat Aibekova

The evolution of forward jumping ants

14:35

 Lohan Valadares

Brain plasticity and behavioural specialisation in the jatai stingless bee (Tetragonisca angustula)

14:50 

 

Final discussion

 

ABSTRACTS:

 

Biomechanics of ant-plant interactions

Walter Federle1

1 Department of Zoology, University of Cambridge, UK

Social insects interact with plants in a variety of ways, as pollinators, herbivores, protectors from herbivores, seed dispersers and even as prey for carnivorous plants. However, life on plants involves a number of biomechanical problems, and the mechanisms and adaptations can have far-reaching ecological and evolutionary consequences. I will demonstrate how studying functional morphology and biomechanics is important for understanding the biology of social insects. I will focus on the role of insect attachment to plant surfaces: How can insects walk with sticky feet? How do plants prevent insects from attaching? How can insects overcome plant defence mechanisms?

 

Kinematic study of six mangrove ant species (Hymenoptera: Formicidae) reveals different swimming styles and abilities

Patrick Schultheiss1 & Bénoit Guénard1

1 School of Biological Sciences, University of Hong Kong, Hong Kong

Most insects are morphologically and behaviourally adapted to a terrestrial lifestyle, and many species struggle if they fall onto the water surface. Yet some terrestrial species exhibit an efficient aquatic locomotion ability that enables them to escape such perilous environments. Here, we perform a comparative study that investigates such swimming behaviour in six taxonomically diverse arboreal species of ants from a mangrove habitat and describe the leg kinematics in detail. Between species, we find large differences in the speed and directedness of their swimming locomotion, and correspondingly large differences in swimming styles, i.e., leg kinematics and synchronisation patterns. Our results demonstrate that some species do in fact display behavioural adaptations for efficient and directed swimming, and that their locomotion patterns are not analogous to those observed during walking. Ultimately, we suggest that the study of swimming behaviour in ants may provide an interesting model system for the study of neural control in insect leg coordination.

 

A biomechanical approach of Messor barbarus locomotor pattern

Jordan Drapin1, Moran Le Gelau1, Vincent Fourcassié1, Santago Arroyave-Tobon, Jean-Marc Linares2, Pierre Moretto1

1 Centre de Recherches sur la Cognition Animale - Centre de Biologie Intégrative, Toulouse, France

2 Aix Marseille University, CNRS, ISM, Marseille, France.

Insects are known to show a high variety of locomotor patterns. Although hexapody is certainly a key for this diversity, it is also often assumed that this could be due to the properties of their musculoskeletal system. Yet, the link between the kinematics of insect locomotion and the biomechanical properties of their muscles and exoskeleton has rarely been investigated. Using the seed harvesting ant Messor barbarus, we are currently developing a simulation model with the software OpenSim. First, we built a polyarticulated model of an ant, integrating the organization of its exoskeleton, as well as the different types of joints between its segments and muscle groups identified by the cross-checking of images obtained from histology and microtomography. We then enriched this model with the 3D kinematics data obtained by filming walking ants with 5 high speed HD video cameras and by tracking 47 control points at strategic locations on their body with the motion analysis software Vicon motus. The model will be used to generate realistic simulations to estimate the forces and constraints developed by the muscles and joints of an ant during free locomotion. It will also allow us to make the mechanical link between the internal and external structures of ant exoskeleton in different conditions in order to lay the foundations for the building of a biomimetic exoskeleton that could be used in hexapod robots.

 

Morphological correlates of dispersal capacities in the yellow-legged hornet

Mathilde Lacombrade 1,2,3, Cristian Pasquaretta1, Juliette Poidatz2, Albéric Germain4, Tamara Gomez-Moracho1, Antoine Wystrach1, Denis Thiéry2, Mathieu Lihoreau1

1 Centre de Recherches sur la Cognition Animale (CRCA), Centre de Biologie Intégrative (CBI) ; CNRS, University Paul Sabatier, Toulouse, France

2 Santé et Agroécologie du Vignoble, INRAe, ISVV, Villenave d’Ornon, France

3 M2i Biocontrol, Parnac, France

4 Inserm, Toulouse, France

Invasive species can spread very fastly in their novel environment through various evolutionary processes. Since its accidental introduction in France, the Asian hornet, a major predator of bees, colonised seven countries in just 15 years. Understanding the mechanisms underlying this fast expansion is essential to predict and control its invasion of new territories. Here we tested the spatial sorting hypothesis – a cumulative process in which assortative mating by fast-dispersing individuals at the invasion front produce offsprings with higher dispersal capacities than at the introduction area. We investigated whether hornet queens at the invasion fronts carry more dispersal traits than in the introduction area. We mesured and compared 2000 queens collected in four countries by citizen volunteers betwen 2017 and 2020. Our first results show differences in wing shape : hornets at the invasion front have thinner and longer wings than at the introduction area, which could be beneficial for dispersal. Differences in wing shape between hornets at the different invasion fronts also indicate climatic or demographical influences on phenotypes. If the spatial sorting phenomenon is confirmed, we predict that the invasion will continue to accelerate.

 

The evolution of trap-jaw mandibles in Strumigenys ants

Evan P. Economo1

1Okinawa Institute of Science and Technology

Understanding how selection on a system of interacting parts results in the breakthrough of a new functional design is a fundamental question in evolutionary biology.  Many ant species of the hyperdiverse genus Strumigenys have mandibles with a latch-spring mechanism capable of ultrafast speeds.  Relative to typical ant mandibles, parts of the system have acquired new roles as the functional design of the system is remodeled.  In this talk I discuss recent research investigating the diversity and evolutionary origins of this system.  We reconstructed a phylogeny of 470 species, and analyzed the mandibles of representative taxa with x-ray microtomography and high-speed videography.  We found that the trap mechanism evolved 7-10 times independently in different parts of the world, and a similar resulting design and performance of the mandible was reached each time.  Furthermore, we identified an anatomical pathway of intermediate forms that sheds light on how the trap mechanism evolved from simpler ancestors.  I will also discuss ongoing work probing the genomic and developmental basis for this stunning case of convergent evolution.

 

Multiple ways to miniaturize: ecology and behaviour dictate space allocation inside the thorax of minute ants.

Adam Khalife1 & Evan P. Economo2

1Institut d’Écologie et des Sciences de l’Environnement, Sorbonne Université, CNRS,  Paris, France

2Biodiversity and Biocomplexity Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa, Japan

Ants are the most diverse social insects and can be found in all terrestrial ecosystems. A main driver to ant species diversification is worker miniaturisation. However, ants at the lower size limit face major challenges. Their thorax must accommodate 1) the nervous, digestive and exocrine system and 2) multiple muscles that articulate the head, the legs and the petiole, conferring to ants their legendary strength. How muscles and organs scale with body size is poorly understood. In addition, size trade-offs inside the thorax could change according to ecological and behavioural traits. Using X-ray computed microtomography (microCT), we compared the internal anatomy of Carebara perpusilla, one of the world’s smallest ant that lives underground, to Melissotarsus sp., a larger but still minute ant that lives below the bark of trees. These two species are closely related, and a third relative, Tetramorium fhg046, was used as a reference non-minute ant. We compared the relative volume of the nervous system and the head, leg and petiole muscles. Observed proportions were linked to ecology and behaviour rather than body size alone. We suggest that minute ants can miniaturise in many ways according to their diet and lifestyle.

 

The evolution of forward jumps in ants

Lazzat Aibekova1, Roberto Keller2, Julian Katzke1, Ajay Narendra3, Francisco Hita Garcia1, Evan P. Economo1

1Biodiversity and Biocomplexity Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa, Japan

2Universidade de Lisboa Faculdade de Ciencias, Lisbon, Portugal

3Department of Biological Sciences, Macquarie University, Sydney, Australia

One rare specialization in the evolution of worker ant locomotion is the ability to jump. Forward jumping behavior independently evolved within four distantly related genera. Previous studies have shown that jumping ants employ different jumping techniques: Harpegnathos uses its middle legs to propel forward; Gigantiops and Myrmecia use both the middle and hind legs, and Gigantiops additionally rotates its gaster to thrust. Employing different techniques to perform the same function might indicate that each species uses different morphological adaptations to facilitate the jump. Previous studies on ants focused on the mechanisms and kinematics of jumping, however, no study has yet identified modifications for jumping in the skeletomuscular system. To understand the underlying cause of the jumping ability in ants, morphological patterns linked with forward leaping was compared with structural features in ecologically generalized ants. The low acceleration achieved by Harpegnathos and Gigantiops indicates that there is less reliance on the biomechanical properties of cuticle, and instead rely more on muscular contractions. The comparison of muscle volumes showed that the relative volume of the trochanter depressor muscle (scm6) of middle and hind legs are 3-5 times bigger in jumping ants than those of closely related non-jumping species. One more muscle that seem to be enlarged in some jumping ants compared to non-jumping ants is the coxal remotor muscle (scm3). In O. rixosus scm3 of both middle and hindlegs are around 1.5 times bigger than in O. kuroiwae. While in H. saltator, scm3 of middle leg is 10 times bigger than in E. sikorae. This can be explained by the jumping technique of this genus, which primarily uses the middle legs to lift-off, while Gigantiops uses both the middle and hind legs. My results suggest that different morphological modifications can indeed explain the observed variation in jumping technique.

 

Brain plasticity and behavioural specialisation in the jataí stingless bee (Tetragonisca angustula)

Lohan Valadares a,1, Bruno Gusmão Vieiraa,2, Fabio Santos Nascimentob,2, Jean-Christophe Sandozb,1

(a) shared co-first authorship

(b) shared senior authorship

(1) Laboratory Evolution Genome Behavior and Ecology, CNRS, Gif-sur-Yvette, France

(2) Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil

Social insects are excellent models for understanding the association between brain relative investment and behavioural variability, because they possess a relatively simple nervous system associated with a large range of complex behaviours. For instance, in the stingless bee Tetragonisca angustula, the dynamics of colony defence are based on age differences among soldiers that allow behavioural specialisation: younger soldiers perform hovering flights (hovering soldiers) around the nest entrance for interception of heterospecific intruders while older soldiers stand at the nest entrance (standing soldiers) for preventing the entry of conspecific intruders. Here, we compared the volume of distinct brain regions across individuals of both classes aiming to investigate the association between behavioural specialisation and brain morphology. We found that brain size is significantly smaller in standing soldiers due a reduction in the volume of the optic lobes as individuals switch from a task relying mostly on vison (hovering) to standing at the nest entrance. Thus, we show that behavioural specialisation and consequently processing of different input stimuli (vision for hovering soldiers and olfaction for standing soldiers) are powerful forces shaping the size of brain regions in social insects.

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