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Using examples of insect-plant interactions, I will show how biomechanical research can provide important insights into ecological and evolutionary questions. Insect-plant interactions must always be studied at least partially in the field, as essential aspects of their biology can be overlooked in the laboratory. Biomechanical factors play an important role in many insect-plant interactions such as pollination, herbivory and plant carnivory. Similar to the effects of plant chemical compounds or optical cues, plants can use mechanical ways to manipulate insect behaviour. For example, rockroses can mechanically detect visiting insects and guide pollinators to as yet unpollinated flowers, hollyhocks deploy slippery petals to guide insects to the fertile flower parts, and some pitcher plants have developed climbing barriers that prevent insects from walking around the pitcher to direct them to the slippery trapping surfaces. Again analogous to chemical factors in interactions, biomechanical factors can lead to adaptations and counter-adaptations, with far-reaching ecological and evolutionary consequences. The complexity of biological effects resulting from biomechanical factors is illustrated by Macaranga ant-plant mutualisms, where &#39;wax barriers&#39; and &#39;wax-running&#39; ants have triggered a whole range of secondary secondary ant and plant adaptive traits, including the presentation of food, epidermis longevity, the presence of preformed entrance holes, and ant colony density and aggressiveness. &#39;Mechanical ecology&#39; – the study of organisms in their natural habitat with a biomechanical perspective - is not only important to elucidate adaptations of organisms, but also allows a broader search for new phenomena and organisms that could serve as inspiration for biomimetics.

SEB Conference 2022

Mechanical ecology of insect-plant interactions

Using examples of insect-plant interactions, I will show how biomechanical research can provide important insights into ecological and evolutionary questions. Insect-plant interactions must always be studied at least partially in the field, as essential aspects of their biology can be overlooked in the laboratory. Biomechanical factors play an important role in many insect-plant interactions such as pollination, herbivory and plant carnivory. Similar to the effects of plant chemical compounds or optical cues, plants can use mechanical ways to manipulate insect behaviour. For example, rockroses can mechanically detect visiting insects and guide pollinators to as yet unpollinated flowers, hollyhocks deploy slippery petals to guide insects to the fertile flower parts, and some pitcher plants have developed climbing barriers that prevent insects from walking around the pitcher to direct them to the slippery trapping surfaces. Again analogous to chemical factors in interactions, biomechanical factors can lead to adaptations and counter-adaptations, with far-reaching ecological and evolutionary consequences. The complexity of biological effects resulting from biomechanical factors is illustrated by Macaranga ant-plant mutualisms, where 'wax barriers' and 'wax-running' ants have triggered a whole range of secondary secondary ant and plant adaptive traits, including the presentation of food, epidermis longevity, the presence of preformed entrance holes, and ant colony density and aggressiveness. 'Mechanical ecology' – the study of organisms in their natural habitat with a biomechanical perspective - is not only important to elucidate adaptations of organisms, but also allows a broader search for new phenomena and organisms that could serve as inspiration for biomimetics.

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2022 will find over 1500 experimental biologists from across the globe converging on the third-largest French city near the Mediterranean coast and the fastest-growing city in the country over the past 25 years.
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2022 found over 1500 experimental biologists from across the globe converging on the third-largest French city near the Mediterranean coast and the fastest-growing city in the country over the past 25 years - Montpellier, France.

Plants consist of over 80% of water, but unlike water, many plant secretions have non-Newtonian, viscoelastic properties. Examples are the trap fluids of many tropical pitcher plants (Nepenthes), where viscoelasticity has been shown to aid prey capture and retention. Measuring the viscoelasticity of pitcher fluids accurately requires in situ rheometry, in the tropical field locations where these plants grow, because the fluid properties degrade rapidly in storage. With an interdisciplinary team of biologists and engineers, we designed a portable extensional rheometer that weighs less than 1kg and can be dismantled into parts for easy transport. We used this device to characterize trap fluids of two pitcher plant species: N. rafflesiana in Brunei, Northern Borneo, and N. pervillei in the Seychelles. Viscoelastic behaviour, quantified as the relaxation time after rapid stretching of a small quantity of fluid, appeared relatively late during trap development (before opening), and dropped off sharply around two to three weeks after trap opening. Our results show that fluid properties are highly dynamic over the lifespan of a pitcher trap, with times of maximum fluid viscoelasticity coinciding with times of high attractiveness and prey capture efficiency.

A portable field rheometer reveals age-dependent changes of viscoelastic trap fluids in carnivorous plants

Animal closing forces such as bite and pinch forces may determine access to food and mates and are therefore important performance metrics related to fitness. However, despite the diversity and ecological importance of smaller animals such as many crustaceans and insects, knowledge on the predictors and evolution of closing forces in these taxa is extremely scarce. Here we present a mobile and light-weight closing force measurement setup that is tailored to measure closing forces of a wide range of animals, especially smaller taxa, and an R package for analysing the measurements. During a measurement, in vivo closing forces are converted to an electrical signal by a highly sensitive piezoelectric force transducer. The transducer is housed in a setup that can be manufactured with a 3D printer and generic parts, and the electric signal is amplified by a custom charge amplifier. The R package automatically extracts maximum force values and individual force curves for further curve shape analyses. The shape of these curves may yield information on the underlying biomechanics, physiology, and behaviour during biting/pinching, and has only rarely been studied. We think that the new measurement setup, its ease of use, reproducible components, and fast assembly will enable rapid force measurements in the field and in the lab. In combination with the R package, it will facilitate research on the micro- and macroevolution of animal closing forces in a wide range of taxa, especially in smaller vertebrates and the megadiverse arthropods.

Measuring and analysing animal closing forces: a mobile setup and new R package

The passion flower Passiflora discophora is a climbing plant that attaches to its substrate by means of adhesive pads, which are located at the distal end of branched tendrils. At the beginning of this process, a circumnutation motion is performed, which serves to locate a host substrate in 3D-space. Once the tips of the tendril are in contact with the substrate, callus-like growth is induced, causing the pads to develop. After the pads become firmly attached to the support, the main axis of the tendril winds up into a coil and thereby shortens. Here we investigate the change in mechanical properties of these spring-like structures during their ontogeny by performing tensional tests on individual tendrils in different ontogenetic stages. As the tendrils from any individual stem are at different stages of their respective ontogeny, depending on their location along the stem, the quality of the stem's attachment changes from its apical end (turgescent tendrils) to its basal end (senescent tendrils). Furthermore, we show for the first time in situ the forces generated during the spiralling of the tendrils.

How the mechanical properties of Passiflora discophoras sping-like tendrils change over time

Monocotyledons comprise about one-quarter of all flowering plants, colonize all bio-geographical and climatic regions of the planet and reveal a striking growth form diversity ranging from tiny swimming to large arborescent species. This growth form diversity is based on a rigid fibrous vascular network embedded into a viscoelastic parenchyma matrix and is established and limited by primary vascular growth. Only few monocot genera, all belonging to the Asparagales, are able to modify their tissue structure via secondary thickening growth. Despite the limitations on tissue level, monocots evolved diverse mechanical properties, that are based on their fiber reinforced bauplan such as very stiff bamboo culms or highly compliant pulvini. However, the mechanical architecture of monocots, and here especially the nodus, remain relatively unexplored, despite the fact that it is the crucial connecting element between internodes and laterals. Here I present how biomechanical experiments and 3D imaging using µCT and MRI techniques as well as plant specific image optimization techniques help to unravel structural design patterns in monocots. 

Structural diversity and biomechanics in monocots

Escape is a life critical defensive behaviour. Some animals, such as click beetles, escape using ultrafast movements produced by power amplification systems. Similarly, Astraeus jewel beetles flick themselves into the air by rapidly opening their hardened forewings (elytra). This behaviour has not been observed in other animals, and the mechanism and kinematics remain a mystery. Here, we combine high-speed videos, SEM images, and micro-CT data to describe the kinematics of the behaviour and identify potential associated structures. Initial data indicates the elytra open at speeds up to 53 m/s, comparable to other known ultrafast movements in insects. Such speeds cannot be achieved by muscles alone, indicating that the behaviour is likely produced by a latch mediated spring actuated (LaMSA) system. We also conducted a behavioural experiment to demonstrate that jewel beetles can flick at much lower body temperatures (~15°C) than required for walking (~30°C) or flying (~37°C). This indicates that the behaviour could be a particularly important escape strategy at low ambient temperatures. Taken together, we reveal a unique, power-amplified, fast movement and showed the potential adaptive values of this defensive behaviour.

Bug off: biomechanics underlying the defensive flicking behaviour of Astraeus jewel beetles

Restricted gene flow has resulted in extensive population differentiation and adaptation to local environments in the tide pool copepod Tigriopus californicus. This differentiation has also set the stage for extensive coadaptation between nuclear and mitochondrial genomes, a form of intrinsic adaptation common to all eukaryotes. The extent of coadaptation is revealed in studies of interpopulation hybrids. There is significant variation in fitness among hybrids attributable to inter-individual variation in genomic composition. Using development time as a proxy for fitness, we previously found that the mtDNA haplotype had a profound effect on the fitness of alleles across the nuclear genome of F2 hybrids. These effects were apparently mediated by mitochondrial performance and correlated with the degree of match or mismatch between mtDNA and nuclear alleles derived from the same parental population. Here we attempt to extend this work in two ways: 1) using RNA-seq on developing F2 larvae to examine relationships between gene expression and larval developmental rates, and 2) using 14+ generations of interpopulation crossing to breakdown linkage disequilibrium to better localize genomic regions involved in mitonuclear coadaption. RNA-seq results suggest the several nuclear-encoded subunits of electron transport system complexes (especially Complex 1) are upregulated in fast developers, and genes involved in ROS metabolism are also differentially expressed. Selection for developmental rate in advanced generation hybrids was largely ineffective, producing no consistent change in mitochondrial performance or developmental rate; still allelic frequencies on parts of chromosomes 2 and 3 responded to selection, genomic regions previously identified in the F2 studies.

The environment within: selective effects of mitonuclear interactions

Developmental programming is a major source of inter-individual variation that can tailor phenotypes to environmental conditions, including thermal conditions. While the underlying mechanisms of developmental plasticity are mostly unknown, there is growing evidence for the involvement of mitochondria in this process. Here, we investigate whether prenatal sound – increasingly recognised as an essential source of information for embryos – can program mitochondrial metabolism. In the arid-adapted zebra finch, prenatal exposure to “heat-calls”, produced by parents incubating at high temperatures, adaptively alters nestling growth in the heat. To test whether mitochondrial programming underlies this adaptive pattern, we measured red blood cell mitochondrial function in nestlings, exposed prenatally to either heat-calls or control-calls, and reared in contrasting thermal environments post-hatch. Exposure to high temperatures always reduced mitochondrial ATP production efficiency. However, as expected to reduce heat production and improve growth, prenatal exposure to heat-calls improved mitochondrial efficiency under mild heat conditions. By contrast, when exposed to an acute heat-challenge, LEAK respiration was higher in heat-call nestlings. Consistent with its role in reducing oxidative damage, LEAK under extreme heat was also higher in fast growing nestlings. These changes in mitochondrial function are consistent with the differential growth pattern induced by prenatal heat-calls. Our study therefore provides the first demonstration of mitochondrial acoustic sensitivity, and brings us closer to understanding the underpinning of acoustic developmental programming and avian strategies for heat adaptation.

Prenatal acoustic programming of mitochondrial function for high temperatures in an arid-adapted bird

While hypoxia (i.e. low dissolved oxygen level in water) events occur naturally, global change and human activities have exacerbated their strength and temporal fluctuations. As populations may not be able to escape the hypoxic conditions, especially in freshwater ponds, it is crucial to understand how organisms can adjust and adapt to these fluctuating environments. When directly exposed, individuals may be able to adjust their phenotypes through plasticity, but continued exposure to hypoxia over generations may require adaptation and evolution. As the mitochondrial metabolism is the key component that fuel aerobic functions, the individual capacity to respond to the environmental change in oxygen availability is likely to rely on mitochondrial functions. Using two populations of wild three-spined sticklebacks (Gasterosteus aculeatus) exposed to different levels of hypoxia conditions in their natural habitats and experimentally exposed to fluctuating hypoxia (20% air saturation during the night and 100% during the day), we investigated the fish metabolic plastic and evolutionary response.  We showed adaptation in fish growth and metabolic rate, fish exposed to hypoxia in their natural habitats possessing higher metabolic capacity, but limited evidence for plasticity to the experimental conditions. These responses were supported by the muscle mitochondrial metabolism, for which similar adaptation were observed. However, no differences were observed in the brain mitochondrial metabolism, suggesting tissue specific response to environmental changes. Overall, these results highlight the capacity of fish to adapt environmental changes across generations, relying on mitochondrial adaptation.

Fish metabolic response to freshwater hypoxia: plasticity and adaptation

Antarctic fish of the suborder Notothenioidei display remarkable metabolic adaptations to life in the Southern Ocean. These comprise very low, energy saving metabolic rates, higher mitochondrial densities, cold adapted enzymes, anti-freeze proteins and last but not least, the loss of hemoglobin in the icefishes (family Channichthyidae). Yet, those adaptations come at a premium and render Antarctic notothenioids especially vulnerable to a warming ocean. As the central players in aerobic energy metabolism, mitochondria and their acclimatory plasticity play an important role in buffering the effects of climate change and much depends on their thermal stability and acclimatory capacity. 
I will present an overview of recent studies on notothenioid mitochondrial and whole animal respiration under acute and chronic thermal exposure and explore the differences in thermal reaction norms, leak rates and thermal stability of the individual respiratory complexes in Antarctic nototheniids (N. rossii, N. coriiceps), trematomids (T. eulepidotus, T. loennbergii) and the haemoglobin-less channichthyids (C. hamatus, C. wilsoni).




Acclimation capacity and thermal sensitivity of notothenioid energy metabolism

Seedling de-etiolation involves massive change in genome expression, many light-responsive genes undergoing pioneering rounds of transcription within minutes. In previous studies we reported that Arabidopsis photomorphogenesis indeed associates with a ~3-fold increase of global RNA Polymerase II elongation activity in most cotyledon nuclei (1), which, together with more recent studies (2), suggests that light induces a switch from a relatively quiescent to a more active transcriptional status during the transition. Studies from others and us focusing on nuclear and chromatin dynamics also unveiled that de-etiolation involves genome-wide variations nuclear architecture and in chromatin hallmarks of transcription elongation status at thousands' protein-coding genes (1, 3-4), which are controlled by DET1 and other light signaling components (3). Yet, because of data normalization practices, the functional consequences of these multilevel adaptations of the chromatin status to an elevated transcriptional regime are not observed when analyzing transcriptomic profiles obtained with classical microarray or RNA-seq analyses. We therefore developed a new methodological setup enabling an absolute quantification of RNA-seq data to explore the functional impact of transcription intensification on gene expression. We will present how this approach can be used to assess to which extent, and for which genes, a global increase of RNA Pol 2 activity is reflected at the transcript level during photomorphogenesis. This new standpoint should help revisiting how signaling paths and chromatin machineries modulate plant genome expression in response to the environment.

References:
1- Bourbousse et al, PNAS (2015) 112(21) e2836-44
2- Godoy Herz, et al. Mol Cell (2019) PMID: 30661982
3- Nassrallah, Rougee et al, eLife (2018) e37892
4- Charron et al, Plant Cell (2009) 21:3732-48

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