Journal of Experimental Biology

Jakubowski, Kristen L.; Ludvig, Daniel; Perreault, Eric J.; Lee, Sabrina S. M.

doi: 10.1242/jeb.244863pmid: 37350252

Regulating ankle mechanics is essential for controlled interactions with the environment and rejecting unexpected disturbances. Ankle mechanics can be quantified by impedance, the dynamic relationship between an imposed displacement and the torque generated in response. Ankle impedance in the sagittal plane depends strongly on the triceps surae and Achilles tendon, but their relative contributions remain unknown. It is commonly assumed that ankle impedance is controlled by changing muscle activation and, thereby, muscle impedance, but this ignores that tendon impedance also changes with activation-induced loading. Thus, we sought to determine the relative contributions from the triceps surae and Achilles tendon during conditions relevant to postural control. We used a novel technique that combines B-mode ultrasound imaging with joint-level perturbations to quantify ankle, muscle and tendon impedance simultaneously across activation levels from 0% to 30% of maximum voluntary contraction. We found that muscle and tendon stiffness, the static component of impedance, increased with voluntary plantarflexion contractions, but that muscle stiffness exceeded tendon stiffness at very low loads (21±7 N). Above these loads, corresponding to 1.3% of maximal strength for an average participant in our study, ankle stiffness was determined predominately by Achilles tendon stiffness. At approximately 20% MVC for an average participant, ankle stiffness was 4 times more sensitive to changes in tendon stiffness than to changes in muscle stiffness. We provide the first empirical evidence demonstrating that the nervous system, through changes in muscle activations, leverages the non-linear properties of the Achilles tendon to increase ankle stiffness during postural conditions.

Knight, Kathryn

doi: 10.1242/jeb.246347pmid: N/A

View largeDownload slide A tobacco hornworm (Manduca sexta). Photo credit: Shelley Adamo. View largeDownload slide A tobacco hornworm (Manduca sexta). Photo credit: Shelley Adamo. Multi-tasking is in all parts of our lives, from fiddling with phones when walking to managing homelife and careers, but we didn't invent priority juggling. Shelley Adamo from Dalhousie University, Canada, explains that seemingly unrelated tissues can multi-task, playing pivotal roles in apparently unconnected situations. For example, the immune system of insects requires large injections of glucose when fighting an infection, but much of the essential fuel comes from an unexpected source: muscle. So how much of a toll does warding off illness take on the muscles of insects, which the creatures depend on for protection and movement? For example, when under attack, tobacco hornworms – the caterpillars of tobacco hawkmoths (Manduca sexta) – thrash from side to side. Might fighting an infection weaken the caterpillars’ muscles and their ability to stand up for themselves? Adamo and Laura McMillan, with a team of graduate students and undergraduate helpers (all from Dalhousie University), decided to find out whether mounting an immune response impacts tobacco hornworm muscles. Knowing that, in insects, infection triggers the release of immune proteins and other compounds from an organ known as the fat body (the insect equivalent of the liver), the team set out to discover whether some of the key genes involved in the infection fighting machine are switched on in muscle when tobacco hornworms suffer an infection. The team injected the caterpillars with a cocktail of dead fungus and bacteria – to trick the insects into trying to fend off an infection without making them ill – to find out what they did. Sure enough, these key genes were activated in the caterpillar muscle after the fake infection, so the muscles do contribute to the infection response. And when the team took a closer look, the muscles also showed activation of the genes encoding infection-fighting molecules that contributed to their protection. But can muscle also liberate glucose from its glycogen stores, releasing it into the insect's blood to fuel the fight? This time, the team collected the caterpillars’ muscles after injection of the pathogen cocktail and, sure enough, the amount of glycogen stored in the muscle, ready to be converted into glucose, fell significantly. The caterpillars appeared to be releasing glycogen from their muscles to fight the simulated infection. And, when the team tricked healthy caterpillars into thinking that they were being attacked by a bird, using tweezers, the insect's muscle glycogen levels crashed as they fought back. However, when they tested how much glycogen the fake-infected insects released from muscle when under attack, it was less than when the insect was fighting an infection alone, as though the muscle was holding back some of its glycogen from combating the infection in the hope of improving its strength to fend off predators (which don't hold back just because their prey is poorly). The team then checked how strong the insects were having received the mock infection by tricking them again into defending themselves against a tweezer attack. The insects that had been exposed to the fake infection were physically weaker after being pecked with tweezers and less able to fend off parasitic wasps that wanted to lay eggs on their luscious bodies. So, tobacco hornworms pay a price for co-opting their muscles to fend off infection. While they benefit from the boost to their immune response provided by glycogen from muscle, this takes a toll on the caterpillar's ability to defend itself from physical attack. This inability to defend themselves is an unintended consequence of fighting infection, when multitasking muscle steps in to provide support. Adamo , S. A., Corkum , E., Kim , J., Lee , T. M., Miller , D. W., Song , S., Wright , C., Zacher , I. D., Zbarsky , J. S. and McMillan , L. E. ( 2023 ). Muscle in the caterpillar Manduca sexta responds to an immune challenge, but at a cost, suggesting a physiological trade-off . J. Exp. Biol. 226 , jeb245861 . https://doi.org/10.1242/jeb.245861 Google Scholar Crossref Search ADS PubMed © 2023. Published by The Company of Biologists Ltd 2023

Roche, Dominique G.; Tytell, Eric D.; Domenici, Paolo

doi: 10.1242/jeb.245686pmid: 37493068

Work carried out since the late 1970s has provided key insights into the comparative biomechanics, kinematics, behaviour and neurobiology of fish escape responses. An escape response is an ecologically important behaviour used by fishes to evade predation and aggression via rapid swimming movements. With environmental change expected to affect the physiology and biomechanics of aquatic ectotherms, there is a growing interest in understanding how environmental stressors affect the swimming performance and behaviour of fishes during escape responses, particularly in the context of predator–prey interactions. As the study of fish swimming continues to expand, there have been repeated calls to standardise experiments and reporting practices to facilitate integrative and comparative studies. Here, we provide a set of practical guidelines for conducting, analysing and reporting experiments on escape responses in fish, including a reporting checklist to assist authors undertaking these experiments. These resources will facilitate executing and reporting escape response experiments in a rigorous and transparent fashion, helping to advance the study of fish swimming in an era of rapid environmental change.

Hoffmann, Ary A.; Sgrò, Carla M.; van Heerwaarden, Belinda

doi: 10.1242/jeb.245749pmid: 37475600

A (quite) large set of experiments has been undertaken to assess the potential for evolutionary changes in invertebrates under current and future climate change conditions. These experimental studies have established some key principles that could affect climate change adaptation, yet there remain substantial obstacles in reaching a meaningful predictive framework. This Review starts with exploring some of the traits considered in individuals and approaches used in assessing evolutionary adaptation relevant to climate, and some of the core findings and their substantial limitations, with a focus on Drosophila. We interpret results in terms of adaptive limits based on population processes versus fundamental mechanistic limits of organisms. We then consider the challenges in moving towards a predictive framework and implications of the findings obtained to date, while also emphasizing the current limited context and the need to broaden it if links to changes in natural populations are to be realized.

Allen, Joshua M.; Hodinka, Brett L.; Barbera, Raven A.; Desjardin, Genavieve C.; Williams, Tony D.

doi: 10.1242/jeb.245974pmid: 37387253

Despite the potential for temporally dependent relationships between trait values and fitness (e.g. as juveniles approach life-stage transitions such as fledging), how developmental stage affects canalization (a measure of robustness to environmental variation) of morphological and physiological traits is rarely considered. To test the sensitivity of morphological and physiological traits to environmental variation in two developmental stages, we manipulated brood size at hatch in European starlings (Sturnus vulgaris) and cross-fostered chicks between enlarged and reduced broods approaching fledging. We measured body size (mass, tarsus, wing length) and physiological state (aerobic capacity, oxidative status) at asymptotic mass on day 15, then cross-fostered chicks between ‘high’ and ‘low’ quality environments and assessed the same traits again on day 20, after 5 days of pre-fledging mass recession. Chicks in reduced broods were heavier at asymptotic mass and had lower reactive oxygen metabolites than enlarged broods, whereas structural size, aerobic capacity and antioxidant capacity were unaffected by experimental brood size. The observed canalization of structural and physiological traits during early development was maintained after cross-fostering, during late development. However, in contrast to early development, antioxidant capacity approaching fledging appeared sensitive to environmental conditions, as trajectories varied by cross-fostering treatment. Elevated reactive oxygen metabolites observed after early development in enlarged brood chicks were maintained after cross-fostering, suggesting that canalized development in low-quality environments could produce oxidative costs that carry over between life stages, even when conditions improve. These data reveal trait-specific relationships between environmental conditions and development, and highlight how natal environment effects may vary by developmental stage.

French, Susannah S.; Demas, Gregory E.; Lopes, Patricia C.

doi: 10.1242/jeb.245858pmid: 37458064

Historically, the fields of ecoimmunology, psychoneuroimmunology and disease ecology have taken complementary yet disparate theoretical and experimental approaches, despite sharing critical common themes. Researchers in these areas have largely worked independently of one another to understand mechanistic immunological responses, organismal level immune performance, behavioral changes, and host and parasite/disease population dynamics, with few bridges across disciplines. Although efforts to strengthen and expand these bridges have been called for (and occasionally heeded) over the last decade, more integrative studies are only now beginning to emerge, with critical gaps remaining. Here, we briefly discuss the origins of these key fields, and their current state of integration, while highlighting several critical directions that we suggest will strengthen their connections into the future. Specifically, we highlight three key research areas that provide collaborative opportunities for integrative investigation across multiple levels of biological organization, from mechanisms to ecosystems: (1) parental effects of immunity, (2) microbiome and immune function and (3) sickness behaviors. By building new bridges among these fields, and strengthening existing ones, a truly integrative approach to understanding the role of host immunity on individual and community fitness is within our grasp.

Lakhiani, Rhea; Shanavas, Sahana; Melnattur, Krishna

doi: 10.1242/jeb.245677pmid: 37489524

Sleep is a familiar, periodic occurrence in our lives. Despite its place in everyday experience, the existence of this suspended state of consciousness has intrigued and puzzled philosophers and scientists for decades. For much of its history, sleep science has focused on humans and mammals. In contrast, in the last 20 years or so, it has become increasingly clear that sleep is essentially universal. Sleep states have been observed in animals from mammals to cnidaria. Here, we review recent progress in sleep science through the lens of comparative physiology. We highlight broad insights into sleep phenomenology, physiology and function that have come from this comparative approach. These include the plasticity of sleep in response to environmental challenges and ecological niches, the discovery of distinct sleep stages in diverse taxa and conserved functions of sleep. Indeed, we argue, a comparative approach is essential to any comprehensive account of sleep.

Tresguerres, Martin; Kwan, Garfield T.; Weinrauch, Alyssa

doi: 10.1242/jeb.245747pmid: N/A

The regulation of ionic, osmotic and acid–base (IOAB) conditions in biological fluids is among the most fundamental functions in all organisms; being surrounded by water uniquely shapes the IOAB regulatory strategies of water-breathing animals. Throughout its centennial history, Journal of Experimental Biology has established itself as a premier venue for publication of comparative, environmental and evolutionary studies on IOAB regulation. This Review provides a synopsis of IOAB regulation in aquatic animals, some of the most significant research milestones in the field, and evolving views about the underlying cellular mechanisms and their evolutionary implications. It also identifies promising areas for future research and proposes ideas for enhancing the impact of aquatic IOAB research.

Lechantre, Amandine; Martinet, Baptiste; Thévenet, Véronique; Souramasing, Oune-Saysavanh; Bico, José; Abou, Bérengère

doi: 10.1242/jeb.245894pmid: 37387691

Viscosity, which impacts the rate of haemolymph circulation and heat transfer, is one of the transport properties that affects the performance of an insect. Measuring the viscosity of insect fluids is challenging because of the small amount available per specimen. Using particle tracking microrheology, which is well suited to characterise the rheology of the fluid part of the haemolymph, we studied the plasma viscosity in the bumblebee Bombus terrestris. In a sealed geometry, the viscosity exhibits an Arrhenius dependence with temperature, with an activation energy comparable to that previously estimated in hornworm larvae. In an open to air geometry, it increases by 4–5 orders of magnitude during evaporation. Evaporation times are temperature dependent and longer than typical insect haemolymph coagulation times. Unlike standard bulk rheology, microrheology can be applied to even smaller insects, paving the way to characterise biological fluids such as pheromones, pad secretions or cuticular layers.

Prazdnikov, Denis V.; Shkil, Fedor N.

doi: 10.1242/jeb.245710pmid: 37357638

Neotropical cichlids demonstrate an enormous diversity of pigment patterns, a morphological trait that plays an important role in adaptation and speciation. It has been suggested that alterations of the activity of the thyroid axis, one of the main endocrine axes regulating fish ontogeny, are involved in the development and diversification of pigment patterns in Neotropical cichlids. To test this hypothesis, we assessed thyroid hormone developmental dynamics and pigment patterning, and experimentally induced hyperthyroidism and hypothyroidism at different developmental stages in the convict cichlid, Amatitlania nigrofasciata, and blue-eye cichlid, Cryptoheros spilurus. We found that the two species display a similar type of coloration development and similar reactions to changes of thyroid hormone level, but species-specific differences in hormonal dynamics and thyroid hormone responsiveness. These findings indicate that thyroid hormone is a necessary but not sufficient signal to induce the transition from larval to juvenile coloration, and is a component of a complex, concerted endocrine cascade that drives skin development.