France

Rose chafer beetles (Protetia cuprea) are pollinators as well as agricultural pests, flying between flowers and trees while foraging for pollen and fruits. Calculating the energy they expend on flying during foraging activity faces the challenge of measuring the metabolic rate (MR) of free-flying insects in an open space. We overcame this challenge by using the bolus injection of 13C Na-bicarbonate technique to measure their metabolic energy expenditure while flying in a large flight arena. Concurrently, we tracked the insects with high-speed cameras to extract their flight trajectory, from which we calculated the mechanical power invested in flying for each flight bout. We found that the chemical (metabolic) energy input converted to mechanical flight energy output at a mean efficiency of 10.4 ± 5.2 %, with a trend of increased efficiency in larger conspecifics (efficiency scaled with body mass to the power of 1.4). The transition during summer from a diet of pollen to that of fruits may affect the energy budget available for foraging. Starved P. cuprea, feeding on apples ad libitum, increased their body mass by an average of 6% in two hours. According to our calculations such a meal can power a 630-meter flight (assuming a carbohydrate assimilation efficiency of 90%). The high cost of aerial locomotion is inherent to the foraging behaviour of rose chafers, explaining their short flight bouts followed by prolonged feeding activity. The ability to measure both flight and its energetic cost is crucial for obtaining realistic estimates for the cost of locomotion.

SEB Conference 2022

The metabolic cost of flight and aerobic efficiency in the rose chafer, Protaetia cuprea (Cetoniinae)

technical paper

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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.

Wing morphing during flight expands the performance envelope of flying animals and likely facilitates their ability to adapt to a broad range of habitats and atmospheric conditions. In birds, wing morphing is achieved by coupling a series of flexible and passive individual feathers to active musculoskeletal components. Although the aerodynamic effects of wing shape are relatively well characterised, the changes to the mechanical properties due to the structural rearrangement of feathers and the effects these changes have on flight performance are unknown. We first used dynamic mechanical testing at the base of in situ feathers of pigeons (Columba livia) to characterise the local mechanical properties. Wing folding decreased feather-anchoring tissue stiffness, an effect overcome in the proximal wing by an increase in stiffness via feather-feather interaction. We next applied computational fluid-structural interaction methods to quantify the effect of increasing or decreasing wing stiffness in the context of wing shape. These data revealed that the trends in wing stiffness due to wing folding can enhance lift production. Specifically, folding prevented destructive interference by the aerostructural deformations on flow vortices during high speed gliding flight. In conclusion, this study proposes that the natural coupling in the avian wing structural system between passive flight feathers and active musculoskeletal actuators allows for aerostructural flow control for enhanced flight performance over a variety of flight speeds.

Mechanisms for aerostructural flow control during avian wing morphing

When flying in near ground environments, birds encounter obstacles that force deviations from their flight paths. This raises the question of how they achieve the necessary guidance and control to perform these manoeuvres safely. In a flight arena equipped with a motion capture system, we challenged four Harris' hawks to negotiate a horizontal bar along their flight path between two perches (14 m apart). The unobstructed trajectory of the birds consists of a powered dive followed by glide up to the landing perch. The horizontal bar was positioned halfway between the perches, and was actuated to go through a vertical composite sinusoidal motion. While the minimum height of the bar was such that the typical unobstructed trajectory would not lead to a collision, the perceived risk of collision caused approximately half of the 880 flights to divert over the bar. The likelihood of diverting was primarily affected by the height of the bar and variation in individual preference. In cases where they would pass over the bar, three individuals directed their flight paths towards the bar shortly after take-off. This tracking mechanism, which arises as a risk averse behaviour, guides the birds nearer to the obstacle and thus increases the risk of collision. Obstacles acting as attractors would explain how many birds collide with overhead lines, despite the marginal probability for a random trajectory to encounter them.

Obstacle negotiation in the vertical plane

To produce the aerodynamic forces required for flight, two-winged insects (Diptera) move their wings back and forth at high wingbeat frequencies. Because the angular accelerations of this oscillating wing system scales quadratically with the wing-beat frequency, acceleration-based forces as a result of wing stroke-accelerations are expected to be particularly high for these flying insects. These acceleration-based forces consist of added-mass forces and Wagner-effect-based forces. Added-mass forces are resulting from the acceleration of fluid around the wing, and the Wagner-effect describes the delay in bound circulation build-up in accelerating wings. Here, we used computational fluid dynamics (CFD) simulations to systematically study how both added-mass forces and the Wagner-effect affect aerodynamic force production and airflow dynamics in accelerating insect wings. Based on the simulation results, we developed an aerodynamic model that captures the stroke-acceleration forces based on the wing-beat kinematics and wing morphology. This shows that current added-mass models fail to accurately predict added-mass forces on insect wings, primarily because these semi-empirical models ignore the Wagner-effect. Our novel Wagner-effect model is based on the interaction between stroke-rate and stroke-acceleration, and accurately predicts the delay in Leading-Edge Vortex build-up in accelerating wings as well as the delay in Leading-Edge Vortex reduction in decelerating wings. Finally, we applied our newly-developed aerodynamic model in a quasi-steady approach to the wingbeats of a fruit fly and malaria mosquito. This shows that particularly for high-frequency flapping flyers such as the mosquito, acceleration-based forces contribute substantially to aerodynamic lift and drag production.

Added-mass and Wagner-effect-based forces in high-frequency flapping insect wings

Humans are efficient bipedal walker and runner. Extant non-human primates (NHP) are not habitual bipeds, yet, they occasionally walk bipedally. According to 2D kinematics, they use a typical &quot;bent-hip, bent-knee&quot; posture coupled with a forward-leaning trunk, a limited stride length, a high stride frequency, and knees that remain flexed during the stance phase. No structural specialization is required for them to occasionally walk bipedally and compared to humans, extant NHPs do not exhibit any adaptations for bipedalism. Hence, it is suggested that the origin of a more habitual form of bipedal locomotion emerged from the common pattern observed in NHPs. However, one wonders whether the general lens through which the bipedal gait in NHPs has been described is discriminating enough to identify subtle differences that might exist between species. We conducted a study on the bipedal walking of olive baboons, at the Primatology Station of the CNRS (UAR 846). We provide detailed information on the 3D kinematics of bipedal walking. Our results show that the common pattern of the joint and segment angles can be easily described in the sagittal plan, but specificities related to the baboon model can be described in the frontal plan, such as the adduction of the thigh at touch-down. We compare these results with the 3D kinematics available for chimpanzees, capuchins, macaques and gibbons and identify subtle differences between species. Fundings: IRN-GDRI0870 & HoBiS-ANR-18-CE27-0010-01

3D kinematics of bipedal walking in the olive baboon, Papio anubis: evolutionary implications

It is well established that conditions experienced during prenatal development affect postnatal telomere length and dynamics in humans and laboratory animal models. However, we still know little about how prenatal environmental and social conditions shape telomere dynamics in wild animal populations. In the last years, we have performed several experimental studies to elucidate the role played by maternal glucocorticoids and the exposure to prenatal social stressors (e.g. exposure to predator cues) on postnatal telomere length and dynamics in a long-lived seabird species, the Yellow-legged gull (Larus michahellis). The results of these studies show that in contrast to previously thought, mothers may promote longer telomeres in their offspring by mildly increasing the allocation of glucocorticoids into their eggs (i.e. corticosterone). However, the effect of glucocorticoids hormones seems to differ depending on their intensity, origin and duration. Indeed, when late-stage embryos are repeatedly exposed to predator cues, they show increased secretion of glucocorticoids soon after hatching, an effect that was accompanied by a loss of telomere length during the early postnatal development. Together, our results show that embryos are not passive agents against their developmental environment, as their telomere dynamics are influenced by the maternal phenotype and the social cues they are able to integrate during their development.

Telomeres in the ocean: how pre- and postnatal factors shape telomere dynamics in a colonial long-lived seabird

Recent cross-sectional comparisons of telomere lengths, a hallmark of ageing, suggest that high temperatures may increase the rate of senescence in ectotherms. Telomeres shorten as a result of exposure to ROS produced by the mitochondria. Given that the rate of ROS production varies with mitochondrial efficiency, there may be a link between an individual’s mitochondrial efficiency and its telomere dynamics, which may be more acute at high temperatures. We tested this hypothesis by examining the relationship between telomere length and mitochondrial function from white muscle and liver of brown trout Salmo trutta of similar age and size, fed ad libitum, and acclimated to high-constant (19.5°C), high-variable (19.5 ± 2.5°C, daily cycle), or ideal (12°C) temperature regimes. Fish under high-constant and high-variable temperature regimes had greater higher average rates of telomere attrition, mitochondrial oxygen consumption rates, and ROS release rates along with lower mitochondrial phosphorylation efficiencies when compared to 12°C acclimated fish. However, telomere changes were positively correlated with mitochondrial phosphorylation efficiency in muscle, but not liver, in fish from the high-constant and high-variable temperature regimes: telomeres shortened in the least efficient individuals but increased in length in the most efficient fish. No relationship was observed in fish acclimated to 12°C. Therefore, individual diversity in muscle mitochondrial efficiency seems to cause variation in cellular senescence, where less efficient individuals have a more rapid shortening of telomeres. This may ultimately suggest that less efficient individuals will have shorter lifespans in warming and fluctuating environments.

Lower muscle mitochondrial efficiency results in more rapid shortening of telomeres in ectotherms at high and fluctuating temperatures

Climate change is increasing both the average ambient temperature and the frequency and severity of heat waves. While direct mortality induced by heat waves is increasingly reported, sub-lethal effects are also likely to impact population dynamics and persistence. We hypothesized that accelerated cellular ageing could be a cost of being exposed to higher ambient temperature. We tested this hypothesis in two common European passerine species by experimentally increasing nest box temperature by ca. 2°C during postnatal growth and measuring telomere length as a biomarker of ageing. In great tits, we also estimated the impact on medium-term survival and measured a large set of physiological markers including thyroid hormones, glucocorticoid signaling, oxidative stress, mitochondrial density and telomere maintenance mechanisms. We show that in both species, increasing early-life temperature does not affect growth or survival to fledging, but leads to an acceleration in the shortening of telomeres. In great tits, such shortening of telomeres was not explained by increased oxidative stress levels, but more likely by an increase in energy demand (i.e. higher thyroid hormones levels, increased expression of glucocorticoid receptor, increased mitochondrial density) leading to a reduction in telomere maintenance mechanisms (i.e. decrease in the gene expression of telomerase and protective shelterin). Additionally, medium-term survival was reduced from 34% in control nests to 19% in heated nests. Our results thus suggest that climate warming might affect cellular ageing in wild passerine populations, with potential impact on population dynamics and persistence.

From climate warming to accelerated cellular ageing: insights from two experimental studies in wild passerine birds

Individual variation in telomere length has been linked with health, survival and senescence. Individual variation in telomere length is due to environmental and genetic effects, which can be partitioned into their relative variance components. Estimating the ratio of additive genetic variance to the total phenotypic variance of telomere length, known as the heritability of telomere length, then facilitates understanding of the evolutionary potential of telomere length. However, telomere length heritability estimates vary greatly, and there is a limited understanding of why this is. To fill this knowledge gap, we conducted a systematic review and meta-analysis. We extracted 104 estimates from 43 studies and 18 species to test whether variation in telomere length heritability estimates is due to: phylogeny, species, environmental setting, age at sampling, laboratory methods, statistical methods, and individual repeated measurements. Overall, we found a moderate heritability of 45% (95% CI: 25% – 65%), and significant phylogenetic and species-specific effects, suggesting differential selection pressures on telomere length across taxa. Twin-based and SNP-based estimates were lower than correlation-based or pedigree-based estimates. Furthermore, we detected a publication bias, where small studies with low or non-significant heritability were under-represented. Our results demonstrate an overall heritable basis of telomere length, and the need for careful selection of statistical methods. Specifically, we recommend variance-partitioning methods with relatedness or SNP data over correlation methods to minimize bias. We also recommend future research to expand into a wider range of taxa, and to explore and validate the use of genome-wide correlation data in calculating quantitative genetic metrics.

Heritability of telomere length: a meta-analysis

The disposable soma theory predicts that ageing is a consequence of the investment in reproduction at the expense of self-maintenance. Depending on their pace of life (POL), individuals prioritise either reproduction (fast POL) or self-maintenance (slow POL). A fast POL is associated with a rapid accumulation of physiological damage and early death, and vice versa for a slow POL. To date, especially in vertebrates, it is unclear if physiological damage accumulates uniformly across the entire body, or if there are within-body mosaics of ageing. Here, we quantified telomere length (TL) by TRF in blood, spleen and reproductive tissue in Japanese quail (Coturnix japonica) artificially selected for high (fast POL) or low (slow POL) reproductive investment to test for POL-dependent within-body mosaics of ageing. We found that TL differed across reproductive and non-reproductive tissues in a sex-specific way, but found no indication that these within-body mosaics of TL were affected by an individual’s POL. In females telomeres were longer in oviduct than in blood or spleen, whereas in males TL in testes was not different from TL in non-reproductive tissues, but telomeres in spleen were longer than telomeres in blood. Our study provides evidence for sex-specific within-body mosaic of ageing, which are, however, independent of an individual’s life history strategy.

Do life history strategies affect within-body mosaics of ageing?

Despite ~80% of all animal species undergoing metamorphosis, the effect of this dramatic developmental process on telomere dynamics is unknown. Given that the rate of telomere shortening has been shown in non-metamorphosing species to be influenced by environmental harshness, the question arises as to whether the re-modelling of tissues that occurs during metamorphosis allows an individual to re-set its telomeres and so leave behind this legacy of past environments. This issue is pertinent to amphibians, a group likely to be heavily impacted in the larval stage (i.e., before metamorphosis) by environmental events such as global warming. We will first briefly discuss the current knowledge gaps in the study of amphibian telomeres, then present new data on telomere length across different tissues and developmental stages (from larva to adulthood) in the frog Xenopus laevis. We will also examine the impact of warming conditions before and after metamorphosis on amphibian telomeres and telomerase. Our results show that telomere length is affected not only by the rate of somatic growth, but also by the degree of metamorphic transformation experienced by particular tissues: during metamorphosis, telomere length can either decline, remain stable or dramatically increase. Furthermore, this life history transition seems to be able to buffer the impact on telomeres of harsh conditions in early life. This leads us to suggest directions for future research on telomere dynamics in amphibians and other species with complex-life cycles.

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