France

The vocal repertoire of birds is incredibly diverse. They vocalize using a specific organ, the syrinx, producing a primary vibration at the origin of a primary sound. This sound propagates through the suprasyringeal system, composed of the trachea, the larynx, and the oral cavity. The large volume of this suprasyringeal system, compared to mammals of similar size, suggests that it plays a role in the modulation of the sound initially emitted. To investigate this, we filmed 21 species of dead birds and manipulated them under biplanar X-ray. Markers were implanted in tissues (e.g., on the trachea contour, glottis, beak) to calculate the passive deformations and volume changes of the vocal tract during a range of movements of the neck/head system. Our results show that neck extension and beak closing are associated with an elongation of the trachea of up to 20% of its initial length. We tested the effect of such elongation on sound modulation using computational simulations. Our work shows that the complexity of bird vocalizations is not only related to the syrinx, but also to the entire upper vocal system. This work provides new elements to better understand complex communication, one of the amazing characteristics we share with birds.

SEB Annual Conference 2022

Influence of the avian upper vocal tract on sound modulation

technical paper

Discover the art of creating extraordinary science at SEB’s Annual Conference at Le Corum Conference Center     in Montpellier, France from 5 to  8 July 2022.

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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 - Montpellier, France

Muscle shortening underpins most skeletal motion, and ultimately animal performance. Shortening is usually assumed to be homogenous within a muscle. However, in swimming fish, the whole body deforms like a bending beam: as the vertebral column flexes laterally, muscle shortening increases along a medio-lateral gradient. Recently it has been shown that fish also bend their bodies dorsally during feeding, resulting in dorsoventral shortening gradients in some regions. This suggests these dorsal motions also follow beam-like bending, where the curvature of the vertebral column predicts the linear, dorsoventral shortening gradient in the muscle. We tested this hypothesis by measuring vertebral curvature and dorsal body (epaxial) muscle shortening during feeding motions in rainbow trout (Oncorhynchus mykiss). We used XROMM to measure dorsal and lateral curvature across the anterior vertebral column and used fluoromicrometry to measure shortening between markers throughout the epaxial muscles. Vertebral curvature and muscle marker position were used to predict muscle strain following beam theory. Predicted strains were compared to the measured strains from fluoromicrometry. Trout flexed the anterior vertebrae dorsally and laterally during feeding strikes. When curvature and marker position in both planes were included, the model’s predicted strain matched the measured strain well across most vertebral regions. Our model confirms dorsal flexion during feeding in trout can be modelled with beam theory, even when accompanied by lateral flexion. We find evidence of linear dorsoventral and mediolateral shortening gradients in the epaxial muscles, although it remains to be determined if these reflect shortening of the fibres within these muscles.

Testing the relationship between muscle deformation and vertebral curvature during feeding in rainbow trout (Oncorhynchus mykiss).

Nuclear Pore Complexes (NPCs) are large macromolecular assemblies embedded into the nuclear envelope (NE). They are involved in the selective nucleocytoplasmic transport of macromolecules, chromatin organization, and DNA repair. NPCs are organized into sub-complexes composed of repetitions of about 30 highly conserved nucleoporins (NUPs). The NUP107–160 complex (also known as Y complex) is located in the outer ring and is conserved between distantly related eukaryotes such as yeast and mammals. Here, we are going to focus on two Arabidopsis mutants deficient for this sub-complex: Atnup160 and Atnup96, also known as suppressor of auxin resistance1 (sar1) and sar3, respectively. NUP160 and NUP96 are critical for the nucleocytoplasmic transport of mRNAs and play important functions in auxin signalling, plant growth and flowering time regulation, as well as in immune defence and cold stress tolerance. In the context of our global study about the possible role of NPCs during meiosis (the specialised cell division that leads to gamete formation), we decided to explore the potential function of NUP160 and NUP96 during this cell division because the corresponding mutants show reduced fertility. The results of our study have demonstrated that meiosis is altered in a percentage of the meiocytes from these mutants, which would explain the reduction in the number of seeds. Our observations have revealed that the alteration of the Y complex causes problems in meiotic recombination, the formation of meiotic structures (such as the synaptonemal complex), and viability of the meiocytes. The possible origins of these problems will be discussed.

Exploring the function of components of the Nuclear Pore Complex during meiosis: SAR1 (NUP160) and SAR3 (NUP96)

Mitochondria play a central role in ATP provisioning, redox and Ca2+ homeostasis and stress signaling of aerobic organisms. Animal mitochondria are extremely sensitive to fluctuating oxygen (O2) levels such as occur during tissue ischemia and/or environmental hypoxia. In hypoxia-sensitive organisms, hypoxia and especially post-hypoxic reoxygenation cause mitochondrial injury due to the elevated production of reactive oxygen species, Ca2+ overload and damage to the metabolic machinery; yet many hypoxia-tolerant species (including intertidal invertebrates) endure frequent hypoxia-reoxygenation cycles without apparent ill effects. The mechanisms of such exceptional mitochondrial robustness are not yet fully understood. I will discuss the mitochondrial responses to intermittent hypoxia in marine intertidal mollusks emphasizing the potentially adaptive functional and proteomic changes of the mitochondria and integration of the mitochondrial responses with cellular protection and stress response pathways (including antioxidant defense, autophagy and apoptosis) that might contribute to high tolerance to fluctuating O2 levels and support recovery in these organisms. I will also discuss the current knowledge gaps with an outlook to future studies needed to shed light on mitochondrial adaptations and evolution of metabolism in the environments with highly variable oxygen levels such as the intertidal zone.

Mitochondrial mechanisms of tolerance to fluctuating oxygen conditions: What can we learn from intertidal animals?

Understanding molecular mechanisms underlying physiology benefits from studies of isolated and/or cultured cells. However, virtually all experiments in cell culture are done in the absence of O2 regulation, resulting in incubator headspace O2 levels of 18-19%. In vivo, O2 levels in heart, skeletal muscle, brain, liver, and indeed most of the mammalian body, are typically 2-6%. The supra-physiological O2 levels in cell culture drive increased cellular reactive oxygen species (ROS) production, affecting many aspects of cell physiology. We have shown that supra-physiological O2 targets mitochondria, with important effects on bioenergetic function and network dynamics. Cellular responses to hormones like 17β-estradiol are significantly different in 18%, versus 5%, O2. Our RNAseq investigations show widespread effects of 18%, versus 5% O2 on diverse molecular processes ranging from DNA repair and cell cycle to energy metabolism to the viral response. Since supra-physiological O2 affects both transcriptional and translational processes, there are additional effects on relative protein abundance that are evident in proteomic analyses. The effects of supra-physiological O2 we have characterized are generally cell line-specific, making them difficult to predict. Given these myriad cellular effects of O2, it is important to reference hypoxia experiments in cell culture to physiological normoxia (e.g. 2-6%), but the vast majority of CO2 incubators used by cell culturists are not capable of regulating O2. We have developed a low-cost (&lt;1000 CAD) cell culture incubator capable of regulating O2, CO2, and temperature in their appropriate physiological ranges. Improved control over O2 levels will improve data quality in hypoxia experiments.

Importance of maintaining physioxia in cell culture

The crucian carp has the rare ability to survive days to months of anoxia, depending on temperature. Transcriptome analyses show that this is accompanied by widespread changes in gene expression. However, the importance of changes on the mRNA level can of course be questioned because it is the proteins that ultimately matter. We have therefore, in addition to global analyses of transcription and translation (ribosomal footprint profiling), measured the levels of proteins and phosphopeptides in tissues of crucian carp exposed to one week of anoxia and subsequent reoxygenation at 8°C. A general conclusion is that the transcriptome is a good indicator for the direction of change but that rather few proteins show a detectable change in their concentration during one week of anoxia and subsequent reoxygenation (e.g. 66 out of 3304 proteins in brain), which probably reflects that protein synthesis is slow and occur on top of a background of existing protein pools. Moreover, most proteins may have structural or housekeeping functions that are not altered during anoxia, and making major changes in protein concentrations would be energetically expensive, and energy use needs to be suppressed in anoxia. Phosphorylation of proteins, on the other hand, is an instant response, but also here relatively few changes were seen. In brain 109 out of 4316 phosphopeptides were regulated, while in liver 395 out of 1293 were regulated. The changes found in the proteome and phosphoproteome are likely to point at important adaptive mechanisms, which include mitochondrial adjustments, AMPK signalling and glucose metabolism.

Responses of the proteome and phosphoproteome to anoxia and reoxygenation in crucian carp (Carassius carassius)

Across diverse taxa, maternal allocation to offspring tends to increase until mothers reach a prime, before declining in later life. Offspring born to very young or old mothers thus are of lower quality, as measured for example in size at birth, and potentially experience reduced lifespan. Here, I describe how we can gain new insights into the evolutionary causes of this age-dependent allocation by studying the tsetse fly: a relatively long-lived fly which gives birth to single offspring the same size as the mother. We experimentally test whether the decline in offspring quality produced by older females in the laboratory is exacerbated by nutritional stress, or mitigated by alleviating costs of reproduction. Using state-dependent models, we explore the evolutionary conditions favouring hump-shaped allocation with age, and how this is affected by physiological constraints and environmental uncertainty. Such models also shed light on why the senescence that we find in laboratory flies seems absent in field conditions, where flies have limited access to food and higher mortality. Finally, I discuss the implications for understanding age-dependent maternal allocation not just for considering offspring longevity, but for population processes and disease transmission.

Age-dependent reproductive allocation in a viviparous fly

Maternal age at birth has been demonstrated to affect offspring performance in aspects associated with fitness, including juvenile survival, lifespan, and fitness. A tendency appears to exist for such maternal age effects to be deleterious (‘maternal senescence’). However, there also appears to be much variation in the degree (and even in the direction) of these effects. Why should maternal senescence evolve and where should we expect it to be strongest (or weakest)? The clearest and most general way to explore this question theoretically is to expand William Hamilton’s models of the evolution of ageing to age-specific maternal genetic effects for vital rates. This approach has been applied specifically only to juvenile survival, but it has yielded results that show: 1) that selection always favours the evolution of this manifestation of maternal senescence; 2) that the evolved rate of senescence will differ from actuarial and reproductive senescence; and 3) exactly how selection drives the age-of-onset of maternal senescence. Here I will discuss how this model of maternal genetic effects can be adapted to all other vital rates, and through these, to explain how natural selection can favour other aspects of maternal senescence, such as the Lansing Effect and reduced offspring fitness caused by advancing maternal age.   

Natural selection and the evolution of maternal age effects

Reproductive senescence is an age related decline in reproductive performance, and is commonly studied in terms of age-related patterns of offspring production. However, parental fitness arises via offspring performance as well as production, so both components require attention to gain a more complete understanding of the trajectory and fitness consequences of reproductive senescence. Here we utilise a longitudinal dataset from a long-term study of European badgers (Meles meles) to investigate maternal and paternal reproductive senescence, and quantify how both offspring production and lifetime performance vary with parental age. First, we show that badgers of both sexes experience a senescent decline in annual offspring production, which occurs with a similar age of onset in the two sexes. Second, we show evidence of deleterious maternal age effects on offspring performance; offspring mortality risk increases and offspring lifespan and life-time reproductive success decreases with within-mother increases in maternal age. Crucially, the maternal ages of onset of these declines in offspring performance are significantly earlier than those for offspring production, such that failure to account for them would lead to underestimation of the severity (in terms of timing and fitness consequences) of maternal reproductive senescence. Finally, we found no evidence of paternal age effects on offspring mortality, lifespan or life-time reproductive success. Overall, our findings illustrate the potential importance of attending to parental age-related changes in offspring performance as well as production, and the potential for sex differences in the relative contributions of these two components to the overall fitness consequences of reproductive senescence.

Parental age effects on offspring performance exacerbate reproductive senescence in female, but not male, European badgers.

Annual populations of animals express all of their reproductive effort in a single year only, with some of them producing offspring across a series of reproductive attempts (e.g. clutches) within the same breeding season. In such organisms, the timing of a reproductive attempt correlates with maternal age (so that offspring produced late in the breeding season are mothered by older females), and thus the phenotype of the offspring may differ between reproductive attempts of the same female. Moreover, environmental conditions experienced by the mother during that breeding season may further modify the phenotypic effects of maternal age. In this study, I investigated the effects of the interaction between maternal age and maternal environment on offspring phenotype using an annual population of three-spined stickleback (Gasterosteus aculeatus). I compared the phenotype of offspring from the early, mid- and late clutches of females, half of which were exposed to environmental stressors across their breeding season. Older females produced heavier eggs and fry that were larger at hatching, regardless of environmental stressors. Offspring of both stressed and non-stressed older mothers showed increased hormonal response to an acute stressor, but their survival patterns showed a complex relationship with both maternal age and stress exposure. Moreover, I observed a positive effect of maternal age on their daughters’ reproductive investment, but only if the mothers experienced stressful conditions during the breeding season. I thus show that annual females nearing the end of their reproductive lifespan increase their reproductive investment, with a potentially intergenerational effect. In addition, maternal age influences offspring phenotype, but this influence is moderated by the environmental conditions the mothers experience during the reproductive period.

Maternal age interacts with environmental conditions in shaping of offspring phenotype in an annual fish species.

The Lansing Effect (LE) is the observation of decreased offspring longevity with increasing maternal age at birth. Whilst there appears to be much awareness of this phenomenon, actual support for a LE is mixed, with various studies reporting positive, negative, or no effects of maternal age on lifespan. We performed a meta-analytic review of published studies with two goals: 1) to determine if there exists a tendency across all studies species to express a LE, and 2) identify factors that might related to the severity (or presence) of the effect. We derived 74 relevant estimates from 20 published studies of 14 species. Our analysis revealed a tendency across all studied animal species to exhibit a LE, but this appeared to be driven by estimates from insect and rotifer species, which were the most heavily studied and presented the most consistent LEs. We found no clear tendency from studies of bird or mammal species, but these were severly understudied. These results emphasize both the need to expand the taxonomic breadth of LE studies beyond laboratory model organisms and to develop new evolutionary theory that might help us understand this among-species variation. 









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Testing the relationship between muscle deformation and vertebral curvature during feeding in rainbow trout (Oncorhynchus mykiss).

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