France

Gabriella Willan (1), Catherine Williams (1,2), Shreya Rai (3), Arkhat Abzhanov (3), Loïc Kéver (4), Anthony Herrel (4,5), Arsalan Marghoub (6), Mehran Moazen (6), Susan Evans (7), Alex Kirby (8), Matt Vickaryous (1)
1 Department of Biomedical Sciences, Ontario Veterinary College, University of Guelph, Canada
2 Zoophysiology, Faculty of Natural Science, Aarhus University, Denmark 
3 Department of Life Sciences, Faculty of Natural Sciences, Imperial College, London, UK
4 UMR 7179 MECADEV C.N.R.S/M.N.H.N., Département Adaptations du Vivant, France
5 Evolutionary Morphology of Vertebrates, Ghent University, Gent, Belgium 
6 Department of Mechanical Engineering, University College London, UK
7 Department of Cell and Developmental Biology, University College London, UK
8 Department of Medical Physics and Biomedical Engineering, University College London, UK 

	Osteoderms are bone-rich elements that form within the dermis of various vertebrates including many species of lizard. Among lizards, osteoderms demonstrate variability in size, shape, and body-wide distribution but a detailed comparative assessment of osteoderm microstructure is lacking. Here, we characterize the histological diversity of osteoderms from representative members of the lizard groups Gekkota (geckos), Anguimorpha (anguids, Shinisaurus, helodermatids, varanids), and Scincomorpha (scincids, cordylids, gerrhosaurids). In virtually all lizards, osteoderms are composed primarily of bone, albeit with a heterogenous and often laminated fibrillary organization. Histologically, most osteoderms are dominated by lamellar, woven-fibred and/or Sharpey-fibred bone, although details of the organization and relative contribution of each bone matrix differs between genera. In addition, we found that multiple genera from each major group also develop a highly mineralized, collagen and cell-poor capping tissue – a feature previously restricted to only a handful of species. Singularly, the osteoderm-like elements from the gekkotan Geckolepis entirely lack bone and instead are composed of a plate of collagen topped with mineralized capping tissue. Initial studies of osteoderm development in the lacertid Timon show that specific markers for osteoblast differentiation (Osterix and β-catenin) can be successfully detected surrounding the growing osteoderm, opening possibilities of dissecting whether developmental strategies vary in sync with histological appearance, under drivers such as phylogeny, ecology and function. 





SEB Annual Conference 2022

Histological heterogeneity: development and tissue-level diversity of lizard osteoderms

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.

SEB’s Annual Conference is celebrated for creating the perfect composition of research, new discoveries and collaborative connections. Be creative and innovative by exchanging ideas and knowledge with masters of biology from all over the world.

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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Please register for the conference by clicking on this link:

https://www.sebiology.org/events/seb-annual-conference-2022/registration.html

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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

technical paper

Mitochondria are not merely the powerhouses of cells, responsible for ATP synthesis, but are also the engines of biosynthesis, as the Krebs cycle provides the precursors for amino-acid, sugar, fatty-acid and nucleotide synthesis, shaping all aspects of growth and development. Flux through the Krebs cycle is contingent on NADH oxida(on, which in turn depends on respiratory function, particularly at complex I. This depends on two genomes, mitochondrial and nuclear, which have radically different modes and tempi of evolution. Even trivial incompatibilities between these genomes can have large effects on fitness, especially when subjected to metabolic or redox stress. Complex I is especially prone to dysfunction as it is the largest complex, with the most mitochondrially encoded subunits, and is a major source of physiological reactive oxygen species. Our work using the Drosophila mitonuclear model shows that beOer complex I function in third-instar larvae and young adults corresponds to faster development, greater fer(lity, higher survival, longer lifespan and better physical performance. By fixing an isogenic nuclear background and varying mtDNA in D. melanogaster, we can dissect the mitochondrial contribution to each phenotype using tissue-specific fluorespirometry and metabolomics. Yet the molecular basis for these unexpected differences remains unclear. Our results suggest that complex I function is not shaped directly by mitonuclear coevolution, nor by adaptive selection on mitochondrial DNA alone, but may depend on epistatic effects linked with macromolecular organization, perhaps cristae membrane structure and supercomplex assembly, which we will explore in future work.

The Determinator: How does respiratory complex I control metabolic flux, fertility and longevity?

Biological armours, unlike architectural skins, face a curious structural paradox, in that they must continue to provide protection and support even as the structure they cover grows. (This is akin to the challenge of keeping fast-growing toddlers clothed.) Tessellated armours have evolved multiple times in animals as solutions for this problem, the gaps between tiles creating zones for activity (e.g. movement, growth), albeit perhaps at the expense of overall armour integrity. Our extended workgroup uses biological tessellations as model systems to explore form-function relationships and constraints in tissues, factors regulating mineralisation and growth, and material properties of biological composites. I discuss these functional morphological concepts in the context of biological tilings, drawing on examples from diverse systems and size scales, to offer perspectives on growth-mechanics trade-offs (both inside and outside the body), while reflecting on the value of cross-disciplinary bridges to invigorate the study of biological tissues.

Tales of tiled tissue trade-offs: Biological tessellations as architectural balance acts of growth and mechanics

Ossified dermal armor is found across the vertebrate tree of life. Despite bony plates being present in some of the earliest vertebrate ancestors (with dermal armor preceding jaws and even ossified skeletons in the evolution of the group), the ossified armor seen in modern actinopteryiigian fish, frogs, lizards, mammals, crocodiles and turtles appear to be apomorphic, having independently evolved in at least 25 lineages. Squamates—whose very name is derived from their scaly armor— have a particularly complex pattern of armor evolution, with members of 12 extant families possessing some form of osteoderms. These structures strengthen the integument, provide additional ornamentation in the form of spines or keels, and may play a role in calcium sequestration and thermoregulation. This study employs comparative phylogenetic analyses of micro-computed tomography (μCT) datasets to quantify and investigate the diversity of dermal armor across Squamata, with broad sampling in the families that are known to possess osteoderms. Our analysis reveals seven independent origins of osteoderms within the order, with three clades—Cordylidae, Anguidae and egerniine skinks—displaying increased rate-shifts in the distribution and extent of their armor. To better understand the mechanisms generating this variation, we sequenced the transcriptome of mammalian osteoderms and identified several pathways known to be involved in the growth of endochondral bone. Ongoing transcriptomic analysis of osteoderm development and selection analysis within the three rate-shifted squamates lineages hints at a universal mechanism for the repeated re-evolution of dermal armor in amniotes.

Scaled up defenses: Patterns and drivers of dermal armor in lizards

Biomechanical behaviour of lizard osteoderms and skin under external loading
Loïc Kéver1, Olivier Damien2, Arsalan Marghoub3, Mehran Moazen3, Susan Evans3, Matthew K. Vickaryous 4, Arkhat Abzhanov5, Anthony Herrel 1,6 
1National Museum of Natural History, France
2CONACyT Autonomous University of Baja California Sur, Mexico
3University College London, UK
4University of Guelph, Canada
5Imperial College London, UK
6Ghent University, Belgium
Dermal bony plates also known as osteoderms are present in several distantly related vertebrate taxa and they are particularly common and diverse among extant lizards. Lizard osteoderms have classically been considered to be protective elements against predator attacks. However, empirical data supporting this hypothesis are scant and one of the basic questions pertaining to their diversity has never been addressed: are there interspecific differences in the deformation of lizard osteoderms under external loading? We sampled formalin fixed specimens from eleven species of lizards with osteoderms of different morphologies, instrumented one of the temporal osteoderms with a rectangular rosette strain gauge and loaded different areas of their head to better understand the mechanical responses of osteoderms to loading. Our goals were to 1) test whether loadings applied in different locations of the head (including on the instrumented osteoderm) generated strains in the instrumented osteoderm, 2) explore whether species differed in the relative stiffness of their osteoderm and skin and 3) provide insights into the morphological features and patterns of organization associated with variation in stiffness. We show that loading neighboring osteoderms can generate large strains in the instrumented osteoderm. Moreover, despite a large overlap between some species, the strains recorded showed interspecific differences in magnitude. Smaller strains were recorded in species with relatively thick osteoderms including Heloderma suspectum, H. horridum and Tiliqua rugosa. 






Biomechanical behaviour of lizard osteoderms and skin under external loading

Osteoderms (ODs) are calcified hard tissues that develop directly within the dermis of many lizards. They can be found all over the body, or only on some parts of the body (like the head, where intimate connections with the bones of the skull are common). OD’s main role has been commonly considered to be mainly protective, however there are some evidences that they can also have other functions. We investigated the potential role of calvarial ODs in the biomechanics of feeding. Two lizard species were selected: one that has ODs all over its head (Tiliqua scincoides), and one that has ODs only over its temporal region (Timon lepidus). Several experiments were performed to quantify the level of principal strains on one of the temporal ODs while measuring bite force. At the same time, finite element models of both lizards were developed based on micro-CT images. After being validated against the experimental measurements, finite element models were used to further investigate several hypothetical scenarios regarding the function of the ODs, such as having no ODs. Our results show that ODs can have a significant role in reducing the level of strain across the skull during feeding. Perhaps the possession of cranial ODs can enhance the biting performance of some lizards.

Calvarial osteoderms and their potential role in Lizard feeding biomechanics

Humans are drawn to patterns and hierarchies in nature, mimicking them particularly in decoration and architecture. Natural patterns, however, are never purely aesthetic and, since evolution works towards optimising a variety of factors simultaneously, natural structural systems are intrinsically multi-functional. In this study, we examine and classify biological tessellations or ‘tilings’: rather than starting from a specific anatomical feature or function, we focus on this unexpectedly ubiquitous natural structural motif and show its prevalence and function across the Tree of Life. Drawing on more than 100 examples, from viruses to vertebrates and over 8 orders of magnitude in size scale, we construct a hierarchical system of classification for this diverse, but largely unexamined trope in biological patterning. We detail our novel classification scheme, which captures tessellation morphology through a set of seven variables, detailing the material, form and function of tiled natural architectures. Examining the relationships of variables in a Multiple Correspondences Analysis, we observe broad structural correlations across and between taxonomic groups (e.g. materials common to particular taxonomic groups, tiling features that tend to co-occur), but also capture links between anatomical characteristics and particular functions (e.g. tiling morphologies associated with structural support or mobility). Our resulting collection of natural tessellations and its companion website are multidisciplinary meeting points, offering new windows for exploring selective pressures and trade-offs that shape anatomical evolution in nature, for interpreting man-made tessellations in history, and for guiding novel approaches in design and architecture.

Tessellated Material Systems: A Catalogue to Explore the Multifunctionality and Biodiversity of a Universal Motif

Impacts of changing environment on fitness are mediated by changes in energy acquisition and allocation within an organism. Maintenance energy costs constitute a substantial part of individual's energy budget. Therefore, individual variation in standard metabolic rate plays an important role in understanding how ectotherms adapt to environmental changes. Despite considerable efforts in this area, many issues remain unresolved. In this talk, I (1) introduce the theoretical framework for the link between environmental change, individual metabolic variation and fitness, (2) present the latest findings in this field, and (3) highlight priorities for future research.

Individual variation in metabolic rate and ectotherm responses to environmental change

The selective harvest of individuals from wild populations constitutes one of the strongest and most widespread human-induced evolutionary pressures for natural populations. In addition to imposing strong selection on potentially heritable fitness traits, intensive harvest could also cause environmental changes in targeted population, such as a reduction in the population density, which could in turn affect the evolutionary potential of the traits in the populations. As metabolic rate is related to many of the biological functions in animals, interacting with growth, movements, and behaviour, selection on this trait could have important repercussions for wild populations. Using wild zebrafish as model species reared at two densities, and simulated trawling fishing pressure as selective harvest, we investigated the potential for harvest-induced evolution on metabolic rate and associated traits (growth, swimming, risk taking behaviour). We showed consistent capture of fish with lower metabolic rate, slower growth and slower swimming, regardless of density. As these traits had significant heritability, such harvest could lead to evolution of the populations over time. However, even though metabolic rate was phenotypically correlated to the other traits, no genetic correlations were observed between metabolic rate and either growth or swimming. Therefore, selection on metabolic rate is unlikely to induce indirect selection on the other traits and vice versa. The potential evolution of metabolic rate, growth and swimming under harvest would thus be more the result of independent direct selection on each trait rather than correlated selection.

The evolutionary impact of harvesting selection and population density on fish metabolic rate and associated traits

Basal metabolic rate is often likened to the idling speed of mammals. Measured during rest in non-reproductive, mature, fasted animals, it has become a gold standard for use in interspecific studies. Recent evolutionary analyses have shown a decoupling between basal metabolism and body temperature in endotherms. However, these studies were based on body temperature datasets that ignored the inherent variability in this trait and consisted of non-comparable temperatures (for example comparing that of a resting animal during the active phase of its activity cycle to an active animal in its rest phase). Using a new dataset of standardised resting body temperatures in mammals, we explore the relationship between basal metabolism and body temperature as well as the evolutionary history of these two traits. We discuss the implications of correcting, or not, for body temperature in studies on metabolic scaling and discuss the role of thermoregulatory phenotypes in shaping mammalian energetics.

The evolution of resting body temperatures in mammals

This study asked whether interindividual variation in maximum and standard aerobic metabolic rates of the Gulf killifish, Fundulus grandis, held under common garden conditions correlate with gill morphology and cardiac mitochondrial bioenergetics, traits reflecting critical steps in the oxygen-supply cascade from the environment to the tissues. Maximum metabolic rate (MMR) was positively related to body mass, total gill filament length, and myocardial oxygen consumption during maximum oxidative phosphorylation (multiple R2 = 0.82). Standard metabolic rate (SMR) was positively related to body mass, total gill filament length, and myocardial oxygen consumption during maximum electron transport system activity (multiple R2 = 0.69). After controlling for body mass, individuals with longer gill filaments, summed over all filaments, or greater cardiac respiratory capacity had higher whole-animal metabolic rates. The overall model fit and the explanatory power of individual predictor variables were better for MMR than for SMR, suggesting that gill morphology and myocardial bioenergetics are more important in determining maximum rather than resting metabolism. Heart ventricle mass was not related to mass-independent variation in MMR or SMR, indicating that the quality of the heart (i.e., the capacity for mitochondrial metabolism) was more influential than heart size. Finally, myocardial oxygen consumption required to offset the dissipation of the transmembrane proton gradient in the absence of ATP synthesis was not correlated with either MMR or SMR. The results support the idea that interindividual variation in aerobic metabolism, particularly maximum metabolic rate, is explained, in part, by variation in specific steps in the oxygen-supply cascade.

Histological heterogeneity: development and tissue-level diversity of lizard osteoderms

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