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Jaw movements during mammalian chewing drive occlusion and food breakdown. As important as jaw movements are for chewing, soft tissues within the oral cavity are essential for handling the food bolus throughout the chewing sequence. For instance, tongue movements and deformations (1) position the food between the tooth rows, (2) help mix the bolus with saliva to initiate digestion and improve swallowability, and (3) transport the bolus to the oropharynx to initiate the swallow. Tongue movements and deformations must be coordinated with jaw movements to ensure chewing performance and efficiency as well as to avoid self-injury, and previous research shows that disruption of the sensory input from the tongue alters jaw movements during chewing in pigs. Even though jaw and tongue movements during mammalian chewing are investigated extensively, their coordination pattern(s) have received less attention. We present three different approaches to quantify the correlation between jaw movements (opening and closing, mediolateral deviation) and tongue movements (positional changes such as protraction-retraction) and deformation (length and width changes) during chewing in pigs. At the sequence level, cross-correlations are used to calculate the lag in time between tongue and jaw kinematics. Cross-correlation analyses can also be carried out at the cycle level, albeit with less statistical power. Finally, functional data analysis standardizes and resamples the data to test for jaw-tongue correlation at each time point, essentially testing bivariate correlation continuously throughout the chewing cycle. We discuss the benefits and limitations of each methodology to emphasize the impact of combining analytical tools.

SEB Conference 2022

Jaw-tongue coordination during chewing in Pigs

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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.

Vertebrate feeding is a complex process with multiple aspects of integration, including among anatomical systems and physiologic levels. Success in feeding, both in enhanced performance and avoidance of failure, is a mission-critical function for all animals. Hiiemae and Crompton (1985) argued for this integration as the basis of understanding vertebrate feeding in general, and mammalian feeding in specific. The return to this perspective within the comparative biology/ biomechanics/ evolution community is reflected in the enthusiasm for this symposium . 

Feeding—from ingestion through mechanical and chemical processing to transport and the ultimate swallow into the mid-GI system—is a continuous process through what was embryologically and evolutionarily a simple tube. Irrespective of anatomical and evolutionary elaboration, this basic tube is the foundation of the function and survival of the organism. Focusing on specific system functions (prey capture or mastication) provides insight into how natural selection may act on regional anatomy. Yet, consideration of the entire gastrointestinal tract and its outgrowths is necessary to understand how natural selection operates on the feeding performance of the organism as a whole. 

Neurophysiologic integration produces the function or behaviour of feeding. Performance in feeding is ultimately a feedback loop, taking sensory input from soft tissues and bones and converting that information into muscular activation in the central nervous system (CNS), including the brain stem and the cerebral cortex. Focusing on individual parts or specific levels of this elaborate system has provided an essential detail of how the system works. Integration among these individual functional components as well as consideration of downstream gastrointestinal structure and function may yield further insights into fundamental constraints and key evolutionary pressures on this essential system. Mammalian feeding is an exemplar of how both anatomical and physiologic integration have provided both the basis for the variation in mammalian evolution as well as the limits on what is possible. 


Hiiemae KM, Crompton AW. Mastication, food transport and swallowing. In: Hildebrand M, Bramble D, Liem K, Wake D, editors. Functional Vertebrate Morphology. Cambridge: Harvard University Press; 1985. pp. 262–90.








Integration across anatomy and physiology is the basis for understanding feeding behaviour in vertebrates

Elasmobranch fishes (sharks and rays) display a skin covered in hypermineralized scales that resemble teeth. These structures are continuously regenerated over the individual’s lifetime, they display a range of morphological variations within one individual, but also between species. Scales and skin are under a wide set of selective pressures, including general resistance to parasites, female protection against male biting during mating, or hydrodynamism in pelagic species. 
The development and regeneration of such structures raises several issues that can be addressed by developmental biologists, such as:  How is the organisation of these arrays of scales regulated? How can the diversity in shape be generated within one individual? How are other physiological systems (e.g., the sensory system) organised over these locally mineralized surfaces? Here I will discuss the contribution of recent studies on the lesser spotted catshark Scyliorhinus canicula to highlight several developmental aspects related to these issues, integrating morphological descriptions, development modelling and transcriptomic data. 

Skeleton in the skin? Teeth in the skin!

The rate at which animals acquire and use energy is an important factor that affects many aspects of animal performance, including reproductive output and thermoregulatory capabilities. Therefore, understanding the factors limiting energy budgets has remained one of the central issues in ecological and evolutionary physiology. We used a unique experimental evolution model – lines of bank voles (Myodes glareolus) selected for high rate of swim-induced aerobic metabolism (VO2swim, A-lines), which evolved a 70% higher VO2swim than that observed in unselected control (C) lines – and asked how the BMR, reproductive output, and thermoregulatory capabilities evolved in response to the selection. After 25 generations, animals from the A-lines achieve over 30% higher forced running maximum metabolic rate than those from unselected, control (C) lines. The selection has also increased the forced running maximum metabolic rate by about 30%37. Voles from the A-lines spend more time on active swimming, and, unlike the C-line voles, during the swimming trial work up to their physiological performance limit they achieve during running. In these lines the animals have developed an increased metabolic capacity, and we tried to understand the mechanism behind it. 




The physiological effects of experimental evolution of aerobic exercise performance in bank voles

Life-history variation emerges due to trade-offs in energy allocation, suggesting energetics shapes life-history evolution. The Atlantic salmon (Salmo salar) exhibits high diversity in the age-at-maturity trait, which is largely controlled by two genomic regions, vgll3 and six6.  This simple genetic control of age-at-maturity enables implementing genomic prediction methods to test potential genetic correlations, and subsequent co-evolution, between age-at-maturity and physiological traits. Here, we tested how variation in these life-history genomic regions affect the central metabolic phenotypes: standard and maximum metabolic rates, and aerobic scope in juvenile Atlantic salmon. We found no evidence for covariation between standard metabolic rate and the two life-history loci. However, we found that one of the life-history loci affected the maximum metabolic rate and aerobic scope, and that the two loci showed physiological epistasis in the control of maximum metabolic rate. We then measured proxies of aerobic and anaerobic capacities from four tissues to study how tissue-specific energetics can mediate genetic variation in life-history.  The results help us to better understand the mechanistic basis of life-history variation as well as metabolic constraints on life-history evolution.

Insights to genetic associations of life-history and metabolic rate via large-effect loci in Atlantic salmon

While some traits such as body size are well known predictors of metabolism, the covariance between metabolism and other traits remains poorly resolved. There are good reasons to suspect that developmental mode (direct or indirect development) should covary with metabolic rate but this covariance has not been explored. We compiled published data for adult metabolic rates and developmental mode for 705 species of marine invertebrates across 13 phyla. Using a phylogenetically-controlled analysis, we found that adult metabolism is shaped by developmental mode – species with planktonic larvae have higher metabolic rates than those with aplanktonic development. This pattern is unaffected by adult size. We also found support for differential temperature-dependence of metabolic rate among developmental modes. Overall, our results suggest developmental mode shapes the physiology of marine organisms in ways that have gone largely unanticipated by theory.

Macroevolutionary patterns in metabolism and development

Reproductive success (and therefore selection) is ultimately related to how well an organism performs in the context of its environment. Performance reflects the interactive trade-off between physiological traits, behaviour, resource availability and mortality. Time-integrated field metabolic rate (FMR) captures the realised energetic cost of performing in a natural setting, accounting for multi-generational acclimation to the environmental and ecological context. In-situ measurements of FMR may be needed to fully appreciate the evolutionary significance of variation in metabolic traits. 

Here we draw on data compiled using a new emerging proxy capable of providing estimates of individual-level FMR together with experienced temperature and growth rate derived from the otoliths of marine fishes. We quantify the extent and nature of among- and within-species variation in FMR observed so far in marine fishes. Among other patterns we show that in most observed populations operating within their natural thermal range, realised FMR is relatively insensitive to temperature, with no clear relationship between individual-level variation in FMR and growth rate. However, temperature has a stronger effect on realised FMR during early juvenile life stages (including in the same individuals), implying that in fishes, thermal effects on selection may be stronger during early juvenile life history stages. 








Variation in field metabolic rates of wild marine fishes: thermal, ontogenetic, phylogenetic and macroecological drivers.

Changing the morphology of the plant vacuole depends on the integrity of the cytoskeleton. So far, only little is known about the nature of this relationship. The plant-specific Networked (Net) family of membrane-associated actin-binding proteins contains two members, Net4A and Net4B, which are of special interest since they localize to the tonoplast. Recently, we could show that Net4 modules the compactness of vacuoles and this in turn affects its space-filling function and eventually inhibits cell elongation and growth. Since the net4a net4b double mutant only has a mild phenotype and other NETs seems not to compensate, we expected a higher molecular complexity and searched for new interactors. Pull-down experiments followed by MS-MS identified several new interactors, potentially participating in the regulation of the vacuole-cytoskeleton interface.

The vacuole - cytoskeleton connection: a handle to regulate growth

The vacuole is a hallmark of the plant cell, generating turgor pressure and thus driving growth. Seed plant embryos also contain numerous specialised Protein Storage Vacuoles (PSV) which are repositories for the nutritional content of seeds. But how do these specialised PSVs form and what mechanism drives this process? Recent work has demonstrated that PSVs are formed by the remodelling of the single embryonic vacuole into many fragmented PSVs. The main constituent of these PSV are seed storage proteins (SSP).  We have shown that SSP undergo liquid-liquid phase separation forming a droplet within the vacuole and these SSP droplets can bend the tonoplast membrane. However, can this process of SSP phase separation drive fragmentation of a single embryonic vacuole into multiple PSV? Additionally, which proteins and conditions drive phase separation of SSP in the embryonic vacuole? We have identified and are characterising protein candidates for drivers of phase separation in the embryonic vacuole and determining their role in PSV biogenesis.

Its all just a phase: Phase separation driving organelle biogenesis.

In plant cells, cargo proteins destined to the vacuoles contain sequence specific information known as vacuolar sorting determinant (VSD) that is recognized and sorted by vacuolar sorting receptors (VSRs) to the vacuoles. To understand how VSR recognizes its cargos, our group have determined the crystal structures of the PA domain of Arabidopsis VSR1 in complex with the vacuolar sorting determinants (VSDs) of a protease aleurain [1] and a 12 S globulin cruciferin (CRU) 1 [2]. Structural comparison with the apo-form of VSR1-PA suggests that cargo-binding induces conformational changes in four regions of VSR1-PA. The VSDs bind to the cargo-binding loop consisting of a conserved motif of 95RGDCYF100. The invariant Arg-95 residue was found to be essential for receptor-cargo interactions and vacuolar sorting of cargo proteins. In vitro pull-down assay showed that VSR1 interacts with the C-terminal decapeptide sequences of CRU1, CRU4 and vicilin-like seed storage protein (VL) 22, but not with those of CRU2, CRU3, VL21 and VL43. Tagging the C-terminal sequences of CRU1 and VL22 to the secretary red fluorescent proteins are sufficient in redirecting the proteins to the vacuoles in Arabidopsis protoplasts. A P453A substitution converts the C-terminal sequence of CRU2 to a C-terminal VSD that is recognized by VSR1. Structural insights on receptor-cargo obtained could be useful in targeting recombinant proteins to protein storage vacuoles in seeds.

This work was supported by grants from the Research Grants  Council  of  Hong  Kong  Special  Administrative  Region,  China (CUHK14151416, C4041-18EF, AoE/M-05/12, AoE/M403/16, and C4033-19E) and The National Natural Science Foundation of China (91854201 and31670179) and by direct grants from The Chinese University of Hong Kong.

[1] Luo F. et al. (2014) “How vacuolar sorting receptor proteins interact with their cargo proteins: crystal structures of apo and cargo-bound forms of the protease-associated domain from an Arabidopsis vacuolar sorting receptor.” Plant Cell, 26, 3693-708
[2] Tsao H.E. et al. (2022) Structural insights into how vacuolar sorting receptors recognize the sorting determinants of seed storage proteins. Proc Natl Acad Sci USA, 119, e2111281119.




How cargo proteins are recognized and sorted to the vacuoles?

Cells typically remain relatively small, because if cells grow beyond a critical limit, the surface of the plasma membrane eventually ceases to accommodate intracellular needs. Compared to animals, plant cells can dramatically increase their size without the apparent need for surface furcation. The vacuole is the biggest plant organelle and has a space-filling function, allowing to occupy up to 90% of the cell volume (Löfke et al., 2015; Scheuring et al., 2016; Dünser et al., 2019). The dynamic regulation of vacuolar size allows plant cells to expand with little increase of the cytosol (Dünser et al., 2019; Dünser et al., 2022), maintaining a favorable cell surface to cytosol ratio during growth. Here we discuss subcellular mechanisms that ensure the coordination of cellular and vacuolar size expansions.

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