Making developmental sense of the senses, their origin and function.

The primary senses-touch, taste, sight, smell, and hearing-connect animals with their environments and with one another. Aside from the eyes, the primary sense organs of vertebrates and the peripheral sensory pathways that relay their inputs arise from two transient stem cell populations: the neural crest and the cranial placodes. In this chapter we consider the senses from historical and cultural perspectives, and discuss the senses as biological faculties. We begin with the embryonic origin of the neural crest and cranial placodes from within the neural plate border of the ectodermal germ layer. Then, we describe the major chemical (i.e. olfactory and gustatory) and mechanical (i.e. vestibulo-auditory and somatosensory) senses, with an emphasis on the developmental interactions between neural crest and cranial placodes that shape their structures and functions.

Cell behaviors that pattern developing tissues: the case of the vertebrate nervous system.

Morphogenesis from cells to tissue gives rise to the complex architectures that make our organs. How cells and their dynamic behavior are translated into functional spatial patterns is only starting to be understood. Recent advances in quantitative imaging revealed that, although highly heterogeneous, cellular behaviors make reproducible tissue patterns. Emerging evidence suggests that mechanisms of cellular coordination, intrinsic variability and plasticity are critical for robust pattern formation. While pattern development shows a high level of fidelity, tissue organization has undergone drastic changes throughout the course of evolution. In addition, alterations in cell behavior, if unregulated, can cause developmental malformations that disrupt function. Therefore, comparative studies of different species and of disease models offer a powerful approach for understanding how novel spatial configurations arise from variations in cell behavior and the fundamentals of successful pattern formation. In this chapter, I dive into the development of the vertebrate nervous system to explore efforts to dissect pattern formation beyond molecules, the emerging core principles and open questions.

Flooding, season and habitat interact to drive changes in vertebrate scavenging and carcass persistence rates.

Scavenging dynamics are influenced by many abiotic and biotic factors, but there is little knowledge of how scavengers respond to extreme weather events. As carrion is a major driver of the organisation and structure of food webs within ecological communities, understanding the response of scavengers to extreme weather events is critical in a world that is increasingly subject to climate change. In this study, vertebrate scavenging and carcass persistence rates were quantified in the Simpson Desert of central Australia; a system that experiences major fluctuations and extremes in weather conditions. Specifically, a total of 80 adult red kangaroo (Osphranter rufus) carcasses were placed on the landscape and monitored using remote sensor cameras. This included 40 carcasses monitored before and then 40 carcasses monitored after a major flooding event. The carcasses were monitored equally before and after the flood across different seasons (warm and cool) and in dune and interdune habitats. Overall, a total of 8124 scavenging events for 97,976 visitation minutes were recorded for 11 vertebrate species within 30 days of carcass placement pre- and post-flood. Vertebrate scavenging increased post-flood in the warm season, especially by corvids which quadrupled their scavenging events during this time. There was little difference in carcass persistence between habitats, but carcasses persisted 5.3-fold longer post-flood in warm seasons despite increased vertebrate scavenging. The results demonstrate that a flood event can influence scavenging dynamics and suggest a need to further understand how seasons, habitats and extreme weather events can drive changes in carrion-based food webs.

Land-use intensity influences European tetrapod food webs.

Land use intensification favours particular trophic groups which can induce architectural changes in food webs. These changes can impact ecosystem functions, services, stability and resilience. However, the imprint of land management intensity on food-web architecture has rarely been characterized across large spatial extent and various land uses. We investigated the influence of land management intensity on six facets of food-web architecture, namely apex and basal species proportions, connectance, omnivory, trophic chain lengths and compartmentalization, for 67,051 European terrestrial vertebrate communities. We also assessed the dependency of this influence of intensification on land use and climate. In addition to more commonly considered climatic factors, the architecture of food webs was notably influenced by land use and management intensity. Intensification tended to strongly lower the proportion of apex predators consistently across contexts. In general, intensification also tended to lower proportions of basal species, favoured mesopredators, decreased food webs compartmentalization whereas it increased their connectance. However, the response of food webs to intensification was different for some contexts. Intensification sharply decreased connectance in Mediterranean and Alpine settlements, and it increased basal tetrapod proportions and compartmentalization in Mediterranean forest and Atlantic croplands. Besides, intensive urbanization especially favoured longer trophic chains and lower omnivory. By favouring mesopredators in most contexts, intensification could undermine basal tetrapods, the cascading effects of which need to be assessed. Our results support the importance of protecting top predators where possible and raise questions about the long-term stability of food webs in the face of human-induced pressures.

Evolution of neuronal cell classes and types in the vertebrate retina.

The basic plan of the retina is conserved across vertebrates, yet species differ profoundly in their visual needs1. Retinal cell types may have evolved to accommodate these varied needs, but this has not been systematically studied. Here we generated and integrated single-cell transcriptomic atlases of the retina from 17 species: humans, two non-human primates, four rodents, three ungulates, opossum, ferret, tree shrew, a bird, a reptile, a teleost fish and a lamprey. We found high molecular conservation of the six retinal cell classes (photoreceptors, horizontal cells, bipolar cells, amacrine cells, retinal ganglion cells (RGCs) and Müller glia), with transcriptomic variation across species related to evolutionary distance. Major subclasses were also conserved, whereas variation among cell types within classes or subclasses was more pronounced. However, an integrative analysis revealed that numerous cell types are shared across species, based on conserved gene expression programmes that are likely to trace back to an early ancestral vertebrate. The degree of variation among cell types increased from the outer retina (photoreceptors) to the inner retina (RGCs), suggesting that evolution acts preferentially to shape the retinal output. Finally, we identified rodent orthologues of midget RGCs, which comprise more than 80% of RGCs in the human retina, subserve high-acuity vision, and were previously believed to be restricted to primates2. By contrast, the mouse orthologues have large receptive fields and comprise around 2% of mouse RGCs. Projections of both primate and mouse orthologous types are overrepresented in the thalamus, which supplies the primary visual cortex. We suggest that midget RGCs are not primate innovations, but are descendants of evolutionarily ancient types that decreased in size and increased in number as primates evolved, thereby facilitating high visual acuity and increased cortical processing of visual information.

Using salamanders as model taxa to understand vertebrate feeding constraints during the late Devonian water-to-land transition.

The vertebrate water-to-land transition and the rise of tetrapods brought about fundamental changes for the groups undergoing these evolutionary changes (i.e. stem and early tetrapods). These groups were forced to adapt to new conditions, including the distinct physical properties of water and air, requiring fundamental changes in anatomy. Nutrition (or feeding) was one of the prime physiological processes these vertebrates had to successfully adjust to change from aquatic to terrestrial life. The basal gnathostome feeding mode involves either jaw prehension or using water flows to aid in ingestion, transportation and food orientation. Meanwhile, processing was limited primarily to simple chewing bites. However, given their comparatively massive and relatively inflexible hyobranchial system (compared to the more muscular tongue of many tetrapods), it remains fraught with speculation how stem and early tetrapods managed to feed in both media. Here, we explore ontogenetic water-to-land transitions of salamanders as functional analogues to model potential changes in the feeding behaviour of stem and early tetrapods. Our data suggest two scenarios for terrestrial feeding in stem and early tetrapods as well as the presence of complex chewing behaviours, including excursions of the jaw in more than one dimension during early developmental stages. Our results demonstrate that terrestrial feeding may have been possible before flexible tongues evolved. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Energetics of collective movement in vertebrates.

The collective directional movement of animals occurs over both short distances and longer migrations, and is a critical aspect of feeding, reproduction and the ecology of many species. Despite the implications of collective motion for lifetime fitness, we know remarkably little about its energetics. It is commonly thought that collective animal motion saves energy: moving alone against fluid flow is expected to be more energetically expensive than moving in a group. Energetic conservation resulting from collective movement is most often inferred from kinematic metrics or from computational models. However, the direct measurement of total metabolic energy savings during collective motion compared with solitary movement over a range of speeds has yet to be documented. In particular, longer duration and higher speed collective motion must involve both aerobic and non-aerobic (high-energy phosphate stores and substrate-level phosphorylation) metabolic energy contributions, and yet no study to date has quantified both types of metabolic contribution in comparison to locomotion by solitary individuals. There are multiple challenging questions regarding the energetics of collective motion in aquatic, aerial and terrestrial environments that remain to be answered. We focus on aquatic locomotion as a model system to demonstrate that understanding the energetics and total cost of collective movement requires the integration of biomechanics, fluid dynamics and bioenergetics to unveil the hydrodynamic and physiological phenomena involved and their underlying mechanisms.

Are vertebrates constrained to two sets of paired appendages? The morphology, development, and evolution of pre-pelvic claspers in the Holocephali.

Holocephalans exhibit auxiliary appendages called pre-pelvic claspers (PPCs) that are located anterior to the pelvic fins, while pelvic claspers are pelvic fin modifications located posteriorly as modified metapterygia. Articulation points of the PPCs have not previously been imaged or evaluated in a comparative context, therefore, they may represent modified pelvic fin structures if they articulate with the propterygium. Alternatively, they could represent the only example of an independent third set of paired appendages in an extant taxon, if they articulate independently from any pelvic fin basal cartilages, challenging the current paradigm that extant jawed vertebrates are constrained to two sets of paired appendages. Two extinct groups, including Placoderms and Acanthodians, exhibit variation in the number of paired appendages, suggesting this may be a plesiomorphic trait. We evaluated PPC developmental growth rates, morphology, and articulation points in spotted ratfish (Hydrolagus Colliei, Holocephali). We also compared variation in PPC morphology among representatives of the three extant holocephalan families. Both, the pre-pelvic and pelvic claspers exhibit a dramatic surge in growth at sexual maturity, and then level off, suggesting synchronous development via shared hormonal regulation. While mature females are larger than males, pelvic fin growth and development is faster in males, suggesting a selective advantage to larger fins with faster development. Finally, microcomputed tomography scans revealed that PPCs are not modified propterygia, nor do they articulate with the propterygium. They articulate with the anterior pre-pelvic process on the anterior puboischiadic bar (or pelvic girdle), suggesting that while they are associated with the pelvic girdle, they may indeed represent a third, independent set of paired appendages in extant holocephalans.

Transposable Elements: Epigenetic Silencing Mechanisms or Modulating Tools for Vertebrate Adaptations? Two Sides of the Same Coin.

Transposable elements constitute one of the main components of eukaryotic genomes. In vertebrates, they differ in content, typology, and family diversity and played a crucial role in the evolution of this taxon. However, due to their transposition ability, TEs can be responsible for genome instability, and thus silencing mechanisms were evolved to allow the coexistence between TEs and eukaryotic host-coding genes. Several papers are highlighting in TEs the presence of regulatory elements involved in regulating nearby genes in a tissue-specific fashion. This suggests that TEs are not sequences merely to silence; rather, they can be domesticated for the regulation of host-coding gene expression, permitting species adaptation and resilience as well as ensuring human health. This review presents the main silencing mechanisms acting in vertebrates and the importance of exploiting these mechanisms for TE control to rewire gene expression networks, challenging the general view of TEs as threatening elements.

Effects of the environment on the evolution of the vertebrate urinary tract.

Evolution of the vertebrate urinary system occurs in response to numerous selective pressures, which have been incompletely characterized. Developing research into urinary evolution led to the occurrence of clinical applications and insights in paediatric urology, reproductive medicine, urolithiasis and other domains. Each nephron segment and urinary organ has functions that can be contextualized within an evolutionary framework. For example, the structure and function of the glomerulus and proximal tubule are highly conserved, enabling blood cells and proteins to be retained, and facilitating the elimination of oceanic Ca+ and Mg+. Urea emerged as an osmotic mediator during evolution, as cells of large organisms required increased precision in the internal regulation of salinity and solutes. As the first vertebrates moved from water to land, acid-base regulation was shifted from gills to skin and kidneys in amphibians. In reptiles and birds, solute regulation no longer occurred through the skin but through nasal salt glands and post-renally, within the cloaca and the rectum. In placental mammals, nasal salt glands are absent and the rectum and urinary tracts became separate, which limited post-renal urine concentration and led to the necessity of a kidney capable of high urine concentration. Considering the evolutionary and environmental selective pressures that have contributed to renal evolution can help to gain an increased understanding of renal physiology.

Sublethal consequences of ultraviolet radiation exposure on vertebrates: Synthesis through meta-analysis.

Ultraviolet radiation (UVR) from the sun is a natural daytime stressor for vertebrates in both terrestrial and aquatic ecosystems. UVR effects on the physiology of vertebrates manifest at the cellular level, but have bottom-up effects at the tissue level and on whole-animal performance and behaviours. Climate change and habitat loss (i.e. loss of shelter from UVR) could interact with and exacerbate the genotoxic and cytotoxic impacts of UVR on vertebrates. Therefore, it is important to understand the range and magnitude of effects that UVR can have on a diversity of physiological metrics, and how these may be shaped by taxa, life stage or geographical range in the major vertebrate groups. Using a meta-analytical approach, we used 895 observations from 47 different vertebrate species (fish, amphibian, reptile and bird), and 51 physiological metrics (i.e. cellular, tissue and whole-animal metrics), across 73 independent studies, to elucidate the general patterns of UVR effects on vertebrate physiology. We found that while UVR's impacts on vertebrates are generally negative, fish and amphibians were the most susceptible taxa, adult and larvae were the most susceptible life stages, and animals inhabiting temperate and tropical latitudes were the most susceptible to UVR stress. This information is critical to further our understanding of the adaptive capacity of vulnerable taxon to UVR stress, and the wide-spread sublethal physiological effects of UVR on vertebrates, such as DNA damage and cellular stress, which may translate up to impaired growth and locomotor performance. These impairments to individual fitness highlighted by our study may potentially cause disruptions at the ecosystem scale, especially if the effects of this pervasive diurnal stressor are exacerbated by climate change and reduced refuge due to habitat loss and degradation. Therefore, conservation of habitats that provide refuge to UVR stress will be critical to mitigate stress from this pervasive daytime stressor.

Tales of the tongue.

Since first evolving 350 million years ago, the tongue has taken myriad forms, unlocking new niches and boosting the diversity of life.

Staying Hydrated in Seawater.

Reduction of intestinal lumen osmotic pressure by the formation of Ca(Mg)CO3, "ichthyocarbonate," is essential for osmoregulation by the only vertebrate group, ray-finned fishes, widely capable of hydrating by ingesting seawater. Ichthyocarbonate formation and excretion are under elaborate physiological control and play an important, yet still poorly defined, role in the oceanic carbon cycle.

Simulating physiological flexibility in the acute glucocorticoid response to stressors reveals limitations of current empirical approaches.

Wild animals often experience unpredictable challenges that demand rapid and flexible responses. The glucocorticoid mediated stress response is one of the major systems that allows vertebrates to rapidly adjust their physiology and behavior. Given its role in responding to challenges, evolutionary physiologists have focused on the consequences of between-individual and, more recently, within-individual variation in the acute glucocorticoid response. However, empirical studies of physiological flexibility are severely limited by the logistical challenges of measuring the same animal multiple times. Data simulation is a powerful approach when empirical data are limited, but has not been adopted to date in studies of physiological flexibility. In this article, I develop a simulation that can generate realistic acute glucocorticoid response data with user specified characteristics. Simulated animals can be sampled continuously through an acute response and across as many separate responses as desired, while varying key parameters. Using the simulation, I develop several scenarios that address key questions in physiological flexibility. These scenarios demonstrate the conditions under which a single glucocorticoid trait can be accurately assessed with typical experimental designs, the consequences of covariation between different components of the acute stress response, and the way that context specific differences in variability of acute responses can influence the power to detect relationships between the strength of the acute stress response and fitness. I also describe how to use the simulation tools to aid in the design and evaluation of empirical studies of physiological flexibility.

Control of Breathing in Ectothermic Vertebrates.

The ectothermic vertebrates are a diverse group that includes the Fishes (Agnatha, Chondrichthyes, and Osteichthyes), and the stem Tetrapods (Amphibians and Reptiles). From an evolutionary perspective, it is within this group that we see the origin of air-breathing and the transition from the use of water to air as a respiratory medium. This is accompanied by a switch from gills to lungs as the major respiratory organ and from oxygen to carbon dioxide as the primary respiratory stimulant. This transition first required the evolution of bimodal breathing (gas exchange with both water and air), the differential regulation of O2 and CO2 at multiple sites, periodic or intermittent ventilation, and unsteady states with wide oscillations in arterial blood gases. It also required changes in respiratory pump muscles (from buccopharyngeal muscles innervated by cranial nerves to axial muscles innervated by spinal nerves). The question of the extent to which common mechanisms of respiratory control accompany this progression is an intriguing one. While the ventilatory control systems seen in all extant vertebrates have been derived from common ancestors, the trends seen in respiratory control in the living members of each vertebrate class reflect both shared-derived features (ancestral traits) as well as unique specializations. In this overview article, we provide a comprehensive survey of the diversity that is seen in the afferent inputs (chemo and mechanoreceptor), the central respiratory rhythm generators, and the efferent outputs (drive to the respiratory pumps and valves) in this group. © 2022 American Physiological Society. Compr Physiol 12: 1-120, 2022.

An overview of the phylogeny of cardiorespiratory control in vertebrates with some reflections on the 'Polyvagal Theory'.

Mammals show clear changes in heart rate linked to lung ventilation, characterized as respiratory sinus arrhythmia (RSA). These changes are controlled in part by variations in the level of inhibitory control exerted on the heart by the parasympathetic arm of the autonomic nervous system (PNS). This originates from preganglionic neurons in the nucleus ambiguous that supply phasic, respiration-related activity to the cardiac branch of the vagus nerve, via myelinated, efferent fibres with rapid conduction velocities. An elaboration of these central mechanisms, under the control of a 'vagal system' has been endowed by psychologists with multiple functions concerned with 'social engagement' in mammals and, in particular, humans. Long-term study of cardiorespiratory interactions (CRI) in other major groups of vertebrates has established that they all show both tonic and phasic control of heart rate, imposed by the PNS. This derives centrally from neurones located in variously distributed nuclei, supplying the heart via fast-conducting, myelinated, efferent fibres. Water-breathing vertebrates, which include fishes and larval amphibians, typically show direct, 1:1 CRI between heart beats and gill ventilation, controlled from the dorsal vagal motor nucleus. In air-breathing, ectothermic vertebrates, including reptiles, amphibians and lungfish, CRI mirroring RSA have been shown to improve oxygen uptake during phasic ventilation by changes in perfusion of their respiratory organs, due to shunting of blood over across their undivided hearts. This system may constitute the evolutionary basis of that generating RSA in mammals, which now lacks a major physiological role in respiratory gas exchange, due to their completely divided systemic and pulmonary circulations.

Effects of the social environment on vertebrate fitness and health in nature: Moving beyond the stress axis.

Social interactions are a ubiquitous feature of the lives of vertebrate species. These may be cooperative or competitive, and shape the dynamics of social systems, with profound effects on individual behavior, physiology, fitness, and health. On one hand, a wealth of studies on humans, laboratory animal models, and captive species have focused on understanding the relationships between social interactions and individual health within the context of disease and pathology. On the other, ecological studies are attempting an understanding of how social interactions shape individual phenotypes in the wild, and the consequences this entails in terms of adaptation. Whereas numerous studies in wild vertebrates have focused on the relationships between social environments and the stress axis, much remains to be done in understanding how socially-related activation of the stress axis coordinates other key physiological functions related to health. Here, we review the state of our current knowledge on the effects that social interactions may have on other markers of vertebrate fitness and health. Building upon complementary findings from the biomedical and ecological fields, we identify 6 key physiological functions (cellular metabolism, oxidative stress, cellular senescence, immunity, brain function, and the regulation of biological rhythms) which are intimately related to the stress axis, and likely directly affected by social interactions. Our goal is a holistic understanding of how social environments affect vertebrate fitness and health in the wild. Whereas both social interactions and social environments are recognized as important sources of phenotypic variation, their consequences on vertebrate fitness, and the adaptive nature of social-stress-induced phenotypes, remain unclear. Social flexibility, or the ability of an animal to change its social behavior with resulting changes in social systems in response to fluctuating environments, has emerged as a critical underlying factor that may buffer the beneficial and detrimental effects of social environments on vertebrate fitness and health.

A cross-taxonomic perspective on the integration of temperature cues in vertebrate seasonal neuroendocrine pathways.

The regulation of seasonality has been an area of interest for decades, yet global climate change has created extra urgency in the quest to understand how sensory circuits and neuroendocrine control systems interact to generate flexibility in biological timekeeping. The capacity of temperature to alter endogenous or photoperiod-regulated neuroendocrine mechanisms driving seasonality, either as a direct cue or through temperature-dependent effects on energy and metabolism, is at the heart of this phenological flexibility. However, until relatively recently, little research had been done on the integration of temperature information in canonical seasonal neuroendocrine pathways, particularly in vertebrates. We review recent advances from research in vertebrates that deepens our understanding of how temperature cues are perceived and integrated into seasonal hypothalamic thyroid hormone (TH) signaling, which is a critical regulator of downstream seasonal phenotypic changes such as those regulated by the BPG (brain-pituitary-gonadal) axis. Temperature perception occurs through cutaneous transient receptor potential (TRP) neurons, though sensitivity of these neurons varies markedly across taxa. Although photoperiod is the dominant cue used to trigger seasonal physiology or entrain circannual clocks, across birds, mammals, fish, reptiles and amphibians, seasonality appears to be temperature sensitive and in at least some cases this appears to be related to phylogenetically conserved TH signaling in the hypothalamus. Nevertheless, the exact mechanisms through which temperature modulates seasonal neuroendocrine pathways remains poorly understood.

Blood pressure adaptation in vertebrates: comparative biology.

With evolution from water to land, the osmotic regulation of body fluids and cardiovascular systems of vertebrates evolved to cope with dryness and gravity. While aquatic vertebrates can use buoyancy to compensate for the effects of gravity, terrestrial vertebrates cannot and must circulate blood throughout their body-a necessity that likely led to the development of strong hearts and high blood pressure. These changes may be supported by anatomic evolution of the cardiovascular system and by functional evolution, with alterations in hormonal systems. Thus, during the evolution of terrestrial animals, increased performance of body functions to endure harsher environments was required, necessitating increased blood pressure. In an age of overeating and insufficient exercise, modern man does not fully use the high levels of physical functions acquired through evolution. Drastic changes in our living environment cause hypertension, the pathogenesis of which remains unknown. To survive in new environments, as might be expected in outer space or underwater, an understanding is required of how changes in blood pressure have occurred that enabled adaptation through evolution in vertebrates.