RESUMO
Many animals migrate across regions of their geographic range as parts of extended events, with groups of individuals proceeding through areas of travel on several successive days. Early migrating individuals may have an advantage over late migrating individuals by gaining early access to the resources at the eventual destination. For situations where early access to resources would provide an advantage, specific sets of locomotor traits might be found among individuals that are earlier migrators. We tested for associations between migration timing and traits related to escape responses, climbing, and morphology in the amphidromous Hawaiian stream goby, 'o'opu nopili (Sicyopterus stimpsoni). In this species, juvenile fish migrate in pulses over several days immediately following flash floods. We collected daily measurements of escape responses and waterfall climbing from juvenile fish arriving at streams from the ocean. We found that escape performance showed mainly stochastic variation across migrating individuals tested on successive days. In contrast, some metrics of climbing performance decrease over successive pulses during a migration event. We also found more variation in body shape among fish from early pulses during migration events compared to later pulses. These results could have implications for guiding conservation efforts, identifying critical time windows for protection as periods with the greatest likelihood of successful migrants.
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Teleost fishes have evolved a number of sound-producing mechanisms, including vibrations of the swim bladder. In addition to sound production, the swim bladder also aids in sound reception. While the production and reception of sound by the swim bladder has been described separately in fishes, the extent to which it operates for both in a single species is unknown. Here, using morphological, electrophysiological and modelling approaches, we show that the swim bladder of male plainfin midshipman fish (Porichthys notatus) exhibits reproductive state-dependent changes in morphology and function for sound production and reception. Non-reproductive males possess rostral 'horn-like' swim bladder extensions that enhance low-frequency (less than 800 Hz) sound pressure sensitivity by decreasing the distance between the swim bladder and inner ear, thus enabling pressure-induced swim bladder vibrations to be transduced to the inner ear. By contrast, reproductive males display enlarged swim bladder sonic muscles that enable the production of advertisement calls but also alter swim bladder morphology and increase the swim bladder to inner ear distance, effectively reducing sound pressure sensitivity. Taken together, we show that the swim bladder exhibits a seasonal functional plasticity that allows it to effectively mediate both the production and reception of sound in a vocal teleost fish.
Assuntos
Batracoidiformes , Comunicação , Som , Animais , Masculino , Acústica , Batracoidiformes/fisiologia , Estruturas AnimaisRESUMO
Movement is an important characteristic of an animal's ecology, reflecting the perception of and response to environmental conditions. To effectively search for food, movement patterns likely depend on habitat characteristics and the sensory systems used to find prey. We examined movements associated with foraging for two sympatric species of lizards inhabiting the Great Basin Desert of southeastern Oregon. The two species have largely overlapping diets but find prey via different sensory cues, which link to their differing foraging strategies-the long-nosed leopard lizard, Gambelia wislizenii, is a visually-oriented predator, while the western whiptail, Aspidoscelis tigris, relies more heavily on chemosensory cues to find prey. Using detailed focal observations, we characterized the habitat use and movement paths of each species. We placed markers at the location of focal animals every minute for the duration of each 30-min observation. Afterward, we recorded whether each location was in the open or in vegetation, as well as the movement metrics of step length, path length, net displacement, straightness index, and turn angle, and then made statistical comparisons between the two species. The visual forager spent more time in open areas, moved less frequently over shorter distances, and differed in patterns of plant use compared to the chemosensory forager. Path characteristics of step length and turn angle differed between species. The visual predator moved in a way that was consistent with the notion that they require a clear visual path to stalk prey whereas the movement of the chemosensory predator increased their chances of detecting prey by venturing further into vegetation. Sympatric species can partition limited resources through differences in search behavior and habitat use.
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Across vertebrate diversity, limb bone morphology is typically expected to reflect differences in the habitats and functional tasks that species utilize. Arboreal vertebrates are often recognized to have longer limbs than terrestrial relatives, a feature thought to help extend the reach of limbs across gaps between branches. Among terrestrial vertebrates, longer limbs can experience greater bending moments that might expose bones to a greater risk of failure. However, changes in habitat or behavior can impose changes in the forces that bones experience. If locomotion imposed lower loads in trees than on the ground, such a release from loading demands might have produced conditions under which potential constraints on the evolution of long limbs were removed, making it easier for them to evolve in arboreal species. We tested for such environmental differences in limb bone loading using the green iguana (Iguana iguana), a species that readily walks over ground and climbs trees. We implanted strain gauges on the humerus and femur, and then compared loads between treatments modeling substrate conditions of arboreal habitats. For hindlimbs, inclined substrate angles were most correlated with strain increases, whereas the forelimbs had a similar pattern but of lesser magnitude. Unlike some other habitat transitions, these results do not support biomechanical release as a mechanism likely to have facilitated limb elongation. Instead, limb bone adaptations in arboreal habitats were likely driven by selective pressures other than responses to skeletal loading.
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Iguanas , Animais , Árvores , Extremidade Inferior , Aclimatação , VertebradosRESUMO
The functional capacities of animals are a primary factor determining survival in nature. In this context, understanding the biomechanical performance of animals can provide insight into diverse aspects of their biology, ranging from ecological distributions across habitat gradients to the evolutionary diversification of lineages. To survive and reproduce in the face of environmental pressures, animals must perform a wide range of tasks, some of which entail tradeoffs between competing demands. Moreover, the demands encountered by animals can change through ontogeny as they grow, sexually mature or migrate across environmental gradients. To understand how mechanisms that underlie functional performance contribute to survival and diversification across challenging and variable habitats, we have pursued diverse studies of the comparative biomechanics of amphidromous goby fishes across functional requirements ranging from prey capture and fast-start swimming to adhesion and waterfall climbing. The pan-tropical distribution of these fishes has provided opportunities for repeated testing of evolutionary hypotheses. By synthesizing data from the lab and field, across approaches spanning high-speed kinematics, selection trials, suction pressure recordings, mechanical property testing, muscle fiber-type measurements and physical modeling of bioinspired designs, we have clarified how multiple axes of variation in biomechanical performance associate with the ecological and evolutionary diversity of these fishes. Our studies of how these fishes meet both common and extreme functional demands add new, complementary perspectives to frameworks developed from other systems, and illustrate how integrating knowledge of the mechanical underpinnings of diverse aspects of performance can give critical insights into ecological and evolutionary questions.
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Evolução Biológica , Peixes , Animais , Fenômenos Biomecânicos , Peixes/fisiologia , Natação , EcossistemaRESUMO
Genetic diseases affecting the skeletal system present with a wide range of symptoms that make diagnosis and treatment difficult. Genome-wide association and sequencing studies have identified genes linked to human skeletal diseases. Gene editing of zebrafish models allows researchers to further examine the link between genotype and phenotype, with the long-term goal of improving diagnosis and treatment. While current automated tools enable rapid and in-depth phenotyping of the axial skeleton, characterizing the effects of mutations on the craniofacial skeleton has been more challenging. The objective of this study was to evaluate a semi-automated screening tool can be used to quantify craniofacial variations in zebrafish models using four genes that have been associated with human skeletal diseases (meox1, plod2, sost, and wnt16) as test cases. We used traditional landmarks to ground truth our dataset and pseudolandmarks to quantify variation across the 3D cranial skeleton between the groups (somatic crispant, germline mutant, and control fish). The proposed pipeline identified variation between the crispant or mutant fish and control fish for four genes. Variation in phenotypes parallel human craniofacial symptoms for two of the four genes tested. This study demonstrates the potential as well as the limitations of our pipeline as a screening tool to examine multi-dimensional phenotypes associated with the zebrafish craniofacial skeleton.
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Estudo de Associação Genômica Ampla , Peixe-Zebra , Animais , Humanos , Peixe-Zebra/genética , Osso e Ossos , Proteínas de Peixe-Zebra/genética , Fenótipo , Proteínas Wnt/genéticaRESUMO
Due to the complexity of fish skulls, previous attempts to classify craniofacial phenotypes have relied on qualitative features or sparce 2D landmarks. In this work we aim to identify previously unknown 3D craniofacial phenotypes with a semiautomated pipeline in adult zebrafish mutants. We first estimate a synthetic 'normative' zebrafish template using MicroCT scans from a sample pool of wild-type animals using the Advanced Normalization Tools (ANTs). We apply a computational anatomy (CA) approach to quantify the phenotype of zebrafish with disruptions in bmp1a, a gene implicated in later skeletal development and whose human ortholog when disrupted is associated with Osteogenesis Imperfecta. Compared to controls, the bmp1a fish have larger otoliths, larger normalized centroid sizes, and exhibit shape differences concentrated around the operculum, anterior frontal, and posterior parietal bones. Moreover, bmp1a fish differ in the degree of asymmetry. Our CA approach offers a potential pipeline for high-throughput screening of complex fish craniofacial shape to discover novel phenotypes for which traditional landmarks are too sparce to detect. The current pipeline successfully identifies areas of variation in zebrafish mutants, which are an important model system for testing genome to phenome relationships in the study of development, evolution, and human diseases. This article has an associated First Person interview with the first author of the paper.
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Crânio , Peixe-Zebra , Animais , Humanos , Fenótipo , Crânio/anatomia & histologia , Microtomografia por Raio-X , Peixe-Zebra/genéticaRESUMO
Locomotor force production imposes strong demands on organismal form. Thus, the evolution of novel locomotor modes is often associated with morphological adaptations that help to meet those demands. In the goby lineage of fishes, most species are marine and use their fused pelvic fins to facilitate station holding in wave-swept environments. However, several groups of gobies have evolved an amphidromous lifecycle, in which larvae develop in the ocean but juveniles migrate to freshwater for their adult phase. In many of these species, the pelvic fins have been co-opted to aid in climbing waterfalls during upstream migrations to adult habitats. During horizontal swimming, forces are produced by axial musculature pulling on the vertebral column. However, during vertical climbing, gravity also exerts forces along the length of the vertebral column. In this study, we searched for novel aspects of vertebral column form that might be associated with the distinctive locomotor strategies of climbing gobies. We predicted that stiffness would vary along the length of the vertebral column due to competing demands for stability of the suction disk anteriorly and flexibility for axial thrust production posteriorly. We also predicted that derived, climbing goby species would require stiffer backbones to aid in vertical thrust production compared to non-climbing species. To test these predictions, we used microcomputed tomography scans to compare vertebral anatomy (centrum length, centrum width, and intervertebral space) along the vertebral column for five gobioid species that differ in climbing ability. Our results support our second prediction, that gobies are more flexible in the posterior portion of the body. However, the main variation in vertebral column form associated with climbing ability was the presence of larger intervertebral spaces in Sicyopterus stimpsoni, a species that uses a distinctive inching behavior to climb. These results build on past kinematic studies of goby climbing performance and lend insights into how the underlying vertebral structure of these fishes may enable their novel locomotion.
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Adaptação Fisiológica/fisiologia , Ecossistema , Locomoção/fisiologia , Perciformes/anatomia & histologia , Coluna Vertebral/anatomia & histologia , Animais , Fenômenos Biomecânicos/fisiologia , Perciformes/fisiologia , Coluna Vertebral/fisiologiaRESUMO
Assessing the factors that contribute to successful locomotor performance can provide critical insight into how animals survive in challenging habitats. Locomotion is powered by muscles, so that differences in the relative proportions of red (slow-oxidative) vs. white (fast-glycolytic) fibers can have significant implications for locomotor performance. We compared the relative proportions of axial red muscle fibers between groups of juveniles of the amphidromous gobiid fish, Sicyopterus stimpsoni, from the Hawaiian Islands. Juveniles of this species migrate from the ocean into freshwater streams, navigating through a gauntlet of predators that require rapid escape responses, before reaching waterfalls which must be climbed (using a slow, inching behavior) to reach adult breeding habitats. We found that fish from Kaua'i have a smaller proportion of red fibers in their tail muscles than fish from Hawai'i, matching expectations based on the longer pre-waterfall stream reaches of Kaua'i that could increase exposure to predators, making reduction of red muscle and increases in white muscle advantageous. However, no difference in red muscle proportions was identified between fish that were either successful or unsuccessful in scaling model waterfalls during laboratory climbing trials, suggesting that proportions of red muscle are near a localized fitness peak among Hawaiian individuals.
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Ecossistema , Peixes/anatomia & histologia , Locomoção/fisiologia , Fibras Musculares Esqueléticas/fisiologia , Músculo Esquelético/anatomia & histologia , Animais , Peixes/fisiologia , Havaí , Músculo Esquelético/fisiologia , RiosRESUMO
Experimental measurements of escape performance in fishes have typically been conducted in still water; however, many fishes inhabit environments with flow that could impact escape behavior. We examined the influences of flow and predator attack direction on the escape behavior of fish, using juveniles of the amphidromous Hawaiian goby Sicyopterus stimpsoni In nature, these fish must escape ambush predation while moving through streams with high-velocity flow. We measured the escape performance of juvenile gobies while exposing them to a range of water velocities encountered in natural streams and stimulating fish from three different directions. Frequency of response across treatments indicated strong effects of flow conditions and attack direction. Juvenile S. stimpsoni had uniformly high response rates for attacks from a caudal direction (opposite flow); however, response rates for attacks from a cranial direction (matching flow) decreased dramatically as flow speed increased. Mechanical stimuli produced by predators attacking in the same direction as flow might be masked by the flow environment, impairing the ability of prey to detect attacks. Thus, the likelihood of successful escape performance in fishes can depend critically on environmental context.