The biomechanics of animal limbs has evolved to meet the functional demands for movement associated with different behaviors and environments. Effective movement relies not only on limb mechanics but ...also on appropriate mechanosensory feedback. By comparing sensory ability and mechanics within a phylogenetic framework, we show that peripheral mechanosensation has evolved with limb biomechanics, evolutionarily tuning the neuromechanical system to its functional demands. We examined sensory physiology and mechanics of the pectoral fins, forelimb homologs, in the fish family Labridae. Labrid fishes exhibit extraordinary morphological and behavioral diversity and use pectoral fin-based propulsion with fins ranging in shape from high aspect ratio (AR) wing-like fins to low AR paddle-like fins. Phylogenetic character analysis demonstrates that high AR fins evolved independently multiple times in this group. Four pairs of species were examined; each included a plesiomorphic low AR and a high AR species. Within each species pair, the high AR species demonstrated significantly stiffer fin rays in comparison with the low AR species. Afferent sensory nerve activity was recorded during fin ray bending. In all cases, afferents of stiffer fins were more sensitive at lower displacement amplitudes, demonstrating mechanosensory tuning to fin mechanics and a consistent pattern of correlated evolution. We suggest that these data provide a clear example of parallel evolution in a complex neuromechanical system, with a strong link between multiple phenotypic characters: pectoral fin shape, swimming behavior, fin ray stiffness, and mechanosensory sensitivity.
Blinking, the transient occlusion of the eye by one or more membranes, serves several functions including wetting, protecting, and cleaning the eye. This behavior is seen in nearly all living ...tetrapods and absent in other extant sarcopterygian lineages suggesting that it might have arisen during the water-to-land transition. Unfortunately, our understanding of the origin of blinking has been limited by a lack of known anatomical correlates of the behavior in the fossil record and a paucity of comparative functional studies. To understand how and why blinking originates, we leverage mudskippers (Oxudercinae), a clade of amphibious fishes that have convergently evolved blinking. Using microcomputed tomography and histology, we analyzed two mudskipper species,
and
, and compared them to the fully aquatic round goby,
. Study of gross anatomy and epithelial microstructure shows that mudskippers have not evolved novel musculature or glands to blink. Behavioral analyses show the blinks of mudskippers are functionally convergent with those of tetrapods:
blinks more often under high-evaporation conditions to wet the eye, a blink reflex protects the eye from physical insult, and a single blink can fully clean the cornea of particulates. Thus, eye retraction in concert with a passive occlusal membrane can achieve functions associated with life on land. Osteological correlates of eye retraction are present in the earliest limbed vertebrates, suggesting blinking capability. In both mudskippers and tetrapods, therefore, the origin of this multifunctional innovation is likely explained by selection for increasingly terrestrial lifestyles.
Mechanosensation is a universal feature of animals that is essential for behavior, allowing detection of animals’ own body movement and position as well as physical characteristics of the ...environment. The extraordinary morphological and behavioral diversity that exists across fish species provide rich opportunities for comparative mechanosensory studies in fins. The fins of fishes have been found to function as proprioceptors, by providing feedback on fin ray position and movement, and as tactile sensors, by encoding pressures applied to the fin surface. Across fish species, and among fins, the afferent response is remarkably consistent, suggesting that the ability of fin rays and membrane to sense deformation is a fundamental feature of fish fins. While fin mechanosensation has been known in select, often highly specialized, species for decades, only in the last decade have we explored mechanosensation in typical propulsive fins and considered its role in behavior, particularly locomotion. In this paper, we synthesize the current understanding of the anatomy and physiology of fin mechanosensation, looking toward key directions for research. We argue that a mechanosensory perspective informs studies of fin-based propulsion and other fin-driven behaviors and should be considered in the interpretation of fin morphology and behavior. In addition, we compare the mechanosensory system innervating the fins of fishes to the systems innervating the limbs of mammals and wings of insects in order to identify shared mechanosensory strategies and how different organisms have evolved to meet similar functional challenges. Finally, we discuss how understanding the biological organization and function of fin sensors can inform the design of control systems for engineered fins and fin-driven robotics.
Mechanosensation in an adipose fin Aiello, Brett R.; Stewart, Thomas A.; Hale, Melina E.
Proceedings - Royal Society. Biological sciences/Proceedings - Royal Society. Biological Sciences,
03/2016, Letnik:
283, Številka:
1826
Journal Article
Recenzirano
Odprti dostop
Adipose fins are found on approximately 20% of ray-finned fish species. The apparently rudimentary anatomy of adipose fins inspired a longstanding hypothesis that these fins are vestigial and lack ...function. However, adipose fins have evolved repeatedly within Teleostei, suggesting adaptive function. Recently, adipose fins were proposed to function as mechanosensors, detecting fluid flow anterior to the caudal fin. Here we test the hypothesis that adipose fins are mechanosensitive in the catfish Corydoras aeneus. Neural activity, recorded from nerves that innervate the fin, was shown to encode information on both movement and position of the fin membrane, including the magnitude of fin membrane displacement. Thus, the adipose fin of C. aeneus is mechanosensitive and has the capacity to function as a ‘precaudal flow sensor’. These data force re-evaluation of adipose fin clipping, a common strategy for tagging fishes, and inform hypotheses of how function evolves in novel vertebrate appendages.
Across insects, wing shape and size have undergone dramatic divergence even in closely related sister groups. However, we do not know how morphology changes in tandem with kinematics to support body ...weight within available power and how the specific force production patterns are linked to differences in behaviour. Hawkmoths and wild silkmoths are diverse sister families with divergent wing morphology. Using three-dimensional kinematics and quasi-steady aerodynamic modelling, we compare the aerodynamics and the contributions of wing shape, size and kinematics in 10 moth species. We find that wing movement also diverges between the clades and underlies two distinct strategies for flight. Hawkmoths use wing kinematics, especially high frequencies, to enhance force and wing morphologies that reduce power. Silkmoths use wing morphology to enhance force, and slow, high-amplitude wingstrokes to reduce power. Both strategies converge on similar aerodynamic power and can support similar body weight ranges. However, inter-clade within-wingstroke force profiles are quite different and linked to the hovering flight of hawkmoths and the bobbing flight of silkmoths. These two moth groups fly more like other, distantly related insects than they do each other, demonstrating the diversity of flapping flight evolution and a rich bioinspired design space for robotic flappers.
The evolution of flapping flight is linked to the prolific success of insects. Across Insecta, wing morphology diversified, strongly impacting aerodynamic performance. In the presence of ecological ...opportunity, discrete adaptive shifts and early bursts are two processes hypothesized to give rise to exceptional morphological diversification. Here, we use the sister-families Sphingidae and Saturniidae to answer how the evolution of aerodynamically important traits is linked to clade divergence and through what process(es) these traits evolve. Many agile Sphingidae evolved hover feeding behaviours, while adult Saturniidae lack functional mouth parts and rely on a fixed energy budget as adults. We find that Sphingidae underwent an adaptive shift in wing morphology coincident with life history and behaviour divergence, evolving small high aspect ratio wings advantageous for power reduction that can be moved at high frequencies, beneficial for flight control. By contrast, Saturniidae, which do not feed as adults, evolved large wings and morphology which surprisingly does not reduce aerodynamic power, but could contribute to their erratic flight behaviour, aiding in predator avoidance. We suggest that after the evolution of flapping flight, diversification of wing morphology can be potentiated by adaptative shifts, shaping the diversity of wing morphology across insects.
The functional capabilities of flexible, propulsive appendages are directly influenced by their mechanical properties. The fins of fishes have undergone extraordinary evolutionary diversification in ...structure and function, which raises questions of how fin mechanics relate to swimming behavior. In the fish family Labridae, pectoral fin swimming behavior ranges from rowing to flapping. Rowers are more maneuverable than flappers, but flappers generate greater thrust at high speeds and achieve greater mechanical efficiency at all speeds. Interspecific differences in hydrodynamic capability are largely dependent on fin kinematics and deformation, and are expected to correlate with fin stiffness. Here we examine fin ray stiffness in two closely related species that employ divergent swimming behaviors, the flapping
and the rowing
To determine the spatial distribution of flexural stiffness across the fin, we performed three-point bending tests at the center of the proximal, middle and distal regions of four equally spaced fin rays. Pectoral fin ray flexural stiffness ranged from 0.0001 to 1.5109 µN m
, and the proximal regions of
fin rays were nearly an order of magnitude stiffer than those of
In both species, fin ray flexural stiffness decreased exponentially along the proximodistal span of fin rays, and flexural stiffness decreased along the fin chord from the leading to the trailing edge. Furthermore, the proportion of fin area occupied by fin rays was significantly greater in
than in
, suggesting that the proportion of fin ray to fin area contributes to differences in fin mechanics.
For many fish species, rhythmic movement of the pectoral fins, or forelimbs, drives locomotion. In terrestrial vertebrates, normal limb-based rhythmic gaits require ongoing modulation with limb ...mechanosensors. Given the complexity of the fluid environment and dexterity of fish swimming through it, we hypothesize that mechanosensory modulation is also critical to normal fin-based swimming. Here, we examined the role of sensory feedback from the pectoral fin rays and membrane on the neuromuscular control and kinematics of pectoral fin-based locomotion. Pectoral fin kinematics and electromyograms of the six major fin muscles of the parrotfish,
, a high-performance pectoral fin swimmer, were recorded during steady swimming before and after bilateral transection of the sensory nerves extending into the rays and surrounding membrane. Alternating activity of antagonistic muscles was observed and drove the fin in a figure-of-eight fin stroke trajectory before and after nerve transection. After bilateral transections, pectoral fin rhythmicity remained the same or increased. Differences in fin kinematics with the loss of sensory feedback also included fin kinematics with a significantly more inclined stroke plane angle, an increased angular velocity and fin beat frequency, and a transition to the body-caudal fin gait at lower speeds. After transection, muscles were active over a larger proportion of the fin stroke, with overlapping activation of antagonistic muscles rarely observed in the trials of intact fish. The increased overlap of antagonistic muscle activity might stiffen the fin system in order to enhance control and stability in the absence of sensory feedback from the fin rays. These results indicate that fin ray sensation is not necessary to generate the underlying rhythm of fin movement, but contributes to the specification of pectoral fin motor pattern and movement during rhythmic swimming.
Sensory Feedback and Animal Locomotion Aiello, Brett R.; Gillis, Gary B.; Fox, Jessica L.
Integrative and comparative biology,
11/2018, Letnik:
58, Številka:
5
Journal Article
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The successful completion of many behaviors relies on sensory feedback. This symposium brought together researchers using novel techniques to study how different stimuli are encoded, how and where ...multimodal feedback is integrated, and how feedback modulates motor output in diverse modes of locomotion (aerial, aquatic, and terrestrial) in a diverse range of taxa (insects, fish, tetrapods), and in robots. Similar to biological organisms, robots can be equipped with integrated sensors and can rely on sensory feedback to adjust the output signal of a controller. Engineers often look to biology for inspiration on how animals have evolved solutions to problems similar to those experienced in robotic movement. Similarly, biologists too must proactively engage with engineers to apply computer and robotic models to test hypotheses and answer questions on the capacity and roles of sensory feedback in generating effective movement. Through a diverse group of researchers, including both biologists and engineers, the symposium attempted to catalyze new interdisciplinary collaborations and identify future research directions for the development of bioinspired sensory control systems, as well as the use of robots to test hypotheses in neuromechanics.
•Campaniform sensilla (CS), distributed across insect wings, sense local wing strain.•Placement of CS determines sensory information available to the animal.•CS placement varies across Insecta but ...there are some general trends.•Merging phylogenetic methods and computational modeling will help reveal principles of CS placement.
Insect wings serve two crucial functions in flight: propulsion and sensing. During flapping flight, complex spatiotemporal patterns of strain on the wing reflect mechanics, kinematics, and external perturbations; sensing wing deformation provides feedback necessary for flight control. Campaniform sensilla distributed across the wing transduce local strain fluctuations into neural signals, so their placement on the wing determines sensory information available to the insect. Thus, understanding the significance of these sensor locations will also reveal how sensing and wing movement are coupled. Here, we identify trends in wing campaniform sensilla placement across flying insects from the literature. We then discuss how these patterns can influence sensory encoding by wing mechanosensors. Finally, we propose combining a comparative approach on model insect clades with computational modeling, leveraging the spectacular natural diversity in wings to uncover biological principles of mechanosensory feedback in flight control.
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