The tempo of species diversification in large clades can reveal fundamental evolutionary mechanisms that operate on large temporal and spatial scales 1–4. Hummingbirds have radiated into a diverse ...assemblage of specialized nectarivores comprising 338 species, but their evolutionary history has not, until now, been comprehensively explored. We studied hummingbird diversification by estimating a time-calibrated phylogeny for 284 hummingbird species, demonstrating that hummingbirds invaded South America by ∼22 million years ago, and subsequently diversified into nine principal clades (see 5–7). Using ancestral state reconstruction and diversification analyses, we (1) estimate the age of the crown-group hummingbird assemblage, (2) investigate the timing and patterns of lineage accumulation for hummingbirds overall and regionally, and (3) evaluate the role of Andean uplift in hummingbird speciation. Detailed analyses reveal disparate clade-specific processes that allowed for ongoing species diversification. One factor was significant variation among clades in diversification rates. For example, the nine principal clades of hummingbirds exhibit ∼15-fold variation in net diversification rates, with evidence for accelerated speciation of a clade that includes the Bee, Emerald, and Mountain Gem groups of hummingbirds. A second factor was colonization of key geographic regions, which opened up new ecological niches. For example, some clades diversified in the context of the uplift of the Andes Mountains, whereas others were affected by the formation of the Panamanian land bridge. Finally, although species accumulation is slowing in all groups of hummingbirds, several major clades maintain rapid rates of diversification on par with classical examples of rapid adaptive radiation.
•We present a time-calibrated multilocus phylogeny for 284 species of hummingbirds•Hummingbird diversification began ∼22 million years ago•Hummingbirds diversified rapidly, but via heterogeneous clade-specific processes•Invasion of new land areas such as the Andes and North America spurred diversification
McGuire et al. generated a time-calibrated multilocus phylogeny of hummingbirds and use it to explore the diversification dynamics of this species-rich New World assemblage. They find that hummingbird diversification began about 22 million years ago and was driven by highly heterogeneous clade-specific and regional diversification processes.
Hummingbirds use distinct control strategies for forward and hovering flight Baliga, Vikram B; Dakin, Roslyn; Wylie, Douglas R ...
Proceedings - Royal Society. Biological sciences/Proceedings - Royal Society. Biological Sciences,
2024-Jan-10, 2024-01-10, 20240110, Letnik:
291, Številka:
2014
Journal Article
Recenzirano
Odprti dostop
The detection of optic flow is important for generating optomotor responses to mediate retinal image stabilization, and it can also be used during ongoing locomotion for centring and velocity ...control. Previous work in hummingbirds has separately examined the roles of optic flow during hovering and when centring through a narrow passage during forward flight. To develop a hypothesis for the visual control of forward flight velocity, we examined the behaviour of hummingbirds in a flight tunnel where optic flow could be systematically manipulated. In all treatments, the animals exhibited periods of forward flight interspersed with bouts of spontaneous hovering. Hummingbirds flew fastest when they had a reliable signal of optic flow. All optic flow manipulations caused slower flight, suggesting that hummingbirds had an expected optic flow magnitude that was disrupted. In addition, upward and downward optic flow drove optomotor responses for maintaining altitude during forward flight. When hummingbirds made voluntary transitions to hovering, optomotor responses were observed to all directions. Collectively, these results are consistent with hummingbirds controlling flight speed via mechanisms that use an internal forward model to predict expected optic flow whereas flight altitude and hovering position are controlled more directly by sensory feedback from the environment.
Relatively little is known about how sensory information is used for controlling flight in birds. A powerful method is to immerse an animal in a dynamic virtual reality environment to examine ...behavioral responses. Here, we investigated the role of vision during free-flight hovering in hummingbirds to determine how optic flow—image movement across the retina—is used to control body position. We filmed hummingbirds hovering in front of a projection screen with the prediction that projecting moving patterns would disrupt hovering stability but stationary patterns would allow the hummingbird to stabilize position. When hovering in the presence of moving gratings and spirals, hummingbirds lost positional stability and responded to the specific orientation of the moving visual stimulus. There was no loss of stability with stationary versions of the same stimulus patterns. When exposed to a single stimulus many times or to a weakened stimulus that combined a moving spiral with a stationary checkerboard, the response to looming motion declined. However, even minimal visual motion was sufficient to cause a loss of positional stability despite prominent stationary features. Collectively, these experiments demonstrate that hummingbirds control hovering position by stabilizing motions in their visual field. The high sensitivity and persistence of this disruptive response is surprising, given that the hummingbird brain is highly specialized for sensory processing and spatial mapping, providing other potential mechanisms for controlling position.
Significance The avian brain has numerous specializations for navigation and processing visual information, but relatively little is known about how flying birds control their position in space. To study the role of vision in controlling hovering flight, we developed a virtual reality environment where visual patterns could be displayed to a freely flying hummingbird. Normal flight could only be performed if the visual background was completely stationary. In contrast, any motion in the background image caused the birds to lose stability. In natural settings, visual motion is constantly produced when objects and observers move relative to each other. This research demonstrates that flying birds are surprisingly sensitive to movements in their visual field and direct flight to respond to those movements.
Avian flight is guided by optic flow—the movement across the retina of images of surfaces and edges in the environment due to self-motion. In all vertebrates, there is a short pathway for optic flow ...information to reach pre-motor areas: retinal-recipient regions in the midbrain encode optic flow, which is then sent to the cerebellum. One well-known role for optic flow pathways to the cerebellum is the control of stabilizing eye movements (the optokinetic response). However, the role of this pathway in controlling locomotion is less well understood. Electrophysiological and tract tracing studies are revealing the functional connectivity of a more elaborate circuit through the avian cerebellum, which integrates optic flow with other sensory signals. Here we review the research supporting this framework and identify the cerebellar output centres, the lateral (CbL) and medial (CbM) cerebellar nuclei, as two key nodes with potentially distinct roles in flight control. The CbM receives bilateral optic flow information and projects to sites in the brainstem that suggest a primary role for flight control over time, such as during forward flight. The CbL receives monocular optic flow and other types of visual information. This site provides feedback to sensory areas throughout the brain and has a strong projection the nucleus ruber, which is known to have a dominant role in forelimb muscle control. This arrangement suggests primary roles for the CbL in the control of wing morphing and for rapid maneuvers.
All visual animals experience optic flow—global visual motion across the retina, which is used to control posture and movement.1 The midbrain circuitry for optic flow is highly conserved in ...vertebrates,2–6 and these neurons show similar response properties across tetrapods.4,7–16 These neurons have large receptive fields and exhibit both direction and velocity selectivity in response to large moving stimuli. Hummingbirds deviate from the typical vertebrate pattern in several respects.17,18 Their lentiformis mesencephali (LM) lacks the directional bias seen in other tetrapods and has an overall bias for faster velocities. This led Ibbotson19 to suggest that the hummingbird LM may be specialized for hovering close to visual structures, such as plants. In such an environment, even slight body motions will translate into high-velocity optic flow. A prediction from this hypothesis is that hummingbird LM neurons should be more responsive to large visual features. We tested this hypothesis by measuring neural responses of hummingbirds and zebra finches to sine wave gratings of varying spatial and temporal frequencies. As predicted, the hummingbird LM displayed an overall preference for fast optic flow because neurons were biased to lower spatial frequencies. These neurons were also tightly tuned in the spatiotemporal domain. We found that the zebra finch LM specializes along another domain: many neurons were initially tuned to high temporal frequencies followed by a shift in location and orientation to slower velocity tuning. Collectively, these results demonstrate that the LM has distinct and specialized tuning properties in at least two bird species.
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•Hummingbird LM cells are tightly tuned to fast optic flow and low spatial frequency•Tuning of zebra finch LM neurons changes from initial to steady-state responses•Many zebra finch LM neurons are velocity oriented during steady state•Hummingbirds and zebra finches exhibit different specializations in optic flow tuning
Midbrain optic flow neurons share many features among tetrapods, but Smyth et al. show that LM cells of hummingbirds and zebra finches exhibit different specializations. Hummingbird cells are tuned to fast optic flow because they prefer low spatial frequency. Zebra finch cell tuning shifts with time, and at steady state, many are velocity oriented.
Hummingbird vision Altshuler, Douglas L.; Wylie, Douglas R.
CB/Current biology,
02/2020, Letnik:
30, Številka:
3
Journal Article
Recenzirano
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Hummingbirds are widely recognized by their hovering flight. In this Quick guide, Altshuler and Wylie describe the visual specializations that allow for the hummingbird’s flight abilities.
Airplanes and helicopters use high aspect ratio wings to reduce the power required to fly, but must operate at low angle of attack to prevent flow separation and stall. Animals capable of slow ...sustained flight, such as hummingbirds, have low aspect ratio wings and flap their wings at high angle of attack without stalling. Instead, they generate an attached vortex along the leading edge of the wing that elevates lift. Previous studies have demonstrated that this vortex and high lift can be reproduced by revolving the animal wing at the same angle of attack. How do flapping and revolving animal wings delay stall and reduce power? It has been hypothesized that stall delay derives from having a short radial distance between the shoulder joint and wing tip, measured in chord lengths. This non-dimensional measure of wing length represents the relative magnitude of inertial forces versus rotational accelerations operating in the boundary layer of revolving and flapping wings. Here we show for a suite of aspect ratios, which represent both animal and aircraft wings, that the attachment of the leading edge vortex on a revolving wing is determined by wing aspect ratio, defined with respect to the centre of revolution. At high angle of attack, the vortex remains attached when the local radius is shorter than four chord lengths and separates outboard on higher aspect ratio wings. This radial stall limit explains why revolving high aspect ratio wings (of helicopters) require less power compared with low aspect ratio wings (of hummingbirds) at low angle of attack and vice versa at high angle of attack.
Animals exhibit an abundant diversity of forms, and this diversity is even more evident when considering animals that can change shape on demand. The evolution of flexibility contributes to aspects ...of performance from propulsive efficiency to environmental navigation. It is, however, challenging to quantify and compare body parts that, by their nature, dynamically vary in shape over many time scales. Commonly, body configurations are tracked by labelled markers and quantified parametrically through conventional measures of size and shape (descriptor approach) or non-parametrically through data-driven analyses that broadly capture spatiotemporal deformation patterns (shape variable approach). We developed a weightless marker tracking technique and combined these analytic approaches to study wing morphological flexibility in hoverfeeding Anna's hummingbirds (Calypte anna). Four shape variables explained >95% of typical stroke cycle wing shape variation and were broadly correlated with specific conventional descriptors such as wing twist and area. Moreover, shape variables decomposed wing deformations into pairs of in-plane and out-of-plane components at integer multiples of the stroke frequency. This property allowed us to identify spatiotemporal deformation profiles characteristic of hoverfeeding with experimentally imposed kinematic constraints, including through shape variables explaining <10% of typical shape variation. Hoverfeeding in front of a visual barrier restricted stroke amplitude and elicited increased stroke frequencies together with in-plane and out-of-plane deformations throughout the stroke cycle. Lifting submaximal loads increased stroke amplitudes at similar stroke frequencies together with prominent in-plane deformations during the upstroke and pronation. Our study highlights how spatially and temporally distinct changes in wing shape can contribute to agile fluidic locomotion.
Over the last half century, work with flies, bees, and moths have revealed a number of visual guidance strategies for controlling different aspects of flight. Some algorithms, such as the use of ...pattern velocity in forward flight, are employed by all insects studied so far, and are used to control multiple flight tasks such as regulation of speed, measurement of distance, and positioning through narrow passages. Although much attention has been devoted to long-range navigation and homing in birds, until recently, very little was known about how birds control flight in a moment-to-moment fashion. A bird that flies rapidly through dense foliage to land on a branch-as birds often do-engages in a veritable three-dimensional slalom, in which it has to continually dodge branches and leaves, and find, and possibly even plan a collision-free path to the goal in real time. Each mode of flight from take-off to goal could potentially involve a different visual guidance algorithm. Here, we briefly review strategies for visual guidance of flight in insects, synthesize recent work from short-range visual guidance in birds, and offer a general comparison between the two groups of organisms.
Optokinetic responses function to maintain retinal image stabilization by minimizing optic flow that occurs during self-motion. The hovering ability of hummingbirds is an extreme example of this ...behavior. Optokinetic responses are mediated by direction-selective neurons with large receptive fields in the accessory optic system (AOS) and pretectum. Recent studies in hummingbirds showed that, compared with other bird species,
) the pretectal nucleus lentiformis mesencephali (LM) is hypertrophied,
) LM has a unique distribution of direction preferences, and
) LM neurons are more tightly tuned to stimulus velocity. In this study, we sought to determine if there are concomitant changes in the nucleus of the basal optic root (nBOR) of the AOS. We recorded the visual response properties of nBOR neurons to large-field-drifting random dot patterns and sine-wave gratings in Anna's hummingbirds and zebra finches and compared these with archival data from pigeons. We found no differences with respect to the distribution of direction preferences: Neurons responsive to upward, downward, and nasal-to-temporal motion were equally represented in all three species, and neurons responsive to temporal-to-nasal motion were rare or absent (<5%). Compared with zebra finches and pigeons, however, hummingbird nBOR neurons were more tightly tuned to stimulus velocity of random dot stimuli. Moreover, in response to drifting gratings, hummingbird nBOR neurons are more tightly tuned in the spatiotemporal domain. These results, in combination with specialization in LM, support a hypothesis that hummingbirds have evolved to be "optic flow specialists" to cope with the optomotor demands of sustained hovering flight.
Hummingbirds have specialized response properties to optic flow in the pretectal nucleus lentiformis mesencephali (LM). The LM works with the nucleus of the basal optic root (nBOR) of the accessory optic system (AOS) to process global visual motion, but whether the neural response specializations observed in the LM extend to the nBOR is unknown. Hummingbird nBOR neurons are more tightly tuned to visual stimulus velocity, and in the spatiotemporal domain, compared with two nonhovering species.
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