Proposing a neural framework for the evolution of elaborate courtship displays
- Department of Biology, University of Pennsylvania, United States
- Neuroscience Graduate Group, University of Pennsylvania, United States
- Department of Ecology, Evolution, and Organismal Biology, Brown University, United States
Figures
Figure 1
Variety of representative courtship displays among the vertebrates.
(A) Seahorses engage in a complex, multi-phase mating ritual, which can involve rapid body vibration, changes in color, and intertwining body movements. Photo credit: Soumit Nandi, with permission. (B) Foot-flagging frogs extend their hindlimbs in a slow sweeping motion, with their digits spread apart to display foot webbing. Photo credit: Nabeshima Seiichiro, with permission. (C) Alligators perform the ‘water dance’ display, whereby deep laryngeal bellows create a striking vibratory pattern of water droplets. Photo credit: Stephen Tabone, with permission. (D) The blue-footed booby engages in a unique postural display which involves a slow spreading of the wings and an upward tilt of the head. Photo credit: Scott Davis, with permission through Tandem Stock. These images are not covered by the CC-BY 4.0 licence and further reproduction of these panels would need permission from the copyright holder(s).
© 2016, Soumit Nandi. Figure 1A photo credit: Soumit Nandi, with permission through Tandem Stock. This image is not covered by the CC-BY 4.0 licence and further reproduction of these panels would need permission from the copyright holder(s).
© 2016, Nabeshima Seiichiro. Figure 1B photo credit: Nabeshima Seiichiro, with permission through Tandem Stock. This image is not covered by the CC-BY 4.0 licence and further reproduction of these panels would need permission from the copyright holder(s).
© 2014, Stephane Tabon. Figure 1C photo credit: Stephen Tabone, with permission through Tandem Stock. This image is not covered by the CC-BY 4.0 licence and further reproduction of these panels would need permission from the copyright holder(s).
Figure 2
Diversity of dance display characteristics among a small group of manakin birds (family: Pipridae).
Each bar represents a specific motor element that is incorporated into the given species’ (shown on the left) overall courtship routines. Each colored bar indicates that the specific element forms part of the bird’s display. The display elements are shown above and loosely categorized into different classes of behavior (e.g. posture, jumping, wing vibration, etc.). We color-coded these categories to also reflect display movements that are associated with gesture and posture (blue), forelimb locomotion (orange), hindlimb locomotion (purple), and generation of acoustic signal (grey). Note that each particular display element is denoted by a number, which corresponds to the original classification by Prum, 1990. Importantly, each bird performs a dramatically different display routine, which incorporates various forms of movement that engage different muscular systems across the body. Species’ displays also differ markedly in terms of their overall complexity, with some species performing displays with few distinct maneuvers and others displaying several distinct elements. Phylogenetic relationships from Leite et al., 2021. Bird illustrations by Ryan Schwark.
Figure 3
The neural circuitry governing vocal display is highly conserved among vertebrates.
Anatomical and functional studies have revealed that fish, songbirds and mammals contain a conserved brainstem module which orchestrates vocal display. The role of the midbrain PAG is central, as it receives inputs from diencephalic and telencephalic structures that encode sociosexual information and in the case of songbirds even a sparse temporal code that helps shape song spectro-temporal features. Excitatory axons from the PAG then project to premotor nuclei located in the medulla, which then ultimately project to the motoneurons that innervate the vocal musculature. In the midshipman fish, vocalization is controlled by a vibratory swim bladder; in songbirds, birdsong is controlled by the muscles of the syrinx and those of respiration; in the mouse, ultrasonic vocalizations (USVs) are produced by laryngeal and respiratory muscles. The mouse PAG contains courtship-specific excitatory neurons which are necessary and sufficient to produce USVs (inset) (Tschida et al., 2019). These neurons are tonically inhibited by GABAergic interneurons, and disinhibition of the neurons by inputs from the preoptic area (POA) engages courtship. In the songbird, respiratory (RAm) and vocal (nXIIts) targets of PAG are separate anatomical structures but are combined in this schematic for simplicity. Animal illustrations by Ryan Schwark.
Figure 4
Working model for how PAG evolution might underlie display variation across species.
PAG organization includes excitatory outputs (cells A-D) that are under tonic inhibition by a collection of interconnecting interneurons (red). Each excitatory cell activates a motor module, with the duration of activation corresponding to the level of inhibition that the cell experiences. In the ancestral PAG (top), cells A, B, and C receive a set level of inhibition from interneurons, which when released, activates the expression of motor modules A, B, and C, respectively, which underlie display performance. In this ancestral PAG, cell D is under high levels of tonic inhibition, and thus does not contribute to the display. However, if evolutionary pressures decrease inhibition to cell D (left), then a new module can be added to the display, thereby increasing its complexity. Likewise, if levels of inhibition on cell D remain the same but are decreased on cell C (right), then motor module D is not added to the display. Rather, motor module C is extended, and thus exaggerated within the context of display behavior.
Figure 5
Theoretical model of how PAG evolution might shape diversification of courtship bow display in New World blackbirds (family: Icteridae).
Shown is the phylogeny of the oropendolas and caciques (Powell et al., 2014) with representative species highlighted by red branches. These taxa all perform bowing displays, but the angle at which they bow differs markedly. In theory, these differences may be related to the degree of tonic inhibition of excitatory streams that flow from the PAG. Greater inhibition (e.g. casqued cacique) is denoted by more red interneurons and more synaptic terminals projecting onto the blue excitatory neuron that leaves the PAG. This results in shorter duration muscle activation and thus a lower bow angle. By contrast, less inhibition (e.g. Montezuma oropendola), denoted by fewer red interneurons and fewer synaptic terminals projecting on to the blue excitatory neuron, results in extended muscle activation and greater bow angle. Indeed, Montezuma oropendolas dangle upside-down from their display branch when they perform their bow (Miles and Fuxjager, 2018b), which is by far the most elaborate form of this behavior in the family (Miles et al., 2017). It is no surprise that this species is also under especially strong sexual selection, relative to the other taxa within this small clade. Bird illustrations by Ryan Schwark.
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Proposing a neural framework for the evolution of elaborate courtship displays
eLife 11:e74860.
https://doi.org/10.7554/eLife.74860
