In this post, we take a behind-the-scenes look at a recent study into the drivers of complexity in bird of paradise displays. Meredith Miles, a PhD student in Dr Matthew Fuxjager’s lab at Wake Forest University, takes an integrative approach into behavioural ecology. This involves studying the molecular and physiological mechanisms that underlie display performance all the way up to the diversity of macroevolutionary pattern generated by sexual selection for displays.

Birds of paradise—the gaudy songbirds known for their bizarre courtship displays and ornamental plumage—evolved from a crow-like ancestor as early as 24 million years ago. These large and charismatic birds boast both cultural and scientific significance; indigenous peoples and 16^th century Europeans alike considered them to be “Birds of God” or mythical phoenixes, and the birds’ elaborate courtship routines have inspired figures from Alfred R. Wallace to Sir David Attenborough. Indeed, this island-endemic lineage serves as a prime example for how sexual selection drives the evolution of extraordinary behavior. Birds of paradise also offer a unique opportunity to leverage the phenotypic complexity of their displays to uncover hidden truths about the process of evolution.

There are over 30 bird of paradise species, each with its own unique visual display. These encompass both color and gesture, and have evolved due to intense sexual selection by female choice. Left: male Raggiana bird of paradise (Paradisea raggiana). Right: male and female Wilson’s birds of paradise (Diphyllodes respublica). Photos: Dr. Marcel Holyoak.

How can we study something as complicated as animal dance and “costume”? At its core, dance is simply an extreme example of a gestural display, or body movement used for communication. The gestural complexity of a given species’ display simply refers to the number of unique movements incorporated into the whole routine. Over the years, diligent naturalists have compiled extensive (and evocative) descriptions of gestural displays, which we used to tally up a gestural complexity score for each species. For example, consider the following description of the king bird of paradise’s Dancing Display:

“… In this display he fluffs out his plumage, squats low to the perch, spreads the pectoral fans high, and cocks the tail so steeply that the wires are tilted forwards reaching above and beyond his head” – Frith and Beehler, 1998.

In this single posture alone, there are four unique movements: the bird (1) crouches down, (2) raises its tail, (3) spreads the specialized breast plumes, and (4) erects the rest of the body plumage. These are common elements we see in the displays of many other species too, and we thus award the species a point in the corresponding gestures. Combing through pages of similar accounts gives us an exhaustive look at each species’ behavior, and ultimately lets us generate a quantitative index of gestural complexity for all birds of paradise.

At first glance, this portion of a king bird of paradise’s Dance Display might look like a single movement—but it actually consists of multiple component gestures that are shared with many other species. Only by breaking down gestural displays into these “raw ingredients” can we begin to understand how animal dance evolves.

What drives the evolution of complex dance routines? These gestures are the key to courtship for birds of paradise, but we found that only display habitat—rather than indices of sexual selection—predicts the macroevolutionary pattern: species that display in the dense forest understory use more gestures than their canopy-displaying counterparts. This may be because display habitat profoundly affects how well a signal can be transmitted to the receiver. Displaying in the “visually cluttered” understory might increase the pressure for males to evolve more visible displays, and one way to accomplish this is through adding more gestures to the dance.

We can also characterize color ornaments by scoring how much male plumage has diverged from its female counterpart. This works thanks to an ancestral state reconstruction of sexual dimorphism, which shows us that birds of paradise descended from an ancestor in which both males and females were drab. Unlike dance complexity, color is not associated with display habitat on a macroevolutionary scale. Instead, males appear to become more colorful in response to the adoption of a lek mating system (which is characterized by extreme sexual selection by female choice). We can even break down our investigation of color to distinguish between melanin-based (blacks, browns, and other “earthtones”) and carotenoid-based (red and yellow) ornaments. Although pigment basis for colors does not change with species display habitat or mating system, it does appear to be influenced by male sociality: species in which males gather together and directly compete at a single display ground trade in melanin colors for bright carotenoid ornaments instead. Together, this suggests that males undergoing a higher relative degree of sexual selection by female choice—as reflected in the lek mating system—will evolve to be more colorful overall. However, increasing pressure of male-male competition appears to specifically influence the evolution of bright red and yellow color patches.

 Four representative species illustrating the main evolutionary trends we uncover in the study. Different selection pressures are each associated with shifts in a specific display trait.

Altogether, our results suggest that these complex displays exhibit modular evolution: each component of the display (e.g., gesture or color) acts as a distinct “module” that undergoes an independent evolutionary trajectory. Modular displays may be evolutionarily significant because they allow for multiple—and potentially opposing—selection pressures to simultaneously act on the same display without impeding one another.

Of course, a female bird of paradise evaluating a male’s display is probably not scoring his choreography and color. Instead, an animal must perceive the display in its entirety, which encompasses auditory and tactile signals as well as visual. And within the visual display itself, gesture is even used to show off specific color ornaments. In this way, modular evolution allows the integrated display’s complexity to be multiplicative rather than additive: its attractiveness to the receiver is more than the sum of its modular parts.  However, it is only by examining these parts individually that we can understand what drives their independent evolution.

More Info:

Miles, M.C. and Fuxjager, M.J. (in press). Synergistic selection regimens drive the evolution of display complexity in birds of paradise. Journal of Animal Ecology.