American Society of Naturalists

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“Phenotypic diversity arises from secondary signal loss in the elaborate visual displays of toucans and barbets”

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Meredith C. Miles and Matthew J. Fuxjager (Aug 2019)

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Secondary loss of signals underlies the evolution of display diversity in toucans

The tail-cock gesture is performed when an individual elevates the tail to be perpendicular with the body, which pushes the rump feathers above the wings and exposes the undertail (small arrows).<br />(Credit: Meredith C. Miles and Matthew J. Fuxjager, ©&nbsp;The&nbsp;University of Chicago Press&nbsp;2019)
The tail-cock gesture is performed when an individual elevates the tail to be perpendicular with the body, which pushes the rump feathers above the wings and exposes the undertail (small arrows).
(Credit: Meredith C. Miles and Matthew J. Fuxjager, © The University of Chicago Press 2019)

The evolution of complexity and diversity are two defining characteristics of life on Earth, but how they relate to each other is still largely a mystery. To address this question, we modeled how a communication system evolved as its individual components were gained and lost throughout evolutionary time. We specifically looked at the visual displays of toucans and barbets, a group of birds found across the continental tropics. Species in the group are mostly known for their big beaks and colorful plumage, but some are a bit more drab. When reading about the birds, we also noticed a common emphasis on tail-based displays. For example, in many species a bird will cock its tail up (and sometimes wave it around) to display, exposing feathers on the rump and undertail. Coincidentally, many species also have contrasting feather patches in the same regions. Some species also ruffle up the rump feathers to display—indeed, including many with a color patch on the rump. Yet others displayed with either gesture (or both) without any special ornaments on the tail.

The small number of traits in this system made it perfect for discrete trait modeling, which we used to explore coevolution between gesture and color—and how coevolution influences the evolutionary trajectory toward phenotypic complexity (e.g., a species that has gained many colors and gestures) and diversity (i.e., the range of unique gesture-color combinations present in species today). Indeed, gestures tend to co-evolve with the color patches they emphasize. However, a species with no display whatsoever is only likely to gain a tail-cocking gesture. The chance of gaining a color ornament first was almost zero! Color ornaments were instead gained by lineages that already tail-cock. As a result, we found only a few likely ways that a species’ display evolves from minimum complexity (no gestures, no ornaments) to maximum complexity. Instead, many displays we see today must have evolved as different signal combinations were lost instead: there are only a few ways to become complex, but many routes to diversity.


Abstract

Complexity and diversity are fundamental characteristics of life, but the relationship between the two remains murky. For example, both gaining and losing complexity can support diversity—so how exactly does complexity influence the emergence of unique phenotypes? Here we address this question by examining how complexity underlies the diversity of elaborate visual displays in an avian clade (Ramphastides, the toucans and barbets). These species communicate in part using body movement and colorful ornaments on the tail. We find that sexual size dimorphism predicts the evolution of one specific signal, the tail-cock gesture, implying that tail-cocking is more likely to evolve under stronger sexual selection. We also discovered process-level constraints on the evolution of complexity: signals are gained along a strict order of operations, where the tail-cock gesture arises before other colors and gestures. Yet virtually any signal can be lost at any time. As a result, many extant phenotypes were more likely to arise through loss of complexity, highlighting the importance of secondary signal loss to phenotypic diversity. Collectively, our results demonstrate how sexual selection catalyzes the evolution of complex phenotypes, which indirectly support diversity by allowing different traits to be modified or lost in the future.