American Society of Naturalists

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“Selection for rhythm as a trigger for recursive evolution in the elaborate display system of woodpeckers”

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Meredith C. Miles, Eric R. Schuppe, and Matthew J. Fuxjager (May 2020)

Display rhythm fosters premating isolation early in a species history, but then impedes signal evolution later on

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Red-bellied woodpecker (<i>Melanerpes carolinus</i>) perched on a tree, readying itself to drum.<br />(Credit: N. Lewis / Shenandoah National Park on Flickr)
Red-bellied woodpecker (Melanerpes carolinus) perched on a tree, readying itself to drum.
(Credit: N. Lewis / Shenandoah National Park on Flickr)

Selection pressures that influences how traits evolve change over time. A consequence of this phenomenon is that selection regimes acting on a trait early in its history can affect how that same trait evolves later on in response to a different selection regime. We study this process in woodpeckers by looking at the evolution of their territorial display, the drum. Individuals produce this iconic signal when they rapidly hammer their bill against trees and other substrates in the environment, warding off potential interlopers during the breeding season. Nearly all 200 woodpecker species drum, but each species differs in terms of its drum speed and length. Here, we report that species also differ with regard to drum rhythm—some woodpeckers drum at constant rates, whereas others change their drum speed following basic mathematical functions (e.g., a linear increase in speed, an exponential decay in speed, etc.). Using various comparative analyses, we show that rhythm is the key feature of the drum that diverges between closely related species overlapping in their geographic range. Such ‘character displacement’ is thought to help species better recognize their own, but the strength of this selective process diminishes overtime as other traits evolve to help mediate this ability. Additionally, we show that rhythm can enhance or inhibit the evolutionary exaggeration of drum speed and length. This is important because this latter feature is favored by contemporary sexual selection to help support territoriality. Thus, selection early in a woodpecker’s history can influence the structure of a drum display in ways that impact how the signal evolves down the road. This may help explain why similar selection regimes that act on separate taxa often result in the emergence of completely different phenotypes.


Abstract

Evolution is never truly predictable, partially because selection is a recursive process: it operates on its own output to generate historical contingencies, so emergent traits can reshape how others evolve in the future. Studies rarely attempt to directly trace how recursion underlies present-day phenotypic pattern on a macroevolutionary basis. To address this gap, we examined how different selection regimes—each operating on a different timescale— recursively guide the evolution of the woodpecker drum display. Some 200 species drum with distinctive speed and length, which are important for territorial competition. Here we report remarkable variation in drum rhythm, with some species drumming at constant rates and others changing speed along a range of mathematical functions. Rhythm undergoes divergent character displacement among sympatric sister species, a process that wanes as other reproductive boundaries emerge over time. Tracing the recursive effects of this process, we found that modifying rhythm potentiates or constraints speed/length elaboration. Additionally, increased sexual size dimorphism predicts the emergence of rhythms associated with constrained evolutionary rates of speed/length, implying that selection can also constrain itself. Altogether, our findings illustrate how recursion introduces contingencies that allow diverse phenotypes to arise from similar selection regimes.