Evolutionary Origins Of Manakins’ Dazzling Dances

A shift to a fruit diet may have paved the way for the evolution of spectacular displays in manakins

Male Lance-tailed Manakin (Chiroxiphia lanceolata) photographed on Isla Boca Brava, Panama

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To the Point

• Fruit first, fancy footwork later: A new study finds the courtship dances of the manakins – one of the most charismatic groups of birds on Earth – trace back to changes deep in their ancestry and may be linked to their fruit-rich diet.
• Same answer, different routes: Manakins re-evolved a sense of sweet taste, as hummingbirds, songbirds and woodpeckers each did separately, by repurposing the receptor for savory taste.
• Genome-enabled discovery: Manakins are one of the most intensively-studied groups of birds: this first set of genomes provides resources to the community to explore the genomic changes underlying their unique behaviors and physiologies.

Few animals put on a show quite like manakins. In the rainforests of Central and South America, males of these small tropical birds, with strikingly bright plumage, often gather at communal display sites, or leks, where they clear their own dance courts and spend much of their lives performing high-speed backflips, snapping their wings like firecrackers, and running through choreographed routines with other males, all to attract a mate. Behind these seemingly effortless performances is far more than meets the eye: years of practice, females who raise the young alone, and, it turns out, a change in diet that began with their distant ancestors.

Over millions of years, the relentless competition for mates is thought to have driven manakin plumage and dances to ever greater extremes through sexual selection, the evolutionary force behind extravagant features such as the peacock’s tail and the stag’s antlers. Only a small number of the most attractive males are usually chosen as mates, and across the generations that intense selection by females pushes favored traits further.

In manakins, diet may also play a role in the evolution of these dazzling displays. A new study, led by Chris Balakrishnan (East Carolina University), Yasuka Toda (Institute of Science Tokyo and Meiji University) and Maude Baldwin of the Max Planck Institute for Biological Intelligence, together with an international team of nearly sixty researchers, uncovered a link between the bird’s diet and changes in display behavior. They sequenced the genomes of lek-mating manakins and observed genetic fingerprints of strong sexual selection as well as changes in taste and digestion. Through reconstruction of dietary patterns, together with genome-wide surveys and lab experiments, they examined the order of those changes in the birds’ evolutionary history to work out their timing.

“Sexual selection varies enormously in strength across animals, sometimes even between close relatives, and we still don’t fully understand why,” said Christopher Balakrishnan who led the genomic analysis. “We set out to explore how manakins evolved such spectacular displays when many of their close relatives, which mostly eat insects, did not. Diet wasn’t our focus at first – we were interested in the flamboyant side: the muscles, the plumage, the dances. But when we compared the manakins’ genomes against those of other birds, it was the genes for tasting and digesting fruit that stood out, and these changes began far back on the birds’ family tree, long before the elaborate displays and breeding behaviors emerged.”

Putting the steps in order

Female Lance-tailed Manakin (Chiroxiphia lanceolata) photographed on Isla Boca Brava, Panama’>

Male manakins are not only showmen but extraordinary athletes: in some species, their wing muscles are among the fastest contracting in nature, a displaying male’s heart can race from rest to near its limit in seconds, and males may spend up to ninety per cent of the daylight hours performing, almost year-round. Such effort burns a lot of energy, and manakins draw it substantially from their fruit-based diets. But eating fruit is not necessarily straightforward for a bird: many plants protect their unripe fruit with toxic compounds making them tough to digest, and many birds cannot even taste sweetness, having lost the necessary receptor far back in their evolutionary history.

Remarkably, some bird species have found a way around these problems through independent evolutionary innovations. Earlier research led by Maude Baldwin and Yasuka Toda has shown that hummingbirds, songbirds and woodpeckers re-evolved a sense of sweetness by chance modifications to the receptor for savory taste that happened to make it sugar responsive. The new study adds manakins to that list, confirmed by tests in lab-grown cells.

“Manakins re-evolved a sweet sense of their own – and did it their own way, by altering a different part of the receptor than songbirds use,” said Yasuka Toda who led the laboratory work on the birds’ taste receptors. “Evolution kept arriving at the same answer along different paths. And taste sits within something larger: fruit in tropical forests is conspicuous and abundant year-round, likely providing the energy needed for females to raise the young alone and for males to put on their incredible displays.”

A second key change was in digestion: the enzyme lactase – which in mammals breaks down milk sugar – has lost much of its activity in manakins. When active, lactase also breaks down certain plant compounds found in unripe fruit, releasing products that block sugar absorption. With reduced lactase activity, the manakins may pass these compounds through harmlessly and absorb more energy from the fruit. The change traces back to when the manakins’ lineage first turned to fruit. Mapping these changes onto a family tree of more than 1,300 related bird species revealed a clear order: the dietary changes came first, deep in the manakins’ ancestry, and the elaborate mating system and displays followed much later.

“When we first saw the signal on lactase, our reaction was: why lactase in a bird? They don’t drink milk,” said Meng-Ching Ko of the Max Planck Institute for Biological Intelligence, who led the analysis of the manakins’ digestion. “But this loss of enzyme activity may help manakins handle the toxins in unripe fruit. It sounds counterintuitive as losing a function may not sound like a benefit, but for the manakins it turns what looks like a digestive limitation into an opportunity. Knowing the order in which these changes unfolded opens further questions, too, about how changes in digestion and enzyme function may impact other aspects of life history. Something as simple as a change in food can reshape an animal’s whole biology – and, for manakins, give rise to some of the most spectacular dances in the forest.”

Manakins are mesmerizing, and have long attracted the interest of a broad community of researchers across the world. They have been the subject of diverse studies on biomechanics, hormones, and decades-long field studies examining their behavioral ecology and sexual selection. This paper is part of a series of studies that were the product of a US National Science Foundation Research Coordination Network grant that aimed to connect researchers working on manakin behavior, ecology and physiology with genomic biologists – three other studies investigated diverse facets of manakin biology, including plumage traits, brain regions involved in social behavior, and the genes expressed in unique ‘superfast’ muscles. More insights into these unusual birds are likely soon to come.

[AG]