The genes of the sexiest birds on the planet | Science

By Elizabeth PennisiMarch 3, 2021 at 1:00 p.m.

For a glimpse into the power of sexual selection, the Golden Collared Manakin Dance is hard to beat. Every June in the rainforests of Panama, sparrow-sized male birds congregate to puff their bright yellow throats, lift their wings, and flap them together in a rapid fire, up to 60 times per second. . When a female prefers a man with her attention, he follows it up with acrobatic jumps, more wing-flapping, and maybe a twisted split-second backflip. “If manakins were human, they would be some of the greatest artists, athletes and socialites in our society,” says Ignacio Moore, an integrative organism biologist at Virginia Polytechnic Institute and State University.

As biologists have understood since Charles Darwin, such exhibitionism evolves when women choose to mate with men who have the most extravagant appearances and displays – an indicator of physical fitness. And now, by studying the genomes of the gold-collared manakin (Manacus vitellinus) and those close to him, the researchers are exploring the genes that underlie these elaborate behaviors and traits. Last month at the Society for Integrative and Comparative Biology virtual meeting, Moore and other researchers presented four manakine genomes, adding to two already published, and singled out the genes at work in muscle and bird brains that might make displays possible.

The work offers “a better understanding of why manakins do all the amazing things they do,” says Emily DuVal, behavioral ecologist at Florida State University. Over the past decade, researchers have learned a lot about how natural selection affects genomes. “In contrast, we know very little about the underlying basis for sexually selected traits,” says Christopher Balakrishnan, evolutionary biologist at East Carolina University (ECU). By mapping traits and genes on the manakin family tree, researchers begin to trace the genetic changes in stages that led to the most elaborate displays and determine whether sexual selection works differently from natural selection.

Other species, including birds of paradise and scrub birds, also stage impressive sexual displays. But manakins have a greater variety of these traits and, being more abundant and more accessible, they are easier to study in depth. We can “assess the genomic basis for these behaviors in a way that is not possible for many other complex behavioral traits in vertebrates,” says Morgan Wirthlin, evolutionary neurobiologist at Carnegie Mellon University.

As Balakrishnan and his colleagues reported at the meeting, a sweet tooth – or beak – may have set the stage for sexual selection in manakins. Their ancestors are known to change their diet from insects to fruit, and researchers suspected that the switch to a more available and abundant food source gave males more energy to procure mates.

By comparing the genomes of manakin relatives that continue to eat insects with those of fruit-eating manakins, Balakrishnan, Maude Baldwin of the Max Planck Institute for Ornithology and her colleagues found evidence that fruit consumption and elaborate male displays evolved in stages. Researchers have learned that the genes encoding a savory taste receptor began to change even before the manakins became fruit eaters. By the time the saffron-crested tyrant-Manakin (Neopelma chrysocephalum) evolved, Baldwin reported at the meeting, the receptor had become sensitive to the sweetness of ripe fruit – a rare trait in birds. This species runs with simple hops – halfway through the elaborate displays of fruit species that evolved later.

Wirthlin and others explored the DNA that changed to make these behaviors possible. In her analysis of five manakin genomes, she focused on ultra-preserved non-coding elements, segments of DNA that have remained almost exactly the same in animals ranging from chickens to humans and are believed to play a crucial role in regulation other genes. Given this retention, she figured they would be a good place to look for possible sexual selection fingerprints.

In the manakin genomes, 57 elements showed slight differences from the corresponding sequences in other species; these changes could alter the activity of the genes they regulate. Some of these elements are grouped around the genes for muscle proteins and hormone receptors and some are close to genes expressed in the brain, two of which, TLE4 and MEIS2, active in an area necessary for rapid visual processing. Both genes are less active in manakins than in zebra finches, Wirthlin reported – a change that could help male manakins cope with the visual demands of their frenzied dances.

Matthew Fuxjager, an integrating biologist at Brown University, is excited by Wirthlin’s discovery that evolution may have stimulated gene activity for hormone receptors in birds. The high speed wing beats in some species require very fast and powerful pectoral wing muscles – which are very sensitive to the male hormone androgen. “Androgens are what accelerates speed,” by altering the activity of muscle performance genes, says Fuxjager.

At the meeting, Balakrishnan reported that he identified other genes that may have also supercharged these crucial muscles. His genomic analysis suggested that the activity of genes involved in muscle metabolism and growth changed early in the evolution of manakin, resulting in more powerful muscles. He hasn’t searched females, but he and Fuxjager believe the demands of flight, not mating, may have driven these early changes. Then, as sexual selection began to act on the later evolving species, changes in androgen receptors and other signaling pathways made the flight muscles in males capable of the very rapid movements necessary for courtship displays. . (Other research shows that female muscles are not as sensitive to androgens.)

Manakin performance involves more than sound and movement – in some species it is also a social act, coordinated between no less than 20 males. In all vertebrates, a network of brain ‘nuclei’ – clusters of similar nerve cells – help control social behavior, and studies presented at the meeting show that the pattern of gene activity in these nuclei varies with testosterone levels. The work of evolutionary biologist Peri Bolton of ECU and ecologists Brent Horton of Millersville University and Brent Ryder of Smithsonian National Zoological Park suggests that changes in androgen receptors may have contributed to the social sophistication of birds as well as ‘to their athleticism.

As dazzling as the manakin exhibits are, researchers are equally in awe of their complex genetic underpinnings. “Our studies tell us that beauty isn’t just about the skin,” says Moore.