A male fruit fly aspiring to mate faces steep odds. First, he must spend up to 20 minutes maniacally buzzing and dancing. Even then, his success or failure hinges on a single split-second maneuver, when he vaults onto the female, parts her wings, and connects his abdomen to hers. If the gymnastics go awry, the female delivers a powerful mule-kick — sending him tumbling away. 

Some species of fruit flies have met this challenge by evolving a strange new body part – a entomological male member, of sorts – resembling a hair comb. It juts off his front legs, helping him grab his mate-to-be more precisely. The evolutionary origin of this ‘sex comb’ represents a tantalizing mystery.

“It’s one thing to evolve longer legs or a different color, but for complex new structures that evolve out of nowhere — we’re still not sure how that happens,” says Ben Hopkins, who recently finished a post-doctoral fellowship in the Department of Evolution and Ecology.

New research by Hopkins and Artyom Kopp, a professor and chair of evolution and ecology, shows how one new body part – the sex comb – sprouted and bloomed with surprising ease.

“You don’t need new genes to make new structures,” says Kopp. Instead, the sex comb evolved when a handful of cells sped up their metabolism for a few hours. 

This discovery could change how we understand evolution across the tree of life, from starfish to hedgehogs and humans, says Kopp: “It shows how you can generate a very complex body with surprisingly subtle genetic changes.”

Inventing Feathers, Fur, and New Taste Buds

Evolution often unfolds gradually — for example, a moth’s wings darkening so it can hide in new habitats.

But scientists have long puzzled over instances where an entirely new body structure emerges — for example, the mammalian fur and bird feathers that evolved out of reptile scales, the four limbs that evolved out of fins as vertebrates ventured onto land, and the eye spot color patterns that emerged on the wings of some butterflies, to scare off potential predators. 

Scientists believe that new structures like these often evolve through “a copy and paste feature,” says Hopkins, now an assistant professor at the University of Florida in Gainesville.

For example, the hairy bristles that cover a fruit fly’s head and legs function as whiskers, allowing the insect to sense objects brushing by. But fruit flies also have other bristles on their legs that can taste chemicals. 

Taste bristles grow from the same specialized cells that make touch bristles. They may have evolved by copying and then modifying the gene program used to make touch bristles, causing some of these cells to develop into something new.

Kopp and Hopkins decided to test this idea by studying how the sex comb evolved in fruit flies. This comb also grows from the same cells that make touch bristles. So they assumed that the genetic program for making touch bristles had again been copied and modified, to include some additional genes that are normally used only in other body parts of the fly.

But as Hopkins examined the cells that produce sex combs and touch bristles on the same developing flies, he found that both express the same genes — even as they’re creating vastly different structures.

“That really went against our expectation,” says Kopp. 

Racing to Build a Bigger Bristle

But Hopkins saw other differences. In the cells that make sex combs, the DNA was copied an extra time, so each cell ended up with twice as much DNA as the cells that make touch bristles. At the same time, the comb-growing cells greatly amplified the activity of genes that produce cellular energy. With that bigger power supply, driven by energy genes turned up to full volume, these cells could enlarge more quickly. And although they were making the same proteins that touch bristle cells make, they produced way more of them.

This small difference happens at a critical moment in the fly’s metamorphosis. Because of this, it has a huge effect.

Both the touch bristle cells and the sex comb cells have only 24 hours to grow while the fly is transforming inside its cocoon-like pupa. After that, the fly’s exoskeleton hardens — blocking further growth. During those fleeting hours, a slower-growing cell can produce a thin, wispy touch bristle. But each faster-growing cell is able to build a much longer and thicker protrusion, more like a tooth. A row of fast-growing cells building these ‘teeth’ side by side produces the comb. 

“It shows surprising flexibility, creating different structures with the same genes,” says Hopkins. This could allow male fruit flies to evolve new structures very quickly when faced with the rapidly changing mating preferences of females.

”Metabolism is closely intertwined with development,” says Kopp. “So altering it at a critical moment can yield profound changes in the adult form.”

This research is funded by the National Institutes of Health and by the Human Frontier Science Program Organization. It utilized advanced scientific facilities at UC Davis, including the Light Microscopy Imaging Facility and the Genome Center.

Additional coauthors include Olga Barmina, Xinying Wang, Mandy M. Situ, and Haley A. Bolanos in the Department of Evolution and Ecology at UC Davis; and Shizhan Nie at the University of Florida Gainesville.