How Cheaters Prosper

Ecologists are chasing an evolutionary conundrum.

By Kristin Ohlson|Tuesday, September 25, 2018
RELATED TAGS: ANIMALS, PLANTS, ECOLOGY
Bee
Bee
A bumblebee “robs” from a flower, extracting the plant’s nectar without providing any pollination.
Christopher Wren

We weave along a path beaten between Rocky Mountain wildflowers that bloom and bobble over our heads, chasing the elusive Orange 78.

She disappears into a cloud of white Sierra fumewort flowers. Then Yellow 54 sails into view and we rush to follow, angling through the surrounding green curtains to keep up. She makes a beeline for the Mertensia ciliate, or mountain bluebell. And it truly is a beeline — Yellow 54 is a bumblebee with a yellow dot and number superglued to her back. She was trapped, tagged, registered and DNA-sampled a few days earlier for research purposes.

Ecology undergraduate researcher Karen Wang drops her fine-mesh bee net, whips out a small recorder and leans in to observe Yellow 54 climbing into the bluebell’s long tubular blooms. “One,” she says of the bee’s quick entrance into the flower, “and out. Two … out. Three … out. Oh, four was a secondary rob! Five was a secondary rob! Six was a secondary rob! Ah,” her voice drops. “Now she’s legitimate again.”

Bees and flowers have one of the most studied mutualisms, the beneficial interactions that occur among species in most ecosystems and probably involve organisms from every kingdom. Flowers produce nectar to attract bees, which enter the flower and climb past the pollen-powdered anthers for a quick energy drink, sometimes mixing some of that nectar with pollen to feed their young. The bees emerge from the bloom coated with the golden grains. Then they move from flower to flower, paying for that nectar by unwittingly fertilizing plants with pollen, letting the plants to make seeds.

Karen-Wang
Karen-Wang
Researcher Karen Wang follows bees through a field near Crested Butte, Colorado, documenting their activities.
Courtesy of Karen Wang

But sometimes bees “cheat” — a somewhat hilarious and disparaging way to describe organisms that don’t perform their role in the mutualism. That’s what Wang spotted Yellow 54 doing. Bees can cheat by chewing a hole in the base of the bloom to get the nectar, a more direct way to the sugary reward that likely omits pollination. Some commit a secondary rob, as Yellow 54 also did, by entering a hole gnawed by another bee. In either case, the plant has done a lot of work — pulled carbon dioxide out of the atmosphere through photosynthesis, converted it into sugars, finessed them into nectar — with no reciprocal reward, at least when Yellow 54 was involved.

Gaming the System

Most people think of bees as models of cooperative behavior. However, researchers keep finding evidence that they and other creatures, from fish to bacteria, often cheat. Some mutualist partners are even more outrageous cheaters than bees. Blue butterflies of the Lycaenidae family have a mutualism with ants, in which the caterpillars secrete a sugary liquid through special organs to feed the ant, and in exchange the ants protect the caterpillars from predators. Occasionally, though, a caterpillar manages to mimic the smell of an ant larva or egg, and the ants will dutifully carry it back to their nest. There, the ants will feed the caterpillar mouth to mouth, as they do with their own young, even as the caterpillar chows down on ant larvae.

“I always think the ants must be so surprised when a butterfly finally emerges,” says University of Toronto evolutionary ecologist Megan Frederickson, who studies mutualisms between ants and plants in tropical forests. “There are great videos showing butterflies having to hurriedly escape the ant nest because the ants all of a sudden realize there’s an invader.”

Wasp
Wasp
A male orchid dupe wasp tries to mate with a flower.
Veronica Carter/Alamy Stock Photo

Other living things have evolved to snatch up the rewards of mutualism with none of the costs. Take orchids. They are one of the world’s three largest flowering plant families, but about a third don’t make nectar to attract insect pollinators. Instead, those plants trick male insects into penetrating their blooms by creating the odor or shape of a female insect. The males thrash around trying to copulate, covering themselves with pollen. Then they spread the pollen to other orchids in an ongoing series of hopeless trysts.

All this cheating has researchers probing how and why cooperation breaks down. Some recently met in Paris for a lively two-day symposium organized by ecologist Judie Bronstein, author of Mutualism. The gathering’s cheeky name was Cheating in Paris, but the concerns they addressed are sobering.

Mutualisms are crucial for the function of the biosphere. Animal pollinators, such as birds and bees, fertilize some 80 percent of Earth’s flowering plants, including the plants we use for food, beverages, fiber and such. Other mutualisms, such as those between soil bacteria and plants, regulate the flow of planetary carbon and nitrogen.

Does widespread cheating indicate that some of these ecosystem services could break down? To answer that, scientists need to determine how widespread cheating is and why it happens.

Ant
Ant
A field ant tends to the larva of a great copper butterfly. The caterpillar’s secretions are attractive to ants, prompting them to protect the caterpillar from predators and parasites.
Alex Wild

“Mutualism is very puzzling because it’s easy to see how partners could exploit each other,” says Bronstein. Every summer, she and her colleagues flock to Crested Butte, Colorado, for what the Rocky Mountain Biological Laboratory there calls “the world’s largest migration of field biologists.”

“It can be costly for plants to make nectar,” Bronstein says, “so why do they make so much nectar? And the bees we’re studying can just chew a hole through the plant to get nectar — it’s faster than entering through the top. Why don’t they all just cheat? Why do they cooperate as much as they do when it doesn’t seem to be in their interest?”

The poet Lord Tennyson wrote that nature is “red in tooth and claw,” but nature also selects for cooperative traits. Bronstein thinks that studying cheating behaviors gives science a sharper tool for exploring cooperation. “If we can understand when and why other organisms cooperate even in the absence of effective policing,” she says, “we may gain a better sense of the conditions that promote cooperation — even in our own species.”

A Standing Army

Yellow 54’s job isn’t as easy as it looks, explains North Carolina State University ecologist Rebecca Irwin. Her lab is studying Yellow 54’s species as well as a handful of other bumblebee species found in the Rocky Mountains. The commonly robbed flowers have tubular blooms, making it tough for a fat little bumblebee to clamber past the anthers to the nectar. Still, these flowers evolved that shape because it confers an evolutionary advantage.

The tubular shape limits the kind of visitors a plant can have and fosters a special relationship with certain pollinators. As a result, those pollinators tend to restrict their forays to a few species of plant, and that helps keep pollination successful because creatures don’t pick up and squander pollen on the flowers of other species. “But there are costs to having this shape,” says Irwin, “and nectar robbing is one of them.”

Even underneath our feet, crucial mutualisms are being tested. Evolutionary ecologist Joel Sachs from the University of California, Riverside, studies legumes — plants belonging to the same family as peas — which release chemicals that invite soil-dwelling bacteria to build nodules, or tumorlike lumps in the plants’ roots. The plants get nitrogen in a usable form from the bacteria, and in exchange the bacteria receive some form of carbon from the plant. Nitrogen comprises 78 percent of our atmosphere and is a key resource for plants. Until the industrial era and modern fertilizer, it was available to plants only from soil bacteria or lightning, which reacts nitrogen and oxygen together, causing a usable form to rain down.

Legume
Legume
Some plants, like this legume, can’t use atmospheric nitrogen. Instead, they get it from soil bacteria (which form the nodules in this image), which extract carbon in return.
Wim van Egmond/Science Source

Most soil bacteria don’t have the genetic chops to form these nodules, but they could still hitchhike into the nodules with the good-buddy mutualist bacteria, joining in the carbon feast without offering up a nitrogen payoff. Flowering plants might not be able to stop bees that steal nectar through a hole in the side of a bloom, but cheating bacteria often get caught. “They’re not very good at persisting within the host tissue,” says Sachs. “Our most recent data shows that plants can put the screws on the bacteria. The plant cells infected by the non-nodulating strains go through programmed cell death.”

Frederickson, the University of Toronto ant researcher, points out that mutualisms aren’t about to break down, and she doesn’t think that the bad behavior from “cheater” bees to bacteria deserve such a harsh label. In a 2015 paper in Ecology Letters, she, Bronstein and others reasoned that to consider an organism a cheater, three things must be true: The organism must gain an advantage, the partner must suffer, and the organism must have evolved from a mutualistic relationship.

“Maybe these cheating species have always had that behavior,” Frederickson says. She points out that most mutualisms remain strong because there is little or no gain from cheating. For example, some 700 species of trees in the tropics make specialized cavities to house ant colonies. These ants, in the words of naturalist Alfred Russell Wallace, are a “standing army kept for the protection of the plant.” The ants protect the trees by eating and stinging herbivorous insects. “These ants, such as some in the Amazon, are just looking for food,” Frederickson says. “They should always be looking for food. There’s nothing to be gained from cheating because that would hurt their short-term interest. The benefit to the plant is a byproduct of the ants’ self-interest, and a lot of mutualisms work like that.”

Even when the ants’ self-interest is less immediate, Frederickson doesn’t expect cheating in this kind of mutualism. In Kenya, ants build colonies in the swollen thorns of acacia trees, which offer both a home and a source of nectar. In exchange, the ants bite the giraffes and elephants that stop to nibble. This protects the tree, while also ensuring that the ants won’t be living in a pile of splinters.

Still, some researchers argue that most mutualisms persist even when cheaters are punished for their actions, raising the possibility that nature could be more cooperative than we tend to assume. Or maybe these partnerships include undocumented benefits that solder the bond. For instance, researchers have turned up so-called cryptic, or hidden, benefits in some of these mutualisms.

In one well-studied case, cleaner fish nip away parasites from host fish but sometimes cheat by nipping at the flesh of the host. In a 2007 paper in the journal Frontiers in Zoology, Redouan Bshary and others said “the tactile stimulation that cleaners provide with their pectoral and pelvic fins might bear additional positive effects, i.e. through calming, similar to massage in humans.” That soothing massage, and the parasite removal, might make up for the occasional nip. So mutualisms can be more complex than they seem.

Wrasse
Wrasse
This roving coral grouper fish is groomed by a bluestreak cleaner wrasse. The cleaner fish sometimes steals a bite of flesh.
Alex Mustard/Naturepl.com

Flight of the Bumblebee

Yellow 54 has long since met her demise — bumblebees only live up to a year — but Irwin’s lab continues to follow up on Wang’s fieldwork, returning to the Rocky Mountains.

It turns out that Yellow 54 was a tiny iconoclast: Most individual bumblebees either seek nectar legitimately or rob, but they rarely combine the two approaches in a single forage for food. Irwin and her colleagues are trying to figure out why the behaviors vary, even within the same species. They measured the bees’ tongues — chilling the insects and unfurling the organ with tiny forceps — to see if size affected the frequency of robbing. (It doesn’t.) They took genetic material from every tagged bee and hope to investigate whether cheating is more common in certain nests. And they want to see if the robbers’ colonies are bigger or smaller than those of rule-follower bees.

They’re also investigating if subalpine plants that are routinely robbed suffer from it. Irwin says this likely varies by species and location. If a plant’s primary pollinators are hummingbirds, marauding bumblebees stealing the nectar make it hard for the plant to reproduce. But if a plant is primarily visited by bees and gets thousands of visits, the occasional theft might not matter.

The lab also wants to learn how bees figure out a shortcut to the nectar. “There are a lot of hypotheses for why bees rob,” Irwin says. “Some people think it’s an innate thing that they all know how to do, some think they saw another bee rob or had some sort of experience that led to the behavior. We want to know how they make the decision to either rob or go legit.”

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