COLUMBUS, Ohio – A genetically unusual population of ants is changing some of the fundamental ways researchers think about insect colonies.
Social insects, like ants and bees, thrive on the caste system – a precise division of duties among colony members. In most of these societies, environment is thought to influence whether larvae develop into queens or sterile female workers, said Steve Rissing, a professor of evolution, ecology and organismal biology at Ohio State University.
But in a new study, Rissing and his colleagues found some genetically odd colonies of harvester ants (Pogonomyrmex), that don't seem to abide by the traditional rules of caste development. They found that genetics – not environment – determines the fate of a developing ant, and consequently the role it will play in the colony.
The researchers report their findings in the latest issue of the journal Current Biology. The team was led by Sara Helms Cahan, an assistant professor of biology at the University of Vermont.
A typical ant colony includes one queen and, in the case of harvester ants, hundreds or thousands of sterile female workers (worker ants are always female and, with a few exceptions, sterile. Soldier ants are larger versions of workers.) During her lifetime, which can last as long as 20 or 30 years, a queen produces mainly worker eggs.
Male ants, which come from unfertilized eggs, typically serve one purpose: to mate with a queen. Males are usually in short supply, and a queen produces male eggs only when it's time to make more colonies. Then a queen produces eggs that give rise to both males and queens (reproductive females). The males and new queens swarm out of the nest, mate, and the young queens try to establish a new a colony. Males, which have short life spans, die shortly after mating.
The type of ants in this study – harvester ants – are one of the largest insect societies in the western United States, with ranges covering hundreds of miles and nests so large they're visible from airplanes.
"This is the ant that runs the west – it's everywhere," Rissing said.
The researchers had noticed that in certain areas – mainly southeastern Arizona and New Mexico – some of the male harvester ants looked different. So they collected several dozen pairs of queens and males and brought these pairs back to the laboratory for genetic testing, with surprising outcomes.
"The DNA of some of these ants was just weird – we certainly didn't expect to get the results that we did," Rissing said. "It seems that the queens in these colonies mate with males from two different genetic lineages. And when a queen and male with the same lineage usually mated, it usually produced a reproductive female – another queen. But when a queen and male from different genetic lineages mated, that pairing overwhelmingly produced a sterile worker.
"This kind of reproductive behavior is very different from what we expect to see in ant societies," he continued. "We'd expect to see the same DNA sequence from all ants in a given colony. But that's not what happened here."
It didn't matter that the laboratory experiments mimicked the founding of a new colony, which depends heavily on workers and only needs one queen: when a queen and male of the same lineage mated, they produced eggs that would give rise to many queens. The results also showed that all of the eggs produced became workers when a queen mated with an alternate-lineage male.
Traditional interpretations of social insect colonies would dictate that the need for workers would influence the fate of an ant's role, thereby overriding any genetic predisposition; this study shows that isn't always so.
These harvester ants had two different genetic lineages the researchers referred to as H1 and H2.
Each H1 and H2 queen was paired with either an H1 or H2 male. In nature, ant queens mate during just one period of time but mate with many males during that time (this causes the queen to build up a sizeable sperm bank.) Queens can store sperm and lay eggs during their entire lifetime.
All queens in the study laid about 60 fertilized eggs, but only 0.3 percent of the eggs from the same-lineage pairing (H1 queen and male; H2 queen and male) developed to adulthood. The queen raised these reproductive females – genetically queens themselves – as workers, although the researchers noted that these ants apparently had difficulty fulfilling their role as workers.
"The same-lineage ants that did make it to adulthood had almost completely lost their ability to develop into functional workers," Rissing said.
In contrast, 87 percent of the alternate-lineage eggs became successful adult workers.
"It's clear what the queen must do – she must mate with more than one male," Rissing said.
The researchers surmised that harvester ant queens can probably tell the difference between the males they mated with. The researchers also noted that the males were different colors, depending on what lineage they belonged to. In the wild, a queen may use this information to make sure she has enough sperm from males of both lineages, which would ensure the success of the colony.
Interestingly, males apparently cannot tell the difference between females. (Rissing said that he and his colleagues could tell the difference only with the help of modern molecular laboratory technology.)
"If males could, that might spell the end of a colony, as males may prefer to mate with a queen of the same lineage," Rissing said. In theory, a male ant wants his genes to live on. If his sperm fertilizes an egg from a queen with a different lineage, his genes will die with the sterile female worker that is produced.
"This population of harvester ants depends on this two-lineage system to survive," Rissing said. "The hybrid worker caste is what links the two otherwise independent H1 and H2 genome-based populations. So far, this is a fairly unusual finding. But as we gain access to more and more tools that help us understand what's going on at the molecular level, we'll likely find that a lot of social insects and other animals aren't conforming to our predictions and expectations."
Rissing and Cahan conducted this study with Glennis Julian of the University of Arizona, and Tanja Schwander and Joel Parker, both with the University of Lausanne in Switzerland.
This work was funded by grants from the Durfee Foundation, the Swiss Society of Naturalists and the Swiss National Science Foundation.
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