Researchers have uncovered an unusual survival strategy in Iberian harvester ants that turns basic biology on its head: The queens can produce eggs that develop into two different ant species.
A team uncovered this bizarre reproductive trait while trying to solve the mystery of a missing ant species. Preliminary data seemed to show that the Iberian harvester ants, or Messor ibericus, were creating hybrid worker ants by reproducing with another species of harvester ant called Messor structor in the Mediterranean region.
But there was a problem. The Italian island of Sicily where the Iberian harvester ant colony was found is about 1,000 kilometers (621 miles) away from the closest known Messor structor population, said Jonathan Romiguier, a senior researcher at France’s University of Montpellier and senior author of a study published September 3 in the journal Nature detailing Messor ibericus’ method of reproduction.
“We had a strong suspicion that something was very unusual about this species, but to be honest, we were far from imagining just how unusual it really was,” Romiguier said. “It was this paradox that led us to investigate the case more closely.”
By studying more than 120 ant populations across Europe, sequencing the genomes of hundreds of ants and carrying out laboratory experiments over five years, the team arrived at a finding stranger than fiction as it watched two different species of ant, one hairy and one virtually hairless, emerge from eggs laid by a single queen.
As the researchers discovered, Iberian harvester queens’ eggs develop differently depending on whether the queen needs mates to produce future Iberian harvester ant queens, or a hybrid workforce that makes up 99% of the colony.
The findings are changing the way scientists understand ant reproduction, showing that ants can produce individuals of another species as part of their life cycle.
Jessica Purcell, assistant professor in the department of entomology at the University of California, Riverside, has encountered Iberian harvester ants while studying other ant species in Italy. Purcell was not involved in the new study, but she authored an article that accompanies the research.
“Harvester ants collect seeds from a variety of plants and bring them back to their colony,” she said. “Many species clip the plants close to their nest entrances so that they have vegetation-free circles around their nests, and then there can be a ring of dense or unusual vegetation beyond that boundary. This produces a distinctive look to the exterior of the nests.”
Messor ibericus and Messor structor once belonged to the same species that split over 5 million years ago, according to the study authors. Even after splitting, the two species lived in the same geographical area in Europe. In some parts of the continent, such as eastern France, the species still live in proximity to one another.
At some point, possibly as early as several million years ago, Iberian harvester ant queens lost the ability to produce their own worker ants, which are female. Researchers have yet to uncover why this happened, but it led the queens to mate with nearby populations of Messor structor ants to create a workforce that was a hybrid of the two species.
“We suspect it stems from an evolutionary conflict between queens and larvae, where a so-called ‘selfish’ genetic element skews larval development toward becoming queens to ensure its transmission to the next generation (since queens reproduce, while workers are largely sterile),” Romiguier wrote in an email.
Iberian harvester ants were then dependent on Messor structor ants for their survival, forcing the queens to track down males of another species, which is known as sperm parasitism.
Rather than dealing with such a time-consuming nuisance, Iberian harvester ants turned to another strategy of reproduction: cloning the sperm of Messor structor ants, a phenomenon called sexual domestication, the study authors said. Scientists have yet to observe this practice in any other animal.
“Much like humanity domesticating livestock, they eventually gained control over the reproduction of these males they once exploited in the wild,” Romiguier said. “This domestication of males became possible through their ability to clone a male from another species using just its sperm.”
Over generations, it became possible for Iberian harvester ants to maintain a lineage of cloned male Messor structor ants within their nest, eliminating the need to live in the same geographic area as another species and resulting in millions of invasive hybrid worker ants building colonies across the Mediterranean.
Iberian harvester ants are examples of a new mode of reproduction called xenoparous, with xeno- meaning “foreign, strange or different” and -parous meaning “produce, bring forth, give birth,” Romiguier said.
“Beyond ants, this shows for the first time the evolution of xenoparity, which is the need to propagate another species’ genome by means of its own eggs,” Romiguier said.
Sequencing the genome of the ants allowed researchers to determine that the only “pure” Iberian harvester ants were queens and males that can mate to produce future queens. Other Iberian harvester ant eggs fertilized with Messor structor sperm resulted in hybrid female workers.
When researchers explored how the Iberian harvester queen ants were able to produce Messor structor ants, they discovered that the queens cloned the male’s genetic material from sperm stored within their own bodies. Somehow, the queen can delete her own nuclear DNA and produce offspring that rely almost entirely on the sperm’s DNA.
These males, however, look different from the Messor structor males produced by Messor structor queens, and they have mitochondria containing Messor ibericus DNA, although it is less than 0.01% of the genetic material, according to the study.
The clone offspring are considered true clones because of how closely they genetically resemble their father, Romiguier said.
Over millions of generations, a clone genome can accumulate some mutations and differ more and more over time from the original first clone, he added.
“It is widely recognized that cloning essentially refers to the copy of the nuclear genome,” he said.
The team kept colonies of Iberian harvester ants in artificial nests in its lab. After monitoring them for two years, the researchers directly observed the birth of two different species of males with distinct genomes from a single queen.
Two Messor structor males that hatched were hairless, while three Messor ibericus males were covered with hair. In ants, hair is one of the criteria that helps differentiate species.
Going forward, the team plans to investigate the exact cellular mechanism that results in the cross-species cloning that Iberian harvester queens perform.
“Currently, we know that the mother’s genetic material is removed from the ovum at some point, leaving only the genetic material of the foreign male in the embryo,” Romiguier said. “However, we still do not know precisely how or when this maternal genetic material is eliminated.”
Understanding the natural cloning process in ants could provide insights for scientists trying to induce cloning artificially in other species, he said.
While hybrid offspring and androgenesis, or reproduction where the genetic material comes solely from the male, have been studied in other ants, the combination of both in this ant is surprising, said Dr. Jacobus J. Boomsma, professor of ecology and evolution in the department of biology at Denmark’s University of Copenhagen. Boomsma was not involved in the new study.
Boomsma said any traits the ants have evolved are adaptations driven by natural selection, and creating fitter hybrid workers provided a competitive advantage, allowing Iberian harvester ants to extend their range vastly.
“And then, having spread way out of reach of natural males of Messor structor, Messor ibericus queens evolved to clone these alien males under their own steam,” Boomsma wrote in an email. “It stabilized the system, but at the expense of losing most genetic variation. So in the long run (a couple of million years) this ant will likely go extinct (almost all asexual species do).”
Purcell called the discovery novel, noting that while there are already known and unusual mating systems in ants, Iberian harvester ants are among the weirdest — and present more mysteries yet to be understood.
“Figuring out the precise order of events in the female reproductive tract and the extent to which the queen can control the outcome for each egg (e.g. will a fertilized egg become a worker, or will her own genetic code be purged to produce a male?) is one of the many possible future directions of study in this amazing system,” Purcell wrote in an email. “I am really looking forward to seeing what Jonathan Romiguier and his team will tackle next!”
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