Diverse life history traits of the formicine-ant species. In clockwise order: (A) Members of F. fusca, who practice independent colony formation; (B) F. obscurepes, which represents the Formica Integra group (Nearctic member of the paraphyletic Rufa group); (C) Formica Gynocrates, which represents the facultatively-dulotic species in F. sanguinea with a worker from Formica vinculans; and (D) The highly modified worker of Polyergus myrmex, which represent the obligately-dulotic formicine ants of the genera Polyergus to bees and Rossomyrmex. Credit: Alex Wild
A story that made the news, a lower-class, but downtrodden, family infiltrates a wealthy neighborhood's house. All hell breaks loose.
If this sounds like the setup of 2020's Academy-award-winning film sensation "Parasite," you'd be right. It could be used as a plot-driver to feature one of the most diverse animal species on Earth: ants.
Christian Rabeling, Arizona State University researcher, is now an associate professor of organismal evolution biology. He can tell you a story that took 30 million years to make, about a myrmecological wonder, the evolution in social parasitism in Ants.
His team includes Marek L. Borowiec (a former post-doctoral researcher), now assistant professor at University of Idaho and Stefan P. Cover (long-term friend, colleague, and safe keeper of the Museum of Comparative Zoology, Harvard University), who have revealed the latest twists in understanding the evolution of ant social paralysis.
Rabeling, who is a professor at ASU's School of Life Sciences as well as a core researcher for the university's social insect group, said that it was important to identify the conditions that ant life histories and how they transition from cooperative colony life into exploitative social parasitism.
Rabeling is fascinated with social parasitism. He first studied this behavior in leaf-cutter and then, in his most recent study, Formica ants.
"So, the first question that was asked was how did Formica ants develop? Rabeling said that no one had performed a thorough phylogenetic analysis.
First, a group of Formica ants lost their ability to form the hub of ant lifecolony formationindependently. After this loss, two more complex social parasitic behaviors occurred.
Rabeling stated, "Here we show that social parasites evolved out of an ancestor that lost his ability to set up new colonies independently and that highly specialized parasites may evolve from less complicated social parasite syndromes."
Rabeling discovered that the same plotline for an ant story was repeated over and over again, just like Hollywood's most successful movies.
Rabeling stated that social parasitism was a life-style strategy that has evolved at least 60 times in Ants. More than 400 socially parasitic species have been identified from six closely related subfamilies.
The online edition of Proceedings of the National Academy of Sciences includes the study.
The supergroup of ants
Rabeling selected Formica ants from the 14,000 species of ants he had to study. This supergroup (or Genus) contains 172 species, with half of them showing social parasitic behavior. It is one of the largest on Earth.
The first step in understanding Formica social parasites better was to create a global evolutionary tree. This allowed them to better understand the historical relationships among the species and also gave them a glimpse into how different species became social parasites.
Scientists use the DNA level to determine the branching relationships among Formica ant species. They also study the inheritance of traits that influence social behavior.
Rabeling's group collected DNA samples from 101 Formica species, which represent all 10 species groups. These data were calibrated over evolutionary time and then calibrated.
They demonstrated that this supergroup was one the most successful in animal life's history, having originated in the Old World about 30 million years ago. It then dispersed multiple times to the New World as land bridges were built.
They discovered that Formica had a common ancestor around 33 million years ago. This suggests that Formica was likely to have originated in Eurasia during an Oligocene period, which followed a long global cooling period.
Rabelings' team took DNA samples from 101 Formica species and calibrated them across the evolution of time. This supergroup of ants was one of the most important in the history and evolution of life. It originated in the Old World about 30 million years ago, and then dispersed multiple times to the New World. Credit: Arizona State University
Bad actors
The colony is the hub of antlife. Underneath a typical ant hill lies a netherworld. This can be several feet underground and is connected to a complex ant subway system that includes tubes and tunnels.
They are adaptable and very adaptable. They can live under boulders, in trees or completely underground without a hill.
A colony is composed of one or two egg-laying queens, many sterile females (workers and soldiers), and often, many winged sexual males. The size of colonies can vary from small rural ones to large urban ones. For example, Formica fusca has colonies with 500 workers while Formica yessensis colonies have 300 million workers.
Many ant behaviors are social and can often be compared to humans. Some are very good: they live in peace, work together to find food and care for their children. Others have turned out to be bad actors, raiding nests of rival species, zombifying worker ants and imposing a caste system in order to benefit the monarchy a all-too-dominant princess.
There are three main types of social parasites that ants have: 1) temporary 2) permanent (pirate ants who steal worker broods from other nests).
Rabeling stated, "We were searching for an ant group that could provide all three life histories. We found it with Formica Ants."
After carefully analyzing all the Formica species' life histories in a huge table and aligning them with the DNA timeline for when each species split, they noticed a pattern: The 3 major social parasites developed at distinct time points.
Rabeling said, "This was a moment in clarity." It's almost like you have many mosaic pieces. One stone can be placed here, another there, and then you'll find a new observation which adds another piece to your mosaic. Once you add the evolutionary time context, it's easy to see the whole picture. It is deeply satisfying."
Rabeling demonstrated that social parasitism was first developed around 18 million years ago. This process begins when the queens lose their ability to form colonies by themselves.
The queens of temporary socially parasitic ant species invade the host nest and kill the queen(s). The host workers then raise the parasitic queen's offspring. The host workforce is slowly replaced until it is entirely made up of temporary social parasite species.
Rabeling stated that "interestingly, evolutionary reversals of social parasitism and independent colony formation were not recovered," suggesting that a transition into a socially parasitic lifestyle cannot be reversed.
The main event has seen the secondarily transformation of more socially parasitic species to other life histories. These include dulotic or permanent social parasitism.
The queens of the dulotic social parasites are temporary social parasites who start their colony's life cycle as temporary social hosts. Once enough workers have been raised, they organize raids on nearby nests to capture their brood. While some brood is eaten, most of the workers hatch in the parasite's nest.
Rabeling said that "they think they're right at home so they don't recognize that they're in another species' nest."
Rabeling's research showed that dulotic behavior developed sometime before 14 million years ago. This is much earlier than temporary parasites. Dulotic behavior and temporary social paralysis did not develop simultaneously in Formica. Instead, dulosis was developed secondarily by a temporary socially dependent ancestor.
Rabeling stated that "the single origin of dulotic behaviour in a diverse Clade of Temporary Social Parasite species supports the hypothesis dat dulosis originated only under rare circumstances." Rabeling points out that Charles Darwin was unable to explain one species of dulotic ant in "Origin of the Species".
Darwin wrote, "By which steps the instinct of F. sanguinea was born I will not pretend that conjecture."
Rabeling is amazed at this history. "It's really amazing that you can trace back the ant question all of the way to the Origin of Species," he said.
Charles Darwin was unable to explain the origin of one species of dulotic ant species in his Origin of the Species Book. Even Darwin was confused. Darwin wrote that I won't pretend to know the exact steps by which F. sanguinea developed its instinct. Here is Darwin's original sketch of a parasitic Formica Ant raiding the pupae of a rival nest. Credit: Source: The Origin of Species
Three hypotheses, not all mutually exclusive, have been offered to explain this highly specialized behavior. They are 1) predation; 2) brood transportation; and 3) territorial competition.
Rabeling stated, "Our phylogenetic and behavioral results indicate that predatory behavior by temporary social parasites could have led to the evolution facultative dulosis (Formica)".
In the final example, the most persistent social parasite (i.e. Inquiline species were first discovered 12 million years ago. They are more tolerant of their host queen and can continue producing host workers, while inquiline queens concentrate their reproductive efforts on sexual offspring.
Rabeling describes the complex behavior by saying that there is a queen who acts parasitically and a queen who acts socially. The two don't integrate for reasons we don’t understand. They live separate lives, and even though they share the same nest, they end up creating two species: the host social parasite and the inquiline. This is a fascinating example of how two species can evolve in direct sympathy. Their different life histories are one reason why they don't interbreed.
Inquilines are dependent on their hosts, and many inquiline species have lost their worker caste.
F. talbotae is the only workerless social parasite that has been confirmed to be inquiline inquiline. F. talbotae, however, is unique because it cannot live peacefully with a queen in a colony. It seems to be targeting host colonies that have lost their queens. This is a very specialized lifestyle, which is only known to a few other species of ants.
Rabeling stated that Formica talbotae was phylogenetically nestled within the difficilis Clade. This suggests that worker-less permanent paralysis evolved from an ancestor who practiced temporary social parasitism. This is the first empirical evidence to support an evolutionary transition from worker-less temporary social parasitism to workerless inquiline social.
The best picture
If you look at the evolutionary path of social parasite evolution, there are many plots that are very similar for all parasitic life history disorders across all eusocial insect species. This can lead to a new picture.
Rabeling stated, "Our findings indicate that social parasites are easily derived in socially polymorphic organisms"
The researchers concluded that brood-stealing or dulotic social parasitism was a common phenomenon in Formica, Polyergus and Rossomyrmex formicine genera. Multiple transitions were made in the genus Formica to more complicated socially parasitic lives histories.
Finally, Formica reflexa, a permanent social parasite, and Formica talbotae the workerless, were created independently of their temporary social parasitic ancestors. Rabeling hopes that this knowledge will inspire others to make new discoveries.
Rabeling stated that the study "outlines the life history changes associated to the transition from an exploitative socially parasitic life history to a cooperative eusocial life history." "Given the diversity of social parasite species within the genus Formica and the high degree of behavioral and morphological specialization, socially parasitic Formica species seem to be an ideal study organism for investigating caste determination as well as exploring the genetic basis of behavioral and life-history evolution,
Attractions coming
This information has been available to scientists for many decades, thanks to extensive fieldwork and the study of the life histories of individual species. With scientific technological advancement and low-cost DNA sequencing now available, it is possible to link ant behavior with genes and molecules that could be playing a part behind the scenes.
Rabeling said, "This is a wonderful period right now." "The most exciting part about this study was the ability to ask these kinds of questions.
Continue reading: Study shows that ant genome erosion is linked to the loss of social, behavioral, and functional traits in 3 inquiline species
