Illuminating the evolution of social parasite ants

Date:
March 3, 2023
Source:
Rockefeller University
Summary:
The findings offer a new way to understand how some ants become
total layabouts.


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FULL STORY ==========================================================================
Ants are known as hard workers, tirelessly attending to their assigned
tasks - - foraging for food, nurturing larvae, digging tunnels, tidying
the nest. But in truth, some are total layabouts. Called workerless social parasites, these rare species exist only as queens, and they die without workers to tend to them. To survive, parastic ants infiltrate a colony of closely related ants, where, as long as they keep their numbers relatively
low, they and their offspring become the leisure class of the colony.


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It's long been thought that these determinedly lazy insects likely
evolved their queenly characteristics one by one, through a series of mutations, in an isolated setting. Now scientists in the Laboratory of
Social Evolution and Behavior at The Rockefeller University, together
with their collaborators at Harvard University, have a new theory. As
they report in Current Biology, they've discovered queen-like mutants -- parasitic ants that spontaneously appeared in colonies of clonal raider
ants, which are typically queenless.

"This mutant is like the precursor to other parasitic species," says
Waring Trible, lead author of the study. "It's a new way of understanding
how ants evolve to become socially parasitic." Delving into the genetics
of these unique ants could be a way to better understand the molecular mechanisms behind caste differentiation, or how an ant develops into a
worker or a queen, which remain unknown. It could also help illuminate biological development in organisms in general.

Hiding in plain sight Among the more than 15,000 identified ant species
are hundreds that qualify as social parasites. Born inside a host colony,
a parasitic ant will leave the colony, use a sex pheromone to attract a
male from another colony to mate with, and once pregnant, will infiltrate
the original colony or find another nearby.

She'll often use subterfuge to sneak past colony guards. The shampoo ant,
for example, will snatch a few ants just outside a nest entrance, lick
them to acquire the colony's signature chemical scent, and then lick
herself all over to transfer it to her own body. Chemically cloaked,
she then can slip inside to live out her life and reproduce both new
queens and males who mate outside the colony. The males die, and the
queens begin the cycle again.

Because of their uniqueness, they've been studied extensively by
biologists since Charles Darwin, still there's been a sticking point
in a prevailing theory of their evolution, says Daniel Kronauer, the
Stanley S. and Sydney R.

Shuman Associate Professor at Rockefeller University, and head of the lab.

They're closely related to their hosts, but if they had to acquire
these parasitic traits over time, they would need to be isolated during reproduction, otherwise interbreeding with their hosts would wash out
their unique traits.

But no one has found intermediately evolved ants -- ones with some social parasite traits but not others -- in the wild, says Kronauer.

When queen-like ants suddenly appeared among the clonal raider ants
in Kronauer's lab in 2015, Trible -- who was looking to investigate
genetic mechanisms behind caste differentiation -- took notice. Because
clonal raider ants typically have no queens and reproduce asexually,
the queen-like mutants stood out: they were born with wings, larger eyes
and ovaries, and as adults showed a general indifference towards labor.

But it turned out they were nothing new -- they'd had been hiding for
years in dense colonies whose numbers obscured their presence. Genetic
analysis revealed that they had mutated into existence inside the colony
in which they were first detected -- a community of otherwise normal ants
that Kronauer had collected in Okinawa, Japan, in 2008, and that still
lived in the lab. It was a clue that the typical story of parasite ant
invasion might need rethinking.

The researchers then ran a series of experiments and genetic analyses. One
of the first experiments was to isolate them to see whether the phenotype
was heritable. Because clonal raider ants reproduce asexually, they
didn't have to worry about interbreeding with other ants.

The queen-like mutants lay eggs that developed into copies of
themselves. "We knew we had something cool," Kronauer says.

They also tested behavior. Foraging parties composed entirely of
queen-like mutants were half the size of those of worker ants, and they
were far less likely to try to enlist other ants to track down food. These behaviors were a sort of intermediary between the diligence of worker
ants and the dependence of queens, and allowed the mutant ants to avoid
the dangers inherent to leaving the safety of the colony.

Despite laying twice as many eggs as their hosts, the ants self-regulate
their head count. As long as their numbers stay below about 25 percent
of the host population, they do well. More than that and they run into
trouble. Queens need help from workers to free their wings as they emerge
from the pupae, and if there are too many queens for the workers to look
after, they'll die entangled in their pupal skin.

"They seem to have the ability to regulate their own reproduction so that
they don't drive their host colony extinct, which is a very smart thing
for a parasite to do," says Trible, a former member of Kronauer's lab who
now runs his own lab at Harvard studying these and other mutants. "This provides these mutants the capacity to survive for long periods of time."
The influence of hormones Whole-genome sequencing revealed that the
parasitic queens have a mutation in chromosome 13, which is structurally similar to chromosomes that regulate colony social structure in other
ants. This mutant chromosome seems to contain a "supergene," a set
of genes that work together to create a phenotype. In this case, the
supergene contains more than 200 individual genes, a disproportionate
number of which assist in the metabolism of hormones. These include
genes that code for cytochrome p450 enzymes, which are required to
synthesize hormones in both ants and humans, and may play a role in
the creation of these highly unusual mutants. (This enzyme family may
be familiar to anyone who has been warned to not drink grapefruit juice
while taking certain medications because the juice inhibits the enzymes
from detoxifying the drugs.) It appears that with this single mutation,
"their form, the higher egg production, the behavior -- it can all shift
in a single mutational step," Kronauer says.

And if that's the case, Trible says, "it would be a way that it's actually possible to go from a normal ant to a parasite within a single species."
That idea -- that two very different forms of an animal can arise in a
single species -- gets at the heart of the mystery of ant castes. Because workerless social parasites arise from a very specific type of mutation affecting ant caste development, studying the queen-like mutants has the potential to reveal insights into the still-unknown molecular mechanisms
that allow ant larvae to develop distinct caste morphologies. "It provides
a very comprehensive framework in which to study their evolution,"
says Kronauer.

Size matters The findings could also lead to further research on an
important process of development known as allometric scaling that happens
in all animals, including humans, Trible says. Allometric scaling keeps
the tissues of an organism proportional to its body size as it grows.

Its mechanisms are unknown, but understanding them likely has relevance to
many aspects of human biology, including disease, says Trible. Perhaps queen-like mutants can provide a new avenue of investigation. "We
don't have good examples of mutations in fruit flies or mice or human
genetic disorders that break allometric scaling in such a dramatic way,"
he says. "We think this queen-like mutant will be a powerful tool for understanding caste development, and caste development is in turn an
ideal model to investigate these larger questions about how allometric
scaling works."
* RELATED_TOPICS
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# Insects_(including_Butterflies) # Evolutionary_Biology #
Invasive_Species # Mating_and_Breeding
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# Exotic_Species # Ecology # Environmental_Awareness #
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o Fire_ant o Ant o Wood_Bison o Bee
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========================================================================== Story Source: Materials provided by Rockefeller_University. Note:
Content may be edited for style and length.


========================================================================== Journal Reference:
1. Waring Trible, Vikram Chandra, Kip D. Lacy, Gina Limo'n, Sean K.

McKenzie, Leonora Olivos-Cisneros, Samuel V. Arsenault, Daniel J.C.

Kronauer. A caste differentiation mutant elucidates the evolution
of socially parasitic ants. Current Biology, 2023; DOI: 10.1016/
j.cub.2023.01.067 ==========================================================================

Link to news story: https://www.sciencedaily.com/releases/2023/03/230303105250.htm

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