Climate shapes arms race between ants and their social parasites

The "slave-making ant" Temnothorax americanus (left) and its host Temnothorax longispinosus
Photo Credit: ©: Romain Libbrecht

The battle between ant hosts and their social parasites is strongly influenced by climate. Temperature and humidity shape how the ants behave, communicate, and even evolve — while host and parasite respond with very different genetic strategies. These are the findings of two recent studies in which researchers at Johannes Gutenberg University Mainz (JGU) and the Senckenberg Biodiversity and Climate Research Centre combined behavioral experiments with state-of-the-art genomic analyses. "Climate clearly explains the variation in host and parasite behavior better than parasite prevalence itself," says Professor Susanne Foitzik, senior author of both studies and chair of Behavioral Ecology and Social Evolution at JGU.

In the first study, published in the Journal of Evolutionary Biology, the team examined a parasite, the so-called "slave-making ant" Temnothorax americanus, and its host, the ant Temnothorax longispinosus. The social parasite invades host nests and steals their brood, which later grows up to work for the parasite colony – an extraordinary form of social parasitism. The researchers focused on how the ants' behavior and chemical communication vary across different climates. By comparing ten natural populations along a 1,000‑kilometer north-south gradient in the United States, they found that climate influenced the conflict more strongly than the local frequency of parasite colonies.

Professor Dr. Susanne Foitzik, chair of Behavioral Ecology and Social Evolution at JGU
Photo Credit: © Courtesy of Susanne Foitzik

Differences in aggression

"Host and parasite populations differ in aggression, raiding activity and their chemical profiles, and these differences follow the temperature and humidity gradient," explains first author Dr. Erwann Collin, who recently completed his doctoral research at JGU's Institute of Organismic and Molecular Evolution. "In warmer and drier regions, host ants showed reduced aggression and often carried their brood away rather than defending the nest. Social parasites from these regions, on the other hand, were more active and more aggressive during raids." In cooler, humid northern sites, the opposite pattern emerged: hosts defended their nests vigorously, while parasites behaved more cautiously.

Chemical communication also shifted systematically with local climate conditions – specifically in terms of the cuticular hydrocarbons, the waxy surface chemicals ants use to recognize nestmates and prevent drying out. Because all colonies were kept under identical laboratory conditions for a full year prior to testing, these differences reflect evolved, long-term adaptations rather than short-term environmental responses.

Genetic adaptations to climate

Building on these findings, the second study, published in Molecular Biology and Evolution, investigated the genetic basis of these climate‑dependent differences in traits. Using advanced molecular methods – including whole-genome sequencing and transcriptomics, the analysis of active genes – the researchers explored how natural selection shapes the genomes of host and parasite populations along the same climatic gradient.

"We discovered a 'geographic mosaic of coevolution', with parasite populations differing more strongly from one region to another than host populations," explains Dr. Maide Macit, first author and recent doctoral graduate of JGU. "Despite these differences, the two related species show similar genetic adaptations to climate, including genes involved in stress tolerance and resistance to drying out." However, their responses to the parasite-host-conflict diverged strongly.

In the host ants, evolution has acted on genes involved in signaling and chemical sensing – genes that help them detect and defend against invading parasites. Several of these genes showed clear signs of selection imposed by the social parasite. Although these genes normally produce immune-related proteins that fight microbes, they appear to be deployed here against a very different kind of enemy: another ant species. In the parasite, evolution has instead targeted regulatory genes that control how raids are coordinated and carried out.

Changing ways of defense

Gene-expression analyses – showing which genes are actively switched on – further underscored how differently the two species respond. "In the hosts, gene activity mainly reflected how common parasite colonies were in each area, whereas in the parasites it was influenced much more strongly by local climate," explains Dr. Barbara Feldmeyer, co-senior author of the study and researcher at the Senckenberg Centre. "We also found that variation in these chemical profiles was linked not only to genetic changes in the enzymes that produce them, but also to changes in odorant-receptor genes – the genes coding for proteins which enable ants to sense chemical signals." This pattern shows how central chemical communication and chemical recognition are to the conflict – and that evolution repeatedly acts on these traits as hosts and parasites adapt to each other.

Together, the two studies offer one of the most integrated perspectives to date on how strongly environmental conditions and biological conflict shape evolution across landscapes. "Host-parasite systems are classic evolutionary arms races," says Susanne Foitzik. "Because both species rely on chemical communication to recognize each other, their interaction provides a powerful framework for future studies on molecular coevolution."

Published in journal: 

1. Journal of Evolutionary Biology

2. Molecular Biology and Evolution

Title:

1. Climate and parasite pressure jointly shape traits mediating the coevolution between an ant social parasite and its host

2. Genomic Signatures of Selection Across Climate Gradients and a Geographic Mosaic of Coevolution in an Ant Social Parasite–Host System

Authors: 

1. Erwann Collin, Maide Nesibe Macit, Marti Wittke, Chris Hörrmann, Claudio Haase, Laura Heil, Maria Litto, Florian Menzel, Barbara Feldmeyer, and Susanne Foitzik

2. Maide Nesibe Macit, Erwann Collin, Maria Esther Nieto-Blazquez, Marion Kever, Maria Litto, Esther Jaitner, Markus Pfenninger, Barbara Feldmeyer, and Susanne Foitzik

Source/Credit: Johannes Gutenberg University Mainz

Reference Number: ebio121525_01

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