Coevolutionary dynamics and geographic mosaics in the Social Parasite Harpagoxenus sublaevis and its two Host Species

Social parasites such as bees, wasps and ants parasitize complete
insect societies. They take advantage of the brood care behaviour
of other social insect species, and thus avoid the costs of
parental care similar to avian brood parasites such as cuckoos and
cowbirds. The European social parasite Harpagoxenus sublaevis is an
obligate slavemaking ant species that exploits mainly two closely
related host species of the genus Leptothorax. To found a new
colony, a slavemaking queen invades a host colony, kills the
resident queen and workers. The inseminated queen raises the alien
brood and the later emerging host workers accept the parasite queen
as their own and become slaves that carry out all necessary colony
tasks. A year later, slavemaking workers emerge, which conduct
regular slave raids on neighbouring host colonies for worker brood
to replenish the labour force of the slavemaker nest. These slave
raids can impose severe selection pressure on the hosts, as
slavemaking colonies attack several host nests per year and raided
host colonies often perish as a consequence of the attack.
According to the geographical mosaic theory of coevolution,
differences in the advance or trajectory of the coevolutionray
process between local communities are predicted due to their
composition and the strength of ecological selection pressures
through competition and resource availability. In our study system,
investigations of the impact of the slave making ant H. sublaevis
at several geographic distant sites allow general conclusions on
the virulence, the degree of reciprocal adaptation and
specialization of the species, and the evolutionary trajectories
within this host-parasite system. The European slave making ant H.
sublaevis and its host species are good examples as parasites and
hosts are widely distributed throughout Eurasia whereas other
social parasites use host species with small or patchy populations,
e.g. Myrmoxenus or Chalepoxenus, where selection should be strong
to decrease their virulence. Furthermore H. sublaevis produces a
large army of slave making workers indicating that this species
remains highly virulent. In accordance with the assumption of a
geographic mosaic in the interaction of H. sublaevis and its hosts,
these studies have shown that parasite prevalence is a good
predictor of the strength of reciprocal adaptation in different
communities. In our genetic, chemical and behavioural studies we
could show that H. sublaevis prefers the smaller host L. muscorum,
which is more limited in dispersal than its larger competitor L.
acervorum. Both hosts showed differences in defense strategies of
which L. acervorum is the more aggressive host, while L. muscorum
tend to flee when getting into contact with its parasite. Moreover
for the genetic more variable parasite the chemical profile of L.
muscorum may be easier to imitate as this host is more limited in
gene flow than its counter part. Further explanation of the better
resemblance of the parasite to its smaller host could be the easier
acquisition of the more volatile shorter hydrocarbons. Also in the
field manipulation study both host species showed different
responses to the parasite pressure of H. sublaevis following the
two strategies, investment in sexuals or in workforce. Moreover our
crossfostering experiment indicated that the local parasite showed
a greater impact on its hosts than the allopatric one. This led to
the conclusion that coevolutionary trajectories differ between
communities, asumed by different historical processes, community
context and ecological conditons at each site which confirms the
geographic mosaic theory of coevolution.