Invasion history shapes host transcriptomic response to a body-snatching parasite

By shuffling biogeographic distributions, biological invasions can both
disrupt long-standing associations between hosts and parasites and
establish new ones. This creates natural experiments with which to study
the ecology and evolution of host-parasite interactions. In estuaries of
the Gulf of Mexico, the white-fingered mud crab (Rhithropanopeus harrisii)
is infected by a native parasitic barnacle Loxothylacus panopaei
(Rhizocephala), which manipulates host physiology and behavior. In the
1960s, L. panopaei was introduced to the Chesapeake Bay and has since
expanded along the southeastern Atlantic coast, while host populations in
the northeast have so far been spared. We use this system to test the
host’s transcriptomic response to parasitic infection and investigate how
this response varies with the parasite’s invasion history, comparing
populations representing (1) long-term sympatry between host and parasite,
(2) new associations where the parasite has invaded during the last sixty
years, and (3) naïve hosts without prior exposure. A comparison of
parasitized and control crabs revealed a core response, with widespread
downregulation of transcripts involved in immunity and molting. The
transcriptional response differed between hosts from the parasite’s native
range and where it is absent, consistent with previous observations of
increased susceptibility in populations lacking exposure to the parasite.
Crabs from the parasite’s introduced range, where prevalence is highest,
displayed the most dissimilar response, possibly reflecting immune
priming. These results provide molecular evidence for parasitic
manipulation of host phenotype and the role of gene regulation in
mediating host-parasite interactions.