Citation:

Tobias, Z., A. Fowler, A. Blakeslee, J. Darling, M. Torchin, A. Miller, G. Ruiz, AND C. Tepolt. Invasion history shapes host transcriptomic response to a body-snatching parasite. MOLECULAR ECOLOGY. Blackwell Publishing, Malden, MA, 30(17):4321-4337, (2021). https://doi.org/10.1111/mec.16038

Impact/Purpose:

Range shifts caused by rapidly changing environmental conditions and continued anthropogenic transport of exotic species are redistributing global biodiversity, blurring biogeographical lines, and bringing novel combinations of species and genes into contact. Understanding how species will respond to these novel encounters, spanning recent and distant timescales, is of critical importance to predicting and managing impacts to native ecosystems. Our study investigated the gene regulatory response of Rhithropanopeus harrisii to infection by Loxothylacus panopaei, and how it differed among populations with different histories of parasitism.

Description:

By shuffling biogeographical 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 behaviour. 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 (i) long-term sympatry between host and parasite, (ii) new associations where the parasite has invaded during the last 60 years and (iii) 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 moulting. 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. 

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