Dual transcriptomics reveals co‐evolutionary mechanisms of intestinal parasite infections in blue mussels Mytilus edulis

Abstract

On theoretical grounds, antagonistic co-evolution between hosts and their parasites should be a widespread phenomenon but only received little empirical support so far. Consequently, the underlying molecular mechanisms and evolutionary steps remain elusive, especially in nonmodel systems. Here, we utilized the natural history of invasive parasites to document the molecular underpinnings of co-evolutionary trajectories. We applied a dual-species transcriptomics approach to experimental cross-infections of blue mussel Mytilus edulis hosts and their invasive parasitic copepods Mytilicola intestinalis from two invasion fronts in the Wadden Sea. We identified differentially regulated genes from an experimental infection contrast for hosts (infected vs. control) and a sympatry contrast (sympatric vs. allopatric combinations) for both hosts and parasites. The damage incurred by Mytilicola infection and the following immune response of the host were mainly reflected in cell division processes, wound healing, apoptosis and the production of reactive oxygen species (ROS). Furthermore, the functional coupling of host and parasite sympatry contrasts revealed the concerted regulation of chitin digestion by a Chitotriosidase 1 homolog in hosts with several cuticle proteins in the parasite. Together with the coupled regulation of ROS producers and antagonists, these genes represent candidates that mediate the different evolutionary trajectories within the parasite's invasion. The host-parasite combination-specific coupling of these effector mechanisms suggests that underlying recognition mechanisms create specificity and local adaptation. In this way, our study demonstrates the use of invasive species' natural history to elucidate molecular mechanisms of host-parasite co-evolution in the wild.

Infection by invasive parasites increases susceptibility of native hosts to secondary infection via modulation of cellular immunity

“…While mussels can mount a cellular immune response and engulf pathogens in the haemolymph (Galimany, Sunila, Hégaret, Ramón, & Wikfors, ), this immune response cannot affect M. intestinalis directly because it occurs in the gut and is too big to be encapsulated. Consequently, the production of reactive oxygen species (ROS) is the predominant immune effector in a M. intestinalis infection (Feis et al., ). Although haemocytes are not directly involved in an immune response against M. intestinalis , the efficiency of a cellular immune response to the secondary bacterial infection was nevertheless affected.…”

“…Six month after infection, M. intestinalis will have reached adulthood and accumulate damage over an extended period of time representing a chronic infection (Feis et al., ) that is typical for the natural situation (Elsner, Jacobsen, Thieltges, & Reise, ). At this time point, each mussel was transferred to a 800‐ml beaker filled with sterile‐filtered sea water.…”

“…In controlled laboratory infections, a negative effect of infection on mussel condition was confirmed but did also not lead to elevated mortality (Feis, Goedknegt, Thieltges, Buschbaum, & Wegner, ). The results of that experiment also showed that infection by M. intestinalis evokes a strong immune response involving reactive oxygen species (ROS) that could also inflict self‐harm and make an immune response to the infection costly (Feis, John, Lokmer, Luttikhuizen, & Wegner, ).…”

“…The primary immune response to bacteria is mediated via a cellular immune response (i.e., phagocytosis; Canesi, Gallo, Gavioli, & Pruzzo, ). Since haemocytes will not directly interact with M. intestinalis , which is living in the gut lumen of the host, immune resources of the host might be diverted to the ROS‐mediated defence against M. intestinalis (Feis et al., ) and not be available for the cellular immune response against Vibrio . Such a trade‐off might make the host more susceptible to secondary infections (e.g., Vibrio ) and was already observed for primary infections of oysters with herpes virus that rendered the host more susceptible to secondary Vibrio infections by suppression of immunity (de Lorgeril et al., ).…”

Evolutionary pathways to invasive success: thermal adaptation, hybridisation and parallel evolution in a marine global invader

“…Oxidative stress related genes can also function in general cellular stress responses, and thus, may evolve in response to various selective environments (Tomanek 2012). Exposure to hyposaline stress, marine pollutants, ocean acidification, pathogens, as well as increased rates of food consumption, have been shown to induce the production of ROS, and may leave signals of selection on genes involved in oxidative stress (e.g., Lockwood and Somero 2011b;Dowd et al 2013Tomanek 2015;Feis et al 2018). Nevertheless, observed signatures of positive selection on oxidative stress-related genomic functions provide corroborative evidence that selective pressures acting on ROS-scavenging cellular pathways are primary feature differentiating M. galloprovincialis from cold-adapted congeners (Gracey et al 2008;Tomanek 2012;, also see Somero et al 2017).…”