Hosts Are Ahead in a Marine Host-Parasite Coevolutionary Arms Race: Innate Immune System Adaptation in Pipefish Syngnathus Typhle Against Vibrio Phylotypes

Abstract

Microparasites have a higher evolutionary potential than their hosts due to an increased mutation rate and a shorter generation time that usually results in parasites being locally adapted to their sympatric hosts. This pattern may not apply to generalist pathogens as adaptation to sympatric host genotypes is disadvantageous due to a narrowing of the host range, in particular under strong gene flow among host populations. Under this scenario, we predict that the immune defense of hosts reveals adaptation to locally common pathogen phylotypes. This was tested in four host populations of the pipefish Syngnathus typhie and associated bacteria of the genus Vibrio. We investigated the population divergence among host and bacteria populations and verified that gene flow is higher among host populations than among parasite populations. Next, we experimentally assessed the strength of innate immune defense of pipefish hosts using in vitro assays that measured antimicrobial activity of blood plasma against sympatric and allopatric Vibrio phylotypes. Pipefish plasma displays stronger antimicrobial activity against sympatric Vibrio phylotypes compared to allopatric ones. This suggests that host defense is genetically adapted against local bacteria with a broad and unspecialized host spectrum, a situation that is typical for marine systems with weak host population structure.

Testing for local host–parasite adaptation: an experiment with Gyrodactylus ectoparasites and guppy hosts

“…In the following sections we expand on the potential explanations for local Gyrodactylus maladaptation, as well as the relative importance of ecological history and evolutionary lineage as drivers of host-parasite co-evolution. Although parasites are generally expected to have an evolutionary advantage over hosts (Ebert, 1994;Saarinen and Taskinen, 2005) due to their short generation time and potentially high host specificity, parasites have not always shown signatures of local adaptation to their sympatric hosts (Kaltz et al, 1999;Oppliger et al, 1999;Koskela et al, 2000;Lemoine et al, 2012;Roth et al, 2012;Konijnendijk et al, 2013;Sternberg et al, 2013). Our study reduced the methodological limitations of many previous studies, and our data indicate that Gyrodactylus does not generally show strong local adaptation to their sympatric guppy hosts.…”

“…Consistent with this, many studies have found that parasites show stronger signals of local adaptation to their hosts than hosts do to their parasites (reviewed in: Greischar and Koskella, 2007;Hoeksema and Forde, 2008) as evidenced by higher infection levels for a given parasite population on sympatric hosts than on allopatric hosts (Ebert, 1994;Saarinen and Taskinen, 2005). However, other studies have not found evidence of local parasite adaptation, or have found apparent local maladaptation of parasites: e.g., infection levels are higher on allopatric than sympatric hosts (Lemoine et al, 2012;Roth et al, 2012;Konijnendijk et al, 2013;Sternberg et al, 2013).…”

Coevolution of venom function and venom resistance in a rattlesnake predator and its squirrel prey

“…These functional data can then be analysed using the statistical approaches developed for assessing local adaptation in hostparasite systems [19,20]. Because local adaptation measures the net fit of genotype to environment at a metapopulation level, it can also be used as a measure of the net outcome of coevolutionary interactions, thus estimating the relative success of each partner and revealing which species is evolutionarily ahead in the interaction [19,21].…”

Adaptation to enemy shifts: rapid resistance evolution to local Vibrio spp. in invasive Pacific oysters

“…This results in asymmetric selection pressures in host-parasite coevolution favouring host adaptation over parasite adaptation. Indeed, it has previously been shown that activation of the pipefish Syngnathus typhle immune system is locally adapted to their phylogenetically divergent Vibrio communities [48].…”