On the Equivalence of Host Local Adaptation and Parasite Maladaptation: An Experimental Test

Abstract

In spatiotemporally varying environments, host-parasite coevolution may lead to either host or parasite local adaptation. Using reciprocal infestations over 11 pairs of plots, we tested local adaptation in the hen flea and its main host, the great tit. Flea reproductive success (number of adults at host fledging) was lower on host individuals from the same plot compared with foreign hosts (from another plot), revealing flea local maladaptation. Host reproductive success (number of fledged young) for nests infested by foreign fleas was lower compared with the reproductive success of controls, with an intermediate success for nests infested by local fleas. This suggests host local adaptation although the absence of local adaptation could not be excluded. However, fledglings were heavier and larger when reared with foreign fleas than when reared with local fleas, which could also indicate host local maladaptation if the fitness gain in offspring size offsets the potential cost in offspring number. Our results therefore challenge the traditional view that parasite local maladaptation is equivalent to host local adaptation. The differences in fledgling morphology between nests infested with local fleas and those with foreign fleas suggest that flea origin affects host resource allocation strategy between nestling growth and defense against parasites. Therefore, determining the mechanisms that underlie these local adaptation patterns requires the identification of the relevant fitness measures and life-history trade-offs in both species.

Infestation ofLernaea cyprinacea(Copepoda: Lernaeidae) in two invasive fish species in Romania,Lepomis gibbosusandPseudorasbora parva

“…Secondly, we have a host-parasite combination, L. gibbosus and L. cyprinacea, which have lived in sympatry in Europe for more than 100 years, and a newly arrived host species population (P. parva). Looking at our data this way, it fits the general model of a parasite species being more effective at infecting the sympatric rather than the allopatric host, showing that the parasite has had more time to develop adaptations for infecting the sympatric host species (Lemoine et al, 2012). However, the differences observed in the parasitological parameters between our host species could also be explained by ecological factors (local conditions, proximity of host and parasite in time and space, etc.…”

“…when invasive species expand their range (Lemoine et al, 2012). One of the factors considered to explain the success of these species is the release of the newly founded populations from the pressure exercised by their original parasites left behind in the initial environment (Mastitsky et al, 2014;Torchin et al, 2003).…”

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).…”

Host ecotype generates evolutionary and epidemiological divergence across a pathogen metapopulation

“…Further support for the importance of spatial scale of pathogen dispersal on local adaptation comes from a recent cross-species comparison that showed hosts to be least resistant to their local parasites, and most resistant to parasites collected several tens to hundreds kilometres away [15]. However, the lack of gene flow among widely separated populations may reduce their evolutionary potential and hence, prevent local adaptation at larger spatial scales [16,17]. Together, these studies suggest that local adaptation is most likely to occur at 'intermediate' spatial scales-where the definition of 'intermediate' will depend on the balance between gene flow, relative dispersal ability of host and parasite and the strength of natural selection [18].…”