A Meta‐Analysis of Factors Affecting Local Adaptation between Interacting Species

Abstract

Adaptive divergence among populations can result in local adaptation, whereby genotypes in native environments exhibit greater fitness than genotypes in novel environments. A body of theory has developed that predicts how different species traits, such as rates of gene flow and generation times, influence local adaptation in coevolutionary species interactions. We used a meta-analysis of local-adaptation studies across a broad range of host-parasite interactions to evaluate predictions about the effect of species traits on local adaptation. We also evaluated how experimental design influences the outcome of local adaptation experiments. In reciprocally designed experiments, the relative gene flow rate of hosts versus parasites was the strongest predictor of local adaptation, with significant parasite local adaptation only in the studies in which parasites had greater gene flow rates than their hosts. When nonreciprocal studies were included in analyses, species traits did not explain significant variation in local adaptation, although the overall level of local adaptation observed was lower in the nonreciprocal than in the reciprocal studies. This formal meta-analysis across a diversity of host-parasite systems lends insight into the role of both biology (species traits) and biologists (experimental design) in detecting local adaptation in coevolving species interactions.

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

“…Many previous studies of host-parasite interactions have not been designed in a way that allows clear insights into local adaptation and co-evolution (Hoeksema and Forde, 2008). In an effort to reduce a number of these limitations, we tracked separate measures of parasite and host fitness in a fully reciprocal cross-infection design conducted in stream mesocosms using four …”

“…Of course, cause and effect could be reversed here in that Marianne River Gyrodactylus do not have to evolve high infectivity because their hosts show such low resistance. Regardless of the specific reasons, these results should be taken as another challenge to the established paradigm that parasites generally are ahead in the ''arms race'' with hosts (Hoeksema and Forde, 2008).…”

“…It may be conceivable that very high virulence in Gyrodactylus might be maladaptive if it increases host mortality in such way that the basic Gyrodactylus reproductive rate is reduced (Dybdahl and Storfer, 2003;Alizon et al, 2008). In this way, lower virulence in Gyrodactylus could evolve in response of the lower resistance of their guppy host (Altizer, 2001;Sternberg et al, 2013) -although the opposite effect has also been reported (Hoeksema and Forde, 2008). Some evidence for this exists in our study in that the least resistant hosts (Marianne River HP and LP) also had the parasites with the lowest performance.…”

“…Parasites are generally considered to be ahead in this arms race due to their shorter generation times which should increase their evolutionary speed (see Lively, 1999;Gandon and Michalakis, 2002;Greischar and Koskella, 2007;Hoeksema and Forde, 2008), and because hosts are usually exposed to many parasite species which makes adaptation to any one species more difficult (Kawecki and Ebert, 2004). 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).…”

“…Our design allowed us to circumvent methodological limitations (Hoeksema and Forde, 2008) by (i) generating separate measures of parasite and host fitness, (ii) conducting experiments in reasonably natural (mesocosm) environments, and (iii) conducting a full reciprocal cross-infection experiment with four Gyrodactylus-guppy populations to disentangle local adaptation from effects of host-parasite co-evolution. We specifically tested whether parasites or hosts showed evidence of local adaptation (higher performance of parasites with sympatric than with allopatric hosts, or higher performance of hosts with sympatric than with allopatric parasites), and whether any local maladaptation was related to drainage of origin (evolutionary lineage) or predation regime (ecological differences).…”