Abstract
AbstractParasitism is expected to select for counter‐adaptations in the host: driving a coevolutionary arms race. However, human interference between honey bees (Apis mellifera) and Varroa mites removes the effect of natural selection and restricts the evolution of host counter‐adaptations. With full‐sibling mating common among Varroa, this can rapidly select for virulent, highly inbred, Varroa populations. We investigated how the evolution of host resistance could affect the infesting population of Varroa mites.We screened a Varroa‐resistant honey bee population near Toulouse, France, for a Varroa resistance trait: the inhibition of Varroa's reproduction in drone pupae. We then genotyped Varroa which had co‐infested a cell using microsatellites. Across all resistant honey bee colonies, Varroa's reproductive success was significantly higher in co‐infested cells but the distribution of Varroa between singly and multiply infested cells was not different from random. While there was a trend for increased reproductive success when Varroa of differing haplotypes co‐infested a cell, this was not significant. This suggests local mate competition, through the presence of another Varroa foundress in a pupal cell, may be enough to help Varroa overcome host resistance traits; with a critical mass of infesting Varroa overwhelming host resistance. However, the fitness trade‐offs associated with preferentially co‐infesting cells may be too high for Varroa to evolve a mechanism to identify already‐infested cells. The increased reproductive success of Varroa when co‐infesting resistant pupal cells may act as a release valve on the selective pressure for the evolution of counter resistance traits: helping to maintain a stable host–parasite relationship.
Highlights
The conflicting fitness optima between hosts and parasites means the evolution of a beneficial adaptation in one is expected to select for a counter-adaptation in the other: driving a co-evolutionary arms race (Bell, 1982)
The Red Queen Hypothesis predicts that a co-evolutionary arms race will drive oscillations in haplotype frequencies in hosts and parasites influenced by the relative frequency and fitness of matching alleles: selecting for increased genetic diversity, recombination, and evolutionary rates
The highly inbred lifestyles of some parasites (Beaurepaire, Krieger, & Moritz, 2017) may make it difficult for a population to evolve when their host develops a new defense. This could be the case for the brood-parasitic mite Varroa destructor, Anderson & Trueman: a devastating parasite of honey bees (Apis mellifera, L.)
Summary
The conflicting fitness optima between hosts and parasites means the evolution of a beneficial adaptation in one is expected to select for a counter-adaptation in the other: driving a co-evolutionary arms race (Bell, 1982). The frequent occurrence of full-sibling mating between Varroa means populations can rapidly become highly inbred, with low proportions of heterozygotes, in the middle of the brood season (June–July in Europe (Calis, Fries, & Ryrie, 1999)) This is when Varroa females are most likely to singly infest a cell and cannot outbreed (Beaurepaire et al, 2017; Fuchs, 1992). Natural selection has resulted in the evolution of a honey bee population with a greatly reduced rate of Varroa population growth (Kefuss et al, 2015) This reduced rate of Varroa population growth has been linked to the inhibition of Varroa's reproduction in pupal cells; the drone brood where Varroa normally produces the most offspring (Conlon et al, 2019; Kefuss et al, 2015; Rosenkranz et al, 2010). Selection for increased recombination, via outbreeding, could increase evolutionary rates in this Varroa population and indicate it is engaged in a co-evolutionary arms race with its host (Beaurepaire, Ellis, Krieger, & Moritz, 2019; Beaurepaire et al, 2017; Bell, 1982; Hamilton et al, 1990)
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