Host adaptations reduce the reproductive success ofVarroa destructorin two distinct European honey bee populations

Abstract

Honey bee societies (Apis mellifera), the ectoparasitic mite Varroa destructor, and honey bee viruses that are vectored by the mite, form a complex system of host–parasite interactions. Coevolution by natural selection in this system has been hindered for European honey bee hosts since apicultural practices remove the mite and consequently the selective pressures required for such a process. An increasing mite population means increasing transmission opportunities for viruses that can quickly develop into severe infections, killing a bee colony. Remarkably, a few subpopulations in Europe have survived mite infestation for extended periods of over 10 years without management by beekeepers and offer the possibility to study their natural host–parasite coevolution. Our study shows that two of these “natural” honey bee populations, in Avignon, France and Gotland, Sweden, have in fact evolved resistant traits that reduce the fitness of the mite (measured as the reproductive success), thereby reducing the parasitic load within the colony to evade the development of overt viral infections. Mite reproductive success was reduced by about 30% in both populations. Detailed examinations of mite reproductive parameters suggest these geographically and genetically distinct populations favor different mechanisms of resistance, even though they have experienced similar selection pressures of mite infestation. Compared to unrelated control colonies in the same location, mites in the Avignon population had high levels of infertility while in Gotland there was a higher proportions of mites that delayed initiation of egg-laying. Possible explanations for the observed rapid coevolution are discussed.

Resistance rather than tolerance explains survival of savannah honeybees (Apis mellifera scutellata) to infestation by the parasitic mite Varroa destructor

“…Cells containing one foundress were considered in determining Varroa reproductive success. Reproductive success was defined by the simultaneous presence of one live mature daughter and one live adult male in a cell (Locke et al 2012).…”

“…The percentage of deformed workers infested with 0, 1 and 2-3 foundresses, was 0.3, 2.4, and 13.3%, respectively. Number of offspring produced (mean ± SD) 2.0 ± 1.2 2.4 ± 1.2 Average number (± SD) of mated daughters (reproductive success) per cell 0.1 ± 0.4 0.4 ± 0.7 Locke et al 2012 Methodology can differ between the studies cited. The number of offspring observed may be slightly overestimated compared to our results since mortality could have occurred, had the honeybee been allowed to emerge.…”

“…Infertility or low reproductive success of the parasite could indicate host resistance (Rosenkranz and Engels, 1994;Rosenkranz, 1999;Locke and Fries, 2011;Locke et al 2012). The proximate mechanism leading to low population growth can be the frequent occurrence of unmated daughter mites that enter brood cells even though they cannot reproduce (Martin et al 1997).…”

“…Reasons for the absence of males have been attributed to males either being killed by the pupae during development, or as a result of not being able to find the feeding site made by the foundress (Donzé et al 1996) Another factor to consider is the importance of host signals used by Varroa mites for oogenesis activation (Garrido and Rosenkranz, 2004). It is possible that larval signals of certain honeybee populations prevent (Milani et al 2004) or delay the initiation of the reproductive cycle of the mites, therefore resulting in a decrease in reproductive success (Locke et al 2012).…”

Selecting honeybees for worker brood that reduces the reproduction of Varroa destructor

“…Some cases suggest a heritable factor present in the brood of the host that may decrease reproduction of V. destructor . These cases include presumably unselected Africanized bees in Brazil through the 1980s and 1990s (Camazine 1986; Rosenkranz and Engels 1994) (but not since then: Garrido et al 2003), naturally selected European bees in Tunisia (Ritter 1990), Uruguay (Ruttner and Marx 1984), Argentina (Eguaras et al 1995), Sweden (Locke and Fries 2011), and France (Locke et al 2012), and bees artificially selected for decreased fertility of mites (Harbo and Hoopingarner 1997) or for lower growth of mite populations in colonies .…”