Breeding for resistance to Varroa destructor in North America

Apidologie 41 (2010) 409–424 c INRA/DIB-AGIB/EDP Sciences, 2010  DOI: 10.1051/apido/2010015 Available online at: www.apidologie.org Review article Breeding for resistance to Varroa destructor in North America* Thomas E. Rinderer1 , Jeffrey W. Harris1 , Gregory J. Hunt2 , Lilia I. de Guzman1 1 USDA- Agricultural Research Service, Honey Bee Breeding, Genetics and Physiology Laboratory, 1157 Ben Hur Road, Baton Rouge, LA, 70820, USA 2 Dept. of Entomology, Purdue University, West Lafayette, IN 47907, USA Received 24 September 2009 – Revised 1 January 2010 – Accepted 30 January 2010 Abstract – Breeding for resistance to Varroa destructor in North America provides the long-term solution to the economic troubles the mite brings. This review reports the development of two breeding successes that have produced honey bees of commercial quality that do not require pesticide treatment to control Varroa, highlights other traits that could be combined to increase resistance and examines the potential uses of marker-assisted selection (MAS) for breeding for Varroa resistance. Breeding work continues with these stocks to enhance their commercial utility. This work requires knowledge of the mechanisms of resistance that can be further developed or improved in selected stocks and studied with molecular techniques as a prelude to MAS. Varroa resistance / breeding program / Russian honey bees / Varroa-sensitive hygiene / marker-assisted selection 1. INTRODUCTION The introduction of Varroa destructor Anderson & Trueman (2000) into North America during the late 1980s caused dramatic changes to beekeeping practices and increased the costs of honey production and pollination. Increased costs stemmed primarily from the control measures necessary to prevent loss of colonies from varroosis. Most beer keepers relied on acaricides such as Apistan TM (fluvalinate) or CheckMite (coumaphos) to control Varroa mites. Unfortunately, use of chemicals has led to the development of acaricide-resistant mites and to increased residues of chemicals in beeswax and honey. A variety of non-chemical control methods were developed to circumvent or delay the problems of acaricide-resistant mites and chemical residues in beekeeping products. Corresponding author: T. Rinderer, * Manuscript editor: Marla Spivak Non-chemical controls for Varroa mites included mite trapping by removal of capped drone brood, screened floors, sticky traps on the bottom board, and use of Varroa-resistant honey bees. Using Varroa-resistant honey bees is ideal since the need for acaricides is either reduced or eliminated without a need for additional Varroa control measures. Breeding for Varroa-resistant honey bees became the primary goal for a number of research groups around the world. Within North America, Varroa resistance has been produced by at least three breeding programs. One program from the University of Minnesota produced measurable Varroa resistance as a consequence of selecting for improved general hygienic behavior (Boecking and Spivak, 1999; Spivak and Reuter, 2001a, b; Ibrahim et al., 2007). The “Minnesota Hygienic” stock (MNHYG) is sold commercially throughout the US (Spivak et al., 2009). Two other programs were initiated at the USDA-ARS Honey Bee Breeding, Genetics and Physiology Laboratory in Baton Rouge, LA, and they are the Article published by EDP Sciences 410 T.E. Rinderer et al. primary focus of the current review. The Russian Honey Bee (RHB) Program and the Varroa-Sensitive Hygiene (VSH) Program were initiated specifically to produce Varroa resistant honey bees that would be suitable for commercial use. Although they differ in general breeding approach, the two programs have produced and released Varroa-resistant honey bees that are sold commercially. These honey bees require substantially fewer acaricide treatments for controlling Varroa mites, and they retain the commercial qualities desired by beekeepers. Both programs have relied upon traditional breeding techniques and an understanding of the known mechanisms of Varroa resistance. One goal is that future selection will include the use of molecular genetics. Specifically, the development of marker-assisted selection (MAS) will likely accelerate breeding progress in these two programs and programs that are currently developing other Varroa resistance traits such as nestmate grooming. 2. MECHANISMS OF RESISTANCE The Russian (or Korean) haplotype of V. destructor is the hypervirulent variant which threatens Apis mellifera beekeeping worldwide (de Guzman et al., 1997, 1999; Anderson and Trueman, 2000). Honey bee colonies that survive infestations of this Varroa haplotype have one or more behavioral or physiological traits which underlie their resistance to Varroa. 2.1. Behavioral mechanisms of resistance 2.1.1. Hygienic behavior Hygienic bees are able to detect, uncap and remove diseased brood (Rothenbuhler, 1964; Gilliam et al., 1983; Spivak and Reuter, 2001b). A general test of hygiene, the removal of freeze-killed brood by colonies (Spivak and Reuter, 1998), correlates relatively well with removal of Varroa-infested brood (Boecking and Drescher, 1992; Spivak, 1996). Removal of mite-infested brood is well established in A. cerana (Peng et al., 1987). The ability to remove brood infested with Varroa has been bred to high levels in A. mellifera colonies bred for VSH (Harbo and Harris, 2005; Harris, 2008). VSH is more pronounced in infested worker brood than in drone brood suggesting that increased mite infestation may occur in VSH colonies when drone brood is abundant (Harris, 2008). As VSH bees uncap and remove infested brood, freed adult female mites usually transfer onto the bees removing the brood (Aumeier and Rosenkranz, 2001) but may eventually become free on the combs and exposed to attack by bees. Thakur et al. (1997) documented that honey bees can detect, grab and bite freemoving mites. The mites may also become phoretic and exposed to grooming. Hence, VSH may be a basic mechanism which can enhance other traits such as nestmate grooming and an increased phoretic period (Ibrahim et al., 2007). 2.1.2. Grooming behavior Honey bees clean themselves (autogrooming) and nestmates (allogrooming) (Haydak, 1945). Grooming may injure or kill Varroa mites (Ruttner and Hänel, 1992), or it may cause mites to either move to other parts of the autogroomer’s body, transfer to a new host or be removed from the bee’s body without causing visible injury (Büchler et al., 1992). Grooming is rarely observed directly. However, variation among honey bee stocks in grooming has been inferred from the proportion of mites that drop to hive floors that are damaged, apparently from bees’ mandibles (Boecking and Spivak, 1999; Fries et al., 1996; Rinderer et al., 2001a; Arechavaleta-Velasco and Guzman-Novoa, 2001). In a study in Mexico that compared mite population growth (MPG) in a genetically diverse set of colonies and beginning with equal mite infestations, the principa (...truncated)