Copyedited by: OUP Journal of Economic Entomology, XX(X), 2018, 1–9 doi: 10.1093/jee/toy377 Apiculture & Social Insects Research Colony Size, Rather Than Geographic Origin of Stocks, Predicts Overwintering Success in Honey Bees Downloaded from https://academic.oup.com/jee/advance-article-abstract/doi/10.1093/jee/toy377/5251959 by guest on 11 January 2019 (Hymenoptera: Apidae) in the Northeastern United States Mehmet Ali Döke,1,2,4 Carley M. McGrady,1 Mark Otieno,3 Christina M. Grozinger,1 and Maryann Frazier1 1Department of Entomology, Center for Pollinator Research, Huck Institutes of the Life Sciences, Pennsylvania State University, PA 16801, 2Current Address: Department of Biology, University of Puerto Rico, San Juan, PR, Phone: 814-441-2144, 3Agricultural Resource Management, Embu University College, Nairobi, Embu, Kenya, and 4Corresponding author, e-mail: [email protected] Subject Editor: James Strange Received 4 February 2018; Editorial decision 10 November 2018 Abstract Honey bees (Apis mellifera L.) are key pollinators of agricultural crops. However, approximately 30% of managed colonies die each winter in the United States. There has been great interest in breeding for ‘locally adapted stocks’ which survive winter conditions in a particular region. Here, we evaluate the impact of geographic origin of stock on colony weight, population size, and overwintering survival. Comparing four different U.S. honey bee stocks (two bred in southern and two bred in northern regions) under standard beekeeping practices in three different apiary locations in central Pennsylvania, we examined possible adaptation of these stocks to temperate conditions. We confirmed the genotypic difference among the stocks from different geographic origins via microsatellite analysis. We found that stock or region of origin was not correlated with weight, population size, or overwintering success. However, overwintering success was influenced by the weight and population size the colonies reached prior to winter where higher colony weight is a strong predictor of overwintering survival. Although the number of locations used in this study was limited, the difference in average colony sizes from different locations may be attributable to the abundance and diversity of floral resources near the honey bee colonies. Our results suggest that 1) honey bees may use similar strategies to cope with environmental conditions in both southern and northern regions, 2) colonies must reach a population size threshold to survive adverse conditions (an example of the Allee effect), and 3) landscape nutrition is a key component to colony survival. Key words: overwintering, diapause, nutrition, landscape, behavior In temperate climates, the winter season constitutes a great challenge adaptations can influence the long-term survival and success of for animals due to shortened photoperiod, dwindling resources, and local populations in their habitat (Reznick and Ghalambor 2001). extreme cold. Species inhabiting temperate regions have evolved In the case of honey bees, breeding for ‘locally adapted stocks’ strategies to survive the winter via molecular, physiological, and may significantly improve the survival and productivity of man- behavioral adaptations (van der Werf et al. 2009, Chen et al. 2014). aged honey bee colonies. Previous proteomic analyses of honey bee As a social insect, honey bees have evolved a variety of mechanisms stocks collected from around the world demonstrated significant to survive the winter, including distinct behavioral (decreased indi- differences in expression patterns of metabolic proteins accord- vidual activity, cessation of brood rearing, and formation of a ther- ing to geographic origin, though survival of these populations in moregulatory cluster) and physiological (altered endocrine profiles, a common, temperate environment was not assessed (Parker et al. increased nutrient stores, and longevity) features [reviewed in Döke 2010). Furthermore, a study spanning multiple regions in Europe et al. (2015)]. However, despite these adaptations, winter is still a demonstrated improved overwintering survival of colonies gener- very stressful period for honey bee colonies in temperate regions, ated from local stocks (Büchler et al. 2014, Hatjina et al. 2014). with ~30% average winter colony losses reported by beekeepers in In this 2-yr study, researchers followed colonies from 16 differ- the United States in the last decade (Kulhanek et al. 2017). ent genotypes that were placed in areas from six climatic regions Populations within a species can exhibit local adaptations to around Europe. Adult bee population and overwintering survival biotic and abiotic elements in their environment and these local was greatest when the genotypes were maintained in their home © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. 1 All rights reserved. For permissions, please e-mail: [email protected]. Copyedited by: OUP 2 Journal of Economic Entomology, 2018, Vol. XX, No. XX range. These results demonstrate the existence of locally adapted into non-Russian colonies (Tarpy and Lee 2005), which is why we stocks in Europe. chose to use nucleus colonies for this group; this approach is consist- However, although European honey bees exhibit the clear, ent with standard beekeeping practices. However, since honey bee genetically distinct population structure necessary to create locally workers mature from egg to adult in 3 wk, and adult workers have adapted stocks (Estoup et al. 1995), U.S. honey bee populations a maximum lifespan of 6 wk in the summer (Winston 1987), all are not comparably structured. U.S. honey bee populations exhibit colonies should have consisted of worker offspring of their respec- genetic differences between vastly separated populations of east and tive queens by mid-July. Queens from different sources were marked west coasts (Delaney et al. 2009), but this has not been demonstrated with different colors. Each genetic stock was represented by 14–16 at a smaller geographic scale, or between Northern and Southern colonies that were equally distributed among three apiary sites (60 Downloaded from https://academic.oup.com/jee/advance-article-abstract/doi/10.1093/jee/toy377/5251959 by guest on 11 January 2019 United States. Honey bee colonies and queens are shipped across colonies in total). the United States by migratory beekeepers and commercial breeding We interviewed the queen bee breeders to obtain information operations, which would serve to move alleles between distant loca- on their breeding practices. Breeder South1 (FL) has been using Pol- tions. Although genetic diversity of honey bees in North America line hygienic Italian (a name given to this stock by the commercial was thought to be limited due to bottleneck events created by intro- provider) queens bred for Varroa Sensitive Hygiene (VSH) behavior duction of bees to this continent (Cobey et al. 2012), heavy selection (Danka et al. 2016) with an outcrossing mating system since 2011. by parasitic mites (Kraus and Page 1995), and consolidation of bee Breeder North1 (VT) has been selecting their own stock for local suc- breeders (Schiff and Sheppard 1995; 1996), an analysis of genetic cess (i.e., survival and productivity) which started from VSH queens diversity in managed honey bee colonies in Europe and United States purchased in 2004 with limited and sparse introductions from other demonstrated that managed populations actually have higher levels regional beekeepers’ stocks. Breeder North2 (WV) is a member of of genetic diversity than their progenitor populations, likely due to the Russian Honeybee Breeders Association (RHBA) and has been increased admixture during breeding practices (Harpur et al. 2012). strictly using queens from the Russian stock since 2003. Both the Pol- In the United States, there is only one study in partial support of line and ARS Russian Bee stocks were developed through selective locally adapted stocks (MacGregor-Forbes 2014), but the research- breeding programs at USDA-ARS Honey Bee Breeding, Genetics and ers only used northern bred queens for requeening while maintain- Physiology Laboratory in Baton Rouge, LA (Rinderer et al. 2000; ing other colonies with their original southern bred queens (which Danka et al. 2016). We could not obtain information on breeding were generated from commercial producers of ‘package’ bees rather practices of breeder South2 (TX). We investigated the genetic differ- than queen breeders) as a control. Under these circumstances, the entiation of the honey bee stocks used in this study through micros- observed increase in overwintering survival of the requeened versus atellite analysis (see Microsatellite Genotyping below). nonrequeened colonies can be due to the act of requeening itself, quality differences between the locally bred and package queens, Apiary Sites local adaptations of northern bred queens, or a combination of these Apiaries A (N40° 46′ 11.98″, W77° 40′ 41.84″) and B (N40° 47′ factors. 21.32″, W77° 40′ 49.36″) are located in a nonagricultural area of Here we test the hypothesis that honey bee breeding efforts in ~10 miles away from Pennsylvania State, University Park campus United States have produced locally adapted honey bee stocks with and within 1 mile of each other. Apiary C (N40° 45′ 32.84″, W77° higher overwintering success in climates where they were bred or 54′ 53.72″) is ~15 miles away from the first two, located in a more reduced overwintering