Honey bee (Apis mellifera) intracolonial genetic diversity influences worker nutritional status Bruce J. Eckholm, Ming H. Huang, Kirk E. Anderson, Brendon M. Mott, Gloria Degrandi-Hoffman To cite this version: Bruce J. Eckholm, Ming H. Huang, Kirk E. Anderson, Brendon M. Mott, Gloria Degrandi-Hoffman. Honey bee (Apis mellifera) intracolonial genetic diversity influences worker nutritional status. Api- dologie, Springer Verlag, 2015, 46 (2), pp.150-163. 10.1007/s13592-014-0311-4. hal-01284439 HAL Id: hal-01284439 https://hal.archives-ouvertes.fr/hal-01284439 Submitted on 7 Mar 2016 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2015) 46:150–163 Original article * INRA, DIB and Springer-Verlag France, 2014 DOI: 10.1007/s13592-014-0311-4 Honey bee (Apis mellifera ) intracolonial genetic diversity influences worker nutritional status 1 2 3 3 Bruce J. ECKHOLM , Ming H. HUANG , Kirk E. ANDERSON , Brendon M. MOTT , 3 Gloria DEGRANDI-HOFFMAN 11025 Zylstra Road, Coupeville, WA 98239, USA 2Eurofins Agroscience Services, Inc., 15250 NC Hwy 86 South, Prospect Hill, NC 27314, USA 3Carl Hayden Bee Research Center, USDA-ARS, 2000 East Allen Road, Tucson, AZ 85719, USA Received 9 January 2014 – Revised 10 July 2014 – Accepted 25 July 2014 Abstract – Honey bee queens mate with multiple males resulting in high intracolonial genetic diversity among nestmates; a reproductive strategy known as extreme polyandry. Several studies have demonstrated the adaptive significance of extreme polyandry for overall colony performance and colony growth. Colonies that are more genetically diverse collect more pollen than colonies with less diversity. However, the effects of intracolonial genetic diversity on worker nutritional status are unknown. We created colonies headed by queens instrumentally insem- inated with sperm from either 1 or 20 drones, then compared protein consumption, digestion, and uptake among nestmates. We found that nurse bees from colonies with multiple-drone-inseminated (MDI) queens consumed more pollen, had lower amounts of midgut tissue protease, and invested more protein into larvae than nurse bees from single-drone-inseminated (SDI) queens. Pollen foragers from MDI colonies had significantly higher hemolymph protein concentration than pollen foragers from SDI colonies. Differences in hemolymph protein concentration between nurses and pollen foragers were significantly smaller among MDI colonies than among SDI colonies. While intracolonial genetic diversity is correlated with increased foraging, our results suggest that this relationship may be driven in part by the elevated resource demands of nurse bees in genetically diverse colonies that consume and distribute more protein in response to the social context within the hive. intracolonial genetic diversity / extreme polyandry / honey bee nutrition 1. INTRODUCTION Page 2000; Schlüns et al. 2005). However, ex- treme polyandry appears to offer a selective ad- Multiple mating by honey bee (Apis mellifera ) vantage at the colony level, largely as a conse- queens is a reproductive behavioral trait known as quence of the increased genetic diversity among extreme polyandry. While relatively uncommon, the queen’s offspring (Keller and Reeve 1994; extreme polyandry (i.e., ≥2 mates/queen) has been Oldroyd et al. 1998; Cole and Wiernasz 1999). documented in 13 genera of the Hymenoptera A honey bee queen mates in flight with many (Hughes et al. 2008). There are inherent risks to males (Tarpy et al. 2004) after which she begins to the queen of mating in the open with multiple lay eggs. The majority of fertilized eggs develop males, such as disease transmission (de Miranda into female workers, forming the colony work- and Fries 2008; da Cruz-Landim et al. 2012)or force. Worker offspring sired by any particular simply not returning to the colony (Tarpy and male with whom the queen mated comprise a “patriline” within the colony and, as a conse- quence of the queen’s multiple mates, the colony is comprised of many patrilines. On average, Corresponding author: B. J. Eckholm, workers within any patriline will be more similar [email protected] to each other than to their half-sisters from differ- Handling Editor: David Tarpy ent patrilines (Page and Laidlaw 1988). Genetic Honey bee (Apis mellifera ) intracolonial genetic diversity influences worker nutritional status 151 variability among patrilines contributes to the trophallaxis. Nurse bees consume and digest overall genetic diversity of the colony and is a stored pollen and distribute it as a proteinaceous key factor in colony health and productivity for jelly to all colony members, including the queen, honey bees (Oldroyd et al. 1992b, Fuchs and larvae, drones, and foragers (Crailsheim 1991). Schade, 1994; Mattila and Seeley, 2007)aswell The transition to foraging behavior is accom- as other social Hymenoptera (e.g. Wiernasz et al. panied by reduced pollen consumption 2004, 2008;Goodismanetal.,2007). In particu- (Crailsheim et al. 1992)aswellasreducedlevels lar, colonies comprised of a genetically diverse of total protein in the hemolymph (Fluri et al. workforce show increased disease resistance 1982). To support their high activity levels, for- (Baer and Schmid-Hempel 1999;Palmerand agers consume some pollen directly; however, Oldroyd 2003;Tarpy2003; Hughes and they also receive protein via trophallaxis with Boomsma 2004; Tarpy and Seeley 2006; Seeley nurse bees (Crailsheim 1991). Nutritional and and Tarpy 2007) and also exhibit improved effi- physiological shifts in workers suggest that ciency in their division of labor [reviewed by changes in nutritional status may initiate and reg- Oldroyd and Fewell (2007)]. Robinson and Page ulate foraging behavior (Toth and Robinson (1989) proposed a genetically based response 2005). Mechanisms that modulate the foraging threshold model to explain how colony function population are likely integral to colony fitness. improves with increased intracolonial genetic di- Of note, colonies comprised of multiple versity. The model predicts that workers have patrilines are often associated with robust foraging genetically based internal thresholds for populations [reviewed by Mattila and Seeley responding to task stimuli and patrilineal variation (2014)]. Among honey bees, patriline-based differ- in these internal thresholds generates division of ences have been shown to influence a number of labor. In support of the response threshold model, foraging-related activities including type of forage patriline-based differences in behavior have been (Oldroyd et al. 1992a), foraging distance (Oldroyd widely reported for honey bees such as guarding et al. 1993), foraging time of day (Kraus et al. (Giray et al. 2000), nest thermoregulation (Jones 2011), scouting (Dreller 1998; Mattila and Seeley et al. 2004), feeding larvae (Chapman et al. 2007), 2011), and dance communication (Mattila and grooming (Frumhoff and Baker 1988), and corpse Seeley 2010). Variation in behavioral states within removal (Robinson and Page 1988). a multiple patriline colony thus enhances the overall Division of labor, whereby workers specialize foraging effort. Indeed, when compared to honey on subsets of colony tasks (Oster and Wilson bee colonies with reduced intracolonial genetic di- 1978), emerges in part from age-related task versity, honey bee colonies with greater partitioning; young adult workers handle in-hive intracolonial genetic diversity are more efficient at tasks such as comb building and brood care (i.e., pollen foraging, resulting in greater amounts of “nursing”), and older workers perform peripheral pollen collected and increased brood production tasks such as guarding and foraging (Winston (Mattila and Seeley 2007; Eckholm et al. 2011). 1987). Moreover, the network of repeated interac- Large amounts of protein are provided to larvae tions between workers of various genetic and by nurse bees (Crailsheim 1990). Nurse bees in- phenotypic dispositions modulates task crease the feeding frequency and feeding duration partitioning (Robinson 1992). Worker interactions of young larvae when stored pollen is available, provide a mechanism for all individuals to assess resulting in higher larval protein content the needs of the colony, primarily determined by (Schmickl and Crailsheim 2002). Pollen foraging the colony’s food supply (Ribbands 1952). Troph- success therefore directly affects colony growth. allaxis, the transfer of food from one worker to However, we speculated that the ability to convert another, serves as a primary mechanism for the inbound food resources to colony growth may assessment of colony state and allocation of nutri- be—like foraging effort—augmented by tion resources (Crailsheim 1998). As the primary intracolonial genetic diversity. To that end, we digesters and distributors of protein in a honey bee established colonies headed by queens instrumen- colony, nurse bees play a central role in tally inseminated with either multiple (n =20) or 152 B.J. Eckholm et al. single (n =1) drones to construct two treatments locations