Genetic architecture of ovary size and asymmetry in European honeybee workers

Abstract

The molecular basis of complex traits is increasingly understood but a remaining challenge is to identify their co-regulation and inter-dependence. Pollen hoarding in honey bees is a complex trait associated with a well-characterized suite of linked behavioral and physiological traits. In European honey bee stocks bi-directionally selected for pollen hoarding, worker (sterile helper) ovary size is pleiotropically affected by quantitative trait loci that were initially identified for their effect on foraging behavior. To gain a better understanding of the genetic architecture of worker ovary size in this model system, we analyzed a series of crosses between the selected strains. The crossing results were heterogeneous and suggested non-additive effects. Three significant and three suggestive quantitative trait loci of relatively large effect sizes were found in two reciprocal backcrosses. These loci are not located in genome regions of known effects on foraging behavior but contain several interesting candidate genes that may specifically affect worker ovary size. Thus, the genetic architecture of this life history syndrome may be comprised of pleiotropic, central regulators that influence several linked traits and other genetic factors that may be downstream and trait specific.

Queen mandibular pheromone modulates hemolymph ecdysteroid titers in adult Apis mellifera workers

“…Ovariole number is determined in larval honey bees by multiple genotypic, nutritional, and hormonal factors (Evans and Wheeler 1999;Schmidt Capella and Hartfelder 2002;Rueppell et al 2011;and many others). There is a reported positive association between worker ovariole number and tendency to show signs of morphological activation of the ovaries Amdam et al 2006;Tsuruda et al 2008;Traynor et al 2014).…”

“…Samples contaminated with fat body or gut contents were discarded, and clear samples were dispensed into siliconized microcentrifuge tubes (Thermo Fisher Scientific, Waltham, MA, USA) containing 100 μL of HPLC-grade methanol (Sigma-Aldrich, St. Louis, MO, USA) and stored at − 40°C to permit multiple samples to be analyzed in the same assay run. To determine ovarian status, whole ovaries were removed and rinsed with saline, suspended in 2-3 mL of saline, then assessed using a 5-point scale (Pernal and Currie 2000), in which 0 indicates ovarioles with no signs of swelling, 4 indicates queen-like ovarioles with elongated ooyctes, and intermediate scores are assigned based on degree of swelling and presence of constrictions between follicles, following standard methods (Rueppell et al 2011). Both ovaries were inspected, and a score was given based on the most advanced development observed.…”

“…Worker ovaries typically contain fewer than a dozen ovarioles (Snodgrass 1956;Winston 1987), and individual differences in number of ovarioles, including differences between the right and left ovaries, is commonly observed (Rueppell et al 2011). The number of ovarioles present at eclosion is established during larval life through an interaction of genetic, nutritional, and hormonal factors (Schmidt Capella and Hartfelder 1998;Rueppell et al 2011). If the ovaries are the primary source of ecdysteroids in adult workers (Amdam et al 2010), a simple hypothesis is that workers with larger ovaries will have higher ecdysteroid titers.…”

The architecture of the pollen hoarding syndrome in honey bees: implications for understanding social evolution, behavioral syndromes, and selective breeding

“…Most importantly for the reproductive ground plan hypothesis, ovary size of worker honey bees was affected by pln2, pln3 (Wang, Amdam et al, 2009), and pln4 (Ihle, Rueppell et al, in preparation), and hormonal dynamics were affected by pln3 (Ihle, Rueppell et al, in preparation). In all instances, mapping studies of these other traits have revealed additional QTL that usually exceeded the pleiotropic effects of the pln QTL in the specific crosses of the high and low pollen hoarding strains: Three additional QTL for the age of first foraging were identified (Rueppell, Pankiw et al, 2004; Rueppell, 2009), one for sucrose responsiveness (Rueppell, Chandra et al, 2006), and three for worker ovary size (Rueppell, Metheny et al, 2011). One QTL for the age of first foraging ( aff2 ) also showed an effect on worker ovary size and two worker ovary size QTL showed effects on hormonal dynamics (Ihle, Rueppell et al, in preparation).…”

QTL-mapping of individual resistance against American foulbrood in haploid honeybee drone larvae (Apis mellifera)

“…Nevertheless, to date QTL in honeybees have been primarily identified for worker specific traits including guarding (Arechavaleta-Velasco and Hunt 2004), stinging (Hunt et al 1998;Guzmán-Novoa et al 2002), foraging (Hunt et al 1995;Page et al 2000, Rüppell et al 2004, hygienic behaviour (Oxley et al 2010), worker-ovary size (Linksvayer et al 2009;Rueppell et al 2011;Graham et al 2011), reproductive traits (Lattorff et al 2007;Oxley et al 2008), larval chalkbrood resistance (Holloway et al 2012) as well as body composition and venom compounds (Mougel et al 2012). We are aware of only three exceptions in which haploid drones have been used, which are on learning behaviour (Chandra et al 2001), sucrose responsiveness (Rueppell et al 2006) and larval Varroa tolerance (Behrens et al 2011).…”