Characterization of Quantitative Trait Loci for the Age of First Foraging in Honey Bee Workers
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Identifying the basis of quantitative trait loci (QTL) remains challenging for the study of complex traits, such as behavior. The honey bee is a good model combining interesting social behavior with a high recombination rate that facilitates this identification. Several studies have focused on the pollen hoarding syndrome, identifying multiple QTL as the genetic basis of its behavioral components. One component, the age of first foraging, is central for colony organization and four QTL were previously described without identification of their genomic location. Enabled by the honey bee genome project, this study provides data from multiple experiments to scrutinize these QTL, including individual and pooled SNP mapping, sequencing of AFLP markers, and microsatellite genotyping. The combined evidence confirms and localizes two of the previous QTL on chromosome four and five, dismisses the other two, and suggests one novel genomic region on chromosome eleven to influence the age of first foraging. Among the positional candidates the Ank2, PKC, Erk7, and amontillado genes stand out due to corroborating functional evidence. This study thus demonstrates the power of combined, genome-based approaches to enable targeted studies of a manageable set of candidate genes for natural behavioral variation in the important, complex social trait “age of first foraging”.
KeywordsGenetic architecture Complex traits Social insects Life history Division of labor Behavioral ontogeny AFLP Foraging onset
I would like to thank Robert Page (ASU) for breeding and providing the original mapping populations, as well as allowing me to use the software MapQTL, Charlie Whitfield (UIUC) for practical assistance with the pooled SNP genotyping and providing his raw data to enable my analyses, and Greg Hunt (Purdue), Michael Munday (UNCG) and Patrick Nolan (UNCG) for advice and help regarding the analysis of candidate genes. Two careful reviewers significantly improved the quality of this manuscript. Practical help was provided by Kim Fondrk (UCD) and Meredith Humphries (UCD) with cloning the AFLP fragments, and Jackie Metheny (UNCG) and Emily Meznar (UNCG) with microsatellite genotyping. Financial support was provided by NSF (#0615502) and NIH (NIA PO1 AG22500).
- Beye M, Gattermeier I, Hasselmann M, Gempe T, Schioett M, Baines JF, Schlipalius D, Mougel F, Emore C, Rueppell O, Sirvio A, Guzman-Novoa E, Hunt G, Solignac M, Page RE (2006) Exceptionally high levels of recombination across the honey bee genome. Genome Res 16:1339–1344. doi: 10.1101/gr.5680406 PubMedCrossRefGoogle Scholar
- Homyk T, Sheppard DE (1977) Behavioral mutants of Drosophila melanogaster. 1. Isolation and mapping of mutations which decrease flight ability. Genetics 87(9):5–104Google Scholar
- Hoogendoorn B, Norton N, Kirov G, Williams N, Hamshere ML, Spurlock G, Austin J, Stephens MK, Buckland PR, Owen MJ, O’Donovan MC (2000) Cheap, accurate and rapid allele frequency estimation of single nucleotide polymorphisms by primer extension and DHPLC in DNA pools. Hum Genet 107:488–493. doi: 10.1007/s004390000397 PubMedCrossRefGoogle Scholar
- Hunt GJ, Amdam GV, Schlipalius D, Emore C, Sardesai N, Williams CE, Rueppell O, Guzman-Novoa E, Arechavaleta-Velasco M, Chandra S, Fondrk MK, Beye M, Page RE Jr (2007) Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94:247–267. doi: 10.1007/s00114-006-0183-1 PubMedCrossRefGoogle Scholar
- Lincoln SE, Daly MJ, Lander ES (1993) Constructing genetic linkage maps with MAPMAKER/EXP version 3.0: a tutorial and reference manual. In: A whitehead institute for biomedical research technical report, Cambridge, MAGoogle Scholar
- Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL 4.0, software for the calculation of QTL positions on genetic maps. Plant Research International, Wageningen, The NetherlandsGoogle Scholar
- Wang Y, Amdam GV, Rueppell O, Wallrichs M, Fondrk MK, Kaftanoglu O, Page RE Jr (2009) PDK1 and HR46 gene homologs tie social behavior to ovary signals. PLoS ONE 4:e4899. doi: 10.1371/journal.pone.0004899