ORIGINAL PAPER Individual-level patterns of division of labor in honeybees highlight flexibility in colony-level developmental mechanisms Brian R. Johnson & Elizabeth Frost Received: 4 October 2011 / Revised: 20 February 2012 / Accepted: 28 February 2012 / Published online: 13 March 2012 # Springer-Verlag 2012 Abstract Honeybee division of labor (DOL) has become a model system for exploring the genetic basis of complex traits and phenotypic plasticity. Although many highly in- formative behavioral studies have been conducted on this topic (both at the cohort and individual levels), most studies have focused on a few behavioral acts, such as the age of first foraging. Few studies have recorded large numbers of relatively complete individual-level patterns of DOL. Such fine-scale patterns would lay the foundation for rigorous molecular analyses of this phenomenon and allow us to differentiate between competing mechanistic models of DOL. Here, we record over 100 individual-level DOL pat- terns of bees living under natural conditions. We found that the transitions between castes (polyphenism states) are often gradual, with bees being in multiple castes at once. This is contrary to the traditional view that changes are abrupt. We also found that bees often skip castes, a key prediction of a recent model of DOL. We further confirm variation in the rate at which bees pass through castes and the age of first foraging. Taken together, these results greatly improve our understand- ing of this model system and allow for a strong revision of current models of honeybee DOL. Keywords Honeybees . Social insects . Division of labor . Superorganism . Polyphenism Introduction The honeybee’ s complex system of division of labor (DOL) has long been a model system for many topics in biology (Page and Robinson 1991; Beshers and Fewell 2001; Johnson 2003; Robinson et al. 2008; Fischman et al. 2011). It is a particularly good model for understanding the genetic basis of complex traits and phenotypic plasticity (Ben-Shahar et al. 2002; Grozinger et al. 2003; Rueppell et al. 2004; Whitfield et al. 2006; Oldroyd and Thompson 2007; Smith et al. 2008; John- son and Tsutsui 2011; Fussnecker et al. 2011). This is due to the sophistication of honeybee DOL (in terms of the number of alternative phenotypes) and because of the species amenability of study. Honeybees not only produce multiple phenotypes from the same genetic machinery but they produce these phenotypes in a flexible adaptive manner (Robinson 2002; Johnson 2010a). Essentially, as bees age, they pass through several developmental phases that specialize them for particu- lar sets of tasks (Seeley 1982; Johnson 2008, 2010a). Although the transitions between phases are unidirectional under most conditions, under some circumstances, bees can accelerate or reverse their development to earlier phases (reviewed in Rob- inson 2002; Johnson 2010a). These circumstances, which can be controlled experimentally, have natural counterparts, mak- ing controlled laboratory studies relevant to our understanding of the adaptive basis of the bee’ s system of division of labor in nature. As conserved genetic pathways are thought to control common developmental and behavioral systems across wide evolutionary distances, this work has the potential to shed light on the mechanistic basis of polyphenism, and the intersection between development and behavior, across the arthropods (Stern 2000; Robinson et al. 2008; Carroll 2008; Bell and Robinson 2011). Communicated by O. Rueppell B. R. Johnson (*) : E. Frost Department of Entomology, University of California, Davis, 1 Shields Ave, Davis, CA 95616, USA e-mail: brnjohnson@ucdavis.edu Behav Ecol Sociobiol (2012) 66:923–930 DOI 10.1007/s00265-012-1341-4