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Research Article

Effects of Selection for Honey Bee Worker Reproduction on Foraging Traits

  • Benjamin P Oldroyd mail,

    To whom correspondence should be addressed. E-mail: boldroyd@bio.usyd.edu.au

    Affiliation: Behaviour and Genetics of Social Insects Laboratory, School of Biological Sciences A12, University of Sydney, New South Wales, Australia

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  • Madeleine Beekman

    Affiliation: Behaviour and Genetics of Social Insects Laboratory, School of Biological Sciences A12, University of Sydney, New South Wales, Australia

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  • Published: March 04, 2008
  • DOI: 10.1371/journal.pbio.0060056

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Oldroyd and Beekman do not test ground plan hypothesis that explains origins of social behavior

Posted by plosbiology on 07 May 2009 at 22:24 GMT

Author: Gro V. Amdam
Position: Associate Professor
Institution: School of Life Sciences, Arizona State University, USA
E-mail: Gro.Amdam@asu.edu
Additional Authors: Robert E. Page, Jr
Submitted Date: April 25, 2008
Published Date: April 30, 2008
This comment was originally posted as a “Reader Response” on the publication date indicated above. All Reader Responses are now available as comments.

Oldroyd and Beekman claim to test the forager reproductive ground plan hypothesis (forager RGPH) of Amdam et al. (2004, 2006) using a selected strain of anarchistic bees. The authors conclude that the forager RGPH is not supported, and criticize studies in support of the hypothesis that used strains selected for high and low levels of pollen hoarding.

The forager RGPH proposes that variation among worker honey bees in age at foraging onset and bias toward collecting pollen or nectar is partly explained by variation in a gene network that can synchronize foraging choice and provisioning behavior with ovarian physiology. This pleiotropic regulatory network and its link to foraging behavior in workers are derived from the reproductive biology of ancestral solitary insects.

Support for the forager RGPH comes from association studies using wild type bees and strains selected for high or low levels of pollen hoarding, from genome mapping studies, and from RNA interference gene knockdown experiments in wild type (reviewed by Page & Amdam 2007). This work shows that sucrose responsiveness, foraging onset, foraging preference for nectar or pollen, ovary size (ovariole filament number) and vitellogenin (yolk) protein levels are linked traits in workers, and suggests that pleiotropy emerges through a reproductive endocrine network similar to systems that coordinate sensory responses and feeding behavior with female reproductive traits in many taxa (Klowden 1990; Than et al. 1994).

The study of Oldroyd and Beekman is flawed:

1. The characterization of our work as derived from selected strains is distorted. Wild type bees were used repeatedly to verify our findings (see Page & Amdam 2007).

2. The anarchistic bees of Oldroyd and Beekman represent a rare behavioral mutation perhaps involving as few as 2 genes, and their reproductive behavior is different from the behavior of wild type (Oldroyd et al. 1999; Barron et al. 2001; Thompson et al. 2006). Thus, previous work by Oldroyd and colleagues suggests that the anarchistic syndrome is not a useful test of the forager RGPH.

3. The anarchistic bees and wild type of Oldroyd and Beekman have unusually small ovaries (about 2 ovarioles per ovary). A larger average ovariole number is needed to evaluate covariance between ovary size and foraging behavior*.

4. Oldroyd and Beekman excluded subsets of bees that collected only pollen or only nectar in all analyses of foraging behavior, resulting in insufficient sample sizes*.

Thus, by comparing cropped data from mutants with abnormal behavior to wild type with compressed ovary size, Oldroyd and Beekman fail to support the forager RGPH. Yet they do not test the hypothesis. They demonstrate the pitfalls of making conclusions based on insufficient analyses of data derived from poorly chosen genetic stocks.

*See “Reply” PDF at www.amdamlab.asu.edu for data and details.

Amdam GV, et al. 2006 Complex social behavior derived from maternal reproductive traits. Nature 439, 76-78

Amdam GV, et al. 2004 Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc Natl Acad Sci USA 101, 11350-11355

Barron AB, et al. 2001 Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review. Behav Ecol Sociobiol 50, 199-208

Klowden M J 1990 The endogenous regulation of mosquito reproductive behavior. Experientia 46, 660-670

Oldroyd BP, Osborne KE 1999 The evolution of worker sterility in honeybees: the genetic basis of failure of worker policing. Proc R Soc Lond 266, 1335-1339

Page RE, Amdam GV 2007 The making of a social insect: developmental architectures of social design. BioEssays 29, 334-343

Than TT, et al. 1994 Sucrose threshold variation during the menstrual cycle. Physiol Behav 56, 237-9

Thompson GJ, et al. 2006 Towards a molecular definition of worker sterility: differential gene expression and reproductive plasticity in honey bees. Insect Mol Biol 15, 637-44

No competing interests declared.