Insect Molecular Biology (2000) 9(6), 625–634
© 2000 Blackwell Science Ltd 625
Blackwell Science, Ltd
Sperm-mediated transformation of the honey bee,
Apis mellifera
K. O. Robinson,
1
H. J. Ferguson,
2,
* S. Cobey,
2
H. Vaessin
3
and B. H. Smith
2
1
Molecular, Cellular, and Developmental Biology Program,
The Ohio State University, Columbus, OH 43210,
2
Department of Entomology, The Ohio State University,
Columbus, OH 43210,
3
Department of Molecular
Genetics and Neurobiotechnology Center, The Ohio State
University, Columbus, OH 43210, USA
Abstract
Our primary objective was to identify techniques to
transform the genome of the honey bee ( Apis mellifera )
with foreign DNA constructs. The strategy we adopted
was to linearize foreign DNA and introduce it with sperm
during the instrumental insemination of virgin queen
honey bees. We analysed extracts from larvae within the
same cohort and isolated the predicted fragment by
means of PCR amplification of genomic DNA. Larvae that
carried the construct also expressed the introduced
DNA. We propagated several transgenic lines for up to
three generations, which demonstrates its heritability.
Once carried by a queen, the construct can be detected
in that queen’s larvae over several months. However,
there was no evidence of integration of the construct,
at least as determined by genomic Southern analysis.
Nevertheless, this demonstrates the general viability
of the technique for introduction of DNA, and it should
be augmented by further use of transposable elements
that enhance integration.
Keywords: honey bee, sperm, transformation, GFP.
Introduction
The ability to manipulate an animal’s genome through trans-
genic approaches is crucial for understanding the relationship
between genes and behaviour (Miklos, 1993; Dubnau & Tully,
1998). However, appropriate sets of techniques have not
yet been fully developed for a wide array of organisms. Yet
there are compelling reasons to develop methods for the
transformation of animals such as the honey bee (Robinson
et al. , 1997). Honey bees have a rich history as an experi-
mental organism for basic research in social behaviour
(Seeley, 1995), neuroethology (Menzel, 1990), and beha-
vioural genetics (Page & Robinson, 1991; Page et al. , 1998).
They exhibit complex social interactions, including, among
other behaviours, dance communication to indicate food
resources (von Frisch, 1967), hormonally based behavioural
castes of worker bees (Robinson et al. , 1997), and well
developed learning capabilities (Menzel, 1990). Quantitative
genetic analyses have shown that behaviours such as pollen
and nectar collection (Robinson & Page, 1989), colony
guarding (Page & Robinson, 1991), colony hygienic behaviour
(Robinson & Page, 1988), and learning (Brandes, 1988;
Brandes et al. , 1988; Brandes & Menzel, 1990; Bhagavan
et al. , 1994; Benatar et al. , 1995; Chandra et al ., 2000) all
have heritable components that influence the behaviour of
individual worker bees. From an economic standpoint, the
demands of increased crop production, coupled with stresses
of disease and pest infestation, have increased the potential
value of directly transforming the honey bee genome
(Rothenbuhler, 1979).
The standard technique for the introduction of plasmid
DNA into an organism involves microinjection into an early
stage pronucleus (mice; Palmiter & Brinster, 1986), into a
one- to two-cell developmental stage (zebrafish; Fadool et al. ,
1998), or into early stage embryos in eggs (fruit flies; Rubin
& Spradling, 1982). Initial efforts to transform honey bee
eggs with plasmid DNA by means of microinjection or
liposome-mediated transfer (Bachiller et al. , 1991) revealed
evidence of transient expression (H.J. Ferguson, unpub-
lished data). However, even if these techniques were
perfected, investigators would still be faced with the difficult
task of rearing manipulated honey bee embryos into adults,
given the high rejection rate that workers show toward
manipulated embryos. For honey bees these techniques
require manipulation of embryos in ways that may limit their
reintroduction into the colony. This arises because social
insects progressively feed and/or care for embryos and
Received 10 May 2000; accepted 16 August 2000. Correspondence: Prof.
B. H. Smith, Department of Entomology, 1735 Neil Ave., The Ohio State
University, Columbus, OH 43210–1220, USA. Tel.: (614) 292 0465; fax: (614)
292 5237; e-mail: smith.210@osu.edu *Present address: USDA-ARS, 5230
Konnowac Pass Road, Wapato, WA 98951, USA.