Current Biology Vol 24 No 10
R382
B 10
A
2.2 s
0s
5.2 s
2 cm
7.3 s
8.5 s
10.9 s
7
6
5
4
3
2
1
0
D7
5
4
3
2
0
*
***
***
1
0
5
10
15
Right Forelimb Reaches
6
5
5
4
3
2
20
0
5
10
15
Right Forelimb Steps
20
20
10
15
5
Preferred Forelimb Reaches
4
3
2
1
**
0
0
7
6
1
* **
**
E
Number of Locusts
*P<0.05; **P<0.01; ***P<0.005
6
Number of Locusts
Despite evidence of asymmetries in
insect sensory perception and motor
control, there is no direct evidence
for functional left–right asymmetry in
their limb control — handedness —
equivalent to that of vertebrates such
as humans (reviewed in [1,2]). Here,
we show that locusts are biased in the
forelimb they use to reach across a
gap in the substrate upon which they
are walking. The strength of this bias
differed among individuals, as did
the forelimb, some locusts favouring
their right forelimb more often, others
their left. In contrast, the locusts’
forelimb movements immediately prior
to reaching, or whilst walking, were
unbiased. This pattern was repeated
when the gap was replaced with a
glass platform; forelimb use was
unbiased when stepping onto the glass
surface but biased when stepping onto
the other side. Thus, locusts show
handedness during targeted forelimb
placement, but not whilst walking, the
switch initiated by visual inputs. This
handedness is context-dependent and
is expressed by individuals rather than
at the population level.
Desert locusts (Schistocerca gregaria)
placed at one end of a horizontal
platform in a white arena walked along
the platform until they encountered a
gap (Figure S1A,B in the Supplemental
Information). Locusts crossed the gap
to the platform on the far side in 82%
(580/707) of trials, the remaining trials
being refusals. Typically, during gapcrossing locusts placed one or both
forelimbs into the gap before replacing
them on the platform edge. They then
reached with one forelimb towards the
opposite platform (Figure 1A). Once
they made contact with one forelimb,
the locusts stepped across the gap with
the opposite forelimb and crossed.
Each locust (N = 29) performed 20
such gap-crossings, during which they
could reach across the gap using either
forelimb. We found that individuals
varied in the strength of their bias;
some showing a strong bias towards a
C7
Number of Locusts
Adrian T.A. Bell1
and Jeremy E. Niven1
Expected Frequency
Observed Frequency
9
8
Number of Locusts
Individual-level,
context-dependent
handedness in the
desert locust
0
* *
0
5
10
15
20
Right Forelimb Steps
25
30
Current Biology
Figure 1. Handedness in targeted forelimb movements during gap-crossing in the locust.
(A) A video sequence showing a gregarious locust crossing a gap. (B) The frequency distribution of gap crosses initiated by the preferred forelimb (N = 29, n = 20; red). The binomial
expectation of no preferred forelimb (p = 0.5; blue) was obtained by mirroring the binomial
distribution to incorporate both left and right forelimb use. (C–E) Frequency distributions of
movements initiated by the right forelimb (red) compared with the expected binomial distribution (p = 0.5; blue). Asterisks indicate significant deviations from the binomial distribution
determined by exact binomial tests. (C) Gap crosses (N = 29, n = 20). (D) Steps into the gap
(N = 29, n = 20). (E) Steps initiating walking on the platform (N = 29, n = 30). See also Figure S1
and Table S1 in the Supplemental Information.
particular forelimb (for example, 90% of
trials), others a weak bias or none at all.
Were locusts unbiased, observations of
their forelimb use should approximate
a binomial distribution. Instead, the
distribution we observed deviated
significantly from the binomial
expectation (G-test, Gadj = 19.73,
3df, p < 0.001, N = 29; Figure 1B; see
Supplemental Experimental Procedures)
with many individuals showing a strong
bias for one forelimb. Individual locusts
differed significantly in the strength and
direction of their bias (G-test, GT = 95.2,
28df, p < 0.001, N = 29), suggesting
there was no consistent bias towards a
particular limb among the population.
Indeed, the population contained
individuals that were significantly
biased towards either their left or right
forelimb (exact binomial tests, Table S1;
Figure 1C).
To determine whether biased forelimb
use was restricted to gap-crossing, we
assessed the forelimb placed into the
gap immediately prior to reaching in the
same cohort of locusts. On this step
the distribution of forelimb use did not
differ from the binomial expectation (Gtest, Gadj = 2.54, 3df, p > 0.05, N = 29),
showing it was unbiased (Figure 1D).
The forelimb an individual placed into
the gap did not significantly influence
the forelimb subsequently used to reach
across the gap (Table S2), consistent
with a switch from unbiased to biased
forelimb use. We also assessed the
first step that initiated walking on
the platform in a second cohort of
locusts. We found that the distribution
of forelimb use on this step did not
differ from the binomial expectation
(G-test, Gadj = 4.14, 3df, p > 0.05, N =
29) showing it too was unbiased (Figure
1E). Thus, the bias in locusts’ forelimb
use was restricted to reaching during
gap-crossing.
The bias in forelimb use may be
triggered by detecting the gap visually
[3] or by placing a forelimb into it.
We used a third cohort of locusts to
distinguish these possibilities. The gap
was bridged with a transparent glass
slide, retaining the visual impression
without the actual gap itself (Figure
S1C). Typically, locusts paused upon
encountering the gap before walking
across the bridge, slowing or pausing
again before stepping onto the far
platform. We found the distribution of
the forelimb placed first onto the glass
slide did not differ from the binomial
expectation (G-test, Gadj = 4.69, 3df,
p > 0.05, N = 30), suggesting the
locusts were unbiased on this step
(Figure S1D). However, the distribution
of the forelimb used to step from the
glass slide onto the opposite platform
differed significantly from the binomial
expectation (G-test, Gadj = 8.90,
Magazine
R383
2df, p < 0.02, N = 30; Figure S1E).
Consistent with this, individual locusts
differed significantly in the strength
and direction of their bias on this step
(G-test, GT = 79.29, 29df, p < 0.001,
N = 30). Moreover, the forelimb an
individual placed onto the glass did
not significantly influence the forelimb
subsequently used to step off (Table
S2), again consistent with a switch from
unbiased to biased. Thus, forelimb
movements are unbiased when the
locusts step onto the bridge but are
biased when stepping off it, suggesting
that visual perception of the gap and/or
step influences the switch.
Our experiments demonstrate
that individual locusts are handed,
manifested as a bias in the forelimb
they use for particular tasks.
Arthropods are known to possess
perceptual and motor asymmetries
[2], but previous studies have either
inferred asymmetrical limb use from
circumstantial evidence [4,5], focussed
on asymmetrical limb use determined
by morphological asymmetry [6], or
reported biased forelimb use from
single behavioural observations [7].
Thus, to our knowledge this is the first
direct evidence an insect, or indeed any
arthropod, possesses individual-level
handedness in the use of otherwise
symmetrical limbs. The contextdependency of the locusts’ handedness
is reminiscent of handedness in
vertebrates, including humans, which
may be absent in some movements (for
example, walking) but pronounced in
others (for example, reaching) [1].
The mechanistic basis of the
locusts’ handedness is unknown but
is likely be the product of biases that
arise through experience rather than
hard-wired neural asymmetry, though
there is evidence that insect brains
can contain structural asymmetries
[8]. With no particular right or left
forelimb bias, and variation in the
strength of the bias, there was
no evidence for population-level
handedness. Theory predicts that
animals living in groups, such as
gregarious locusts, should possess
population-level lateralisation of
some behaviours [1,9]. However,
there is no conflict between this
theory and our results because not
all behaviours need be lateralised.
Handedness may be advantageous to
locusts by reducing the computations
involved in forelimb selection for
targeted movements [10], though
this does not explain the weak
handedness of some locusts.
Nevertheless, our results demonstrate
that the relatively small nervous
systems of insects are capable of
producing functional asymmetry in
forelimb movements.
Supplemental Information
Supplemental Information includes
experimental procedures, one figure and two
tables and can be found with this article online
at http://dx.doi.org/10.1016/j.cub.2014.03.064.
Acknowledgements
We would like to thank Mike Land and Tom
Collett for comments on an earlier version of
the manuscript, Jörn Scharlemann for help
with statistical analyses, Andy Philippides for
discussions, and Mark Speight for sharing
unpublished data. ATAB is supported by the
BBSRC and the University of Sussex. JEN
is supported by a Royal Society University
Research Fellowship.
References
1. Rogers, L.J., Vallortigara, G. and Andrew,
R.J. (2013). Divided Brains: The Biology and
Behaviour of Brain Asymmetries (Cambridge:
Cambridge University Press).
2. Frasnelli, E., Vallortiagara, G., and Rogers, L.J.
(2012). Left-right asymmetries of behaviour
and nervous system in invertebrates. Neurosci.
Biobehav. Rev. 36, 1273–1291.
3. Niven, J.E., Buckingham, C.J., Lumley, S., Cuttle,
M.F., and Laughlin, S.B. (2010). Visual targeting
of forelimbs in ladder-walking locusts. Curr. Biol.
20, 86–91.
4. Heuts, B.A., and Lambrechts, D.Y.M. (1999)
Positional biases in leg loss of spiders and
harvestmen (Arachnida). Entomol. Ber. (Amst.)
59, 13–20.
5. Rowell, C.H.F. (1964). Central control of an insect
segmental reflex: I. Inhibition by different parts
of the central nervous system. J. Exp. Biol. 41,
559–572.
6. Govind, C.K. (1989). Asymmetry in lobster claws.
Am. Sci. 77, 468–474.
7. Ades, C. and Ramires, E.N. (2002). Asymmetry
of leg use during prey handling in the spider
Scytodes globula (Scytodidae). J. Insect Behav.
15, 563–570.
8. Pascual, A., Huang, K.L., Neveu, J. and Preat,
T. (2004). Neuroanatomy: brain asymmetry and
long-term memory. Nature 427, 605–606.
9. Ghirlanda, S. and Vallortigara, G. (2004). The
evolution of brain lateralization: A gametheoretical analysis of population structure. Proc.
R. Soc. B 271, 853–857.
10. Levy, J. (1977). The mammalian brain and the
adaptive advantage of cerebral asymmetry. Ann.
N. Y. Acad. Sci. 299, 264–272.
1School
of Life Sciences and Centre for
Computational Neuroscience and Robotics,
University of Sussex, Falmer, Brighton BN1
9QG, UK.
E-mail: [email protected]
This is an open-access article distributed
under the terms of the Creative Commons
Attribution-NonCommercial-No Derivative
Works License, which permits non-commercial
use, distribution, and reproduction in any
medium, provided the original author and
source are credited.