Brief comm 20/1/00 mx

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U
ltrasonic hearing is common in
moths, which rely on it for defence
and communication
1,2
, but it has
never been demonstrated in butterflies.
Here we describe a new type of ultrasound-
sensitive ear that we have discovered in an
unusual group of nocturnally active,
neotropical butterflies, the Hedyloidea.
Hedylids have ears on their wings and
respond to ultrasound by making flight
manoeuvres to avoid bats. On the basis of
phylogenetic and comparative anatomical
evidence, we propose that hearing in Lepi-
doptera and day flight in butterflies both
result from an intense selection pressure
imposed by echolocating bats more than 50
million years ago.
Diurnality has traditionally been used to
distinguish butterflies from moths, and
underlies a major difference in the sensory
worlds of these two groups. Butterflies are
predominantly diurnal and rely on a well-
developed visual system for communication
and predator detection
3
. Although it has
been proposed that some butterflies have
low-frequency hearing
4,5
, ultrasonic hearing
is unknown for this taxon. In contrast, most
moths have tympanal ears that function
primarily to detect echolocation calls used
by insectivorous bats to locate and track
their prey
1
.
The Hedyloidea, which have previously
been identified as moths, are now believed
to be the closest relatives, and possibly the
‘living ancestors’, of modern-day butterflies
(Papilionoidea, Hesperoidea)
6,7
. The fore-
wing modifications of Hedyloidea have
been suggested to function in hearing or
scent production
6
, but until now they had
not been studied in living individuals.
Because hedylids fly at night and are there-
fore exposed to bats, we predicted that they
should have ultrasound-sensitive ears and
exhibit bat-avoidance behaviour.
Our anatomical investigations of Macro-
soma heliconiaria, collected live on Barro
Colorado Island, Panama, have revealed a
tympanal ear
4
of intriguing design. The
eardrum (tympanal membrane) is nestled
within a tympanic cavity at the narrow end
of a canal that resembles the pinna of a rab-
bit ear (Fig. 1a,b). The thin (1 
mm) mem-
brane stretches over a large air-filled
chamber and has three vibration-sensitive
chordotonal sensory organs attached to
separate regions of its inner surface, similar
to the frequency-discriminating ears of
acridid grasshoppers
8
. The ears move with
the wing and so may be efficient at localiz-
ing sounds during flight. Comparative
anatomical studies indicate that ears are
widespread throughout the Hedyloidea
(about 40 species), and are equally devel-
oped in both sexes.
When stimulated with an intense ultra-
sonic stimulus, hedylids perform one of
several flight manoeuvres (Fig. 1c), includ-
ing steep dives or climbs, upward or down-
ward loops, spirals and horizontal sweeps.
These responses, shown through ablation
studies to be governed by the tympanal
ears, are unpredictable in their direction,
and are characterized by short latencies
(45.4
59.35 ms) and substantial increases
(400.1%) in flight speeds. These features are
of selective advantage to an insect in a close-
range encounter with a bat
9
.
The discovery of hearing in the Hedy-
loidea provides an insight into the evolution
of lepidopteran ears and diurnality in but-
terflies. Mapping ultrasonic hearing onto a
phylogeny of the Lepidoptera
10
shows that it
has evolved independently at least six times,
all within the obtectomeran lineage (Fig. 2).
Current fossil evidence indicates that the