Download Courtship role reversal and deceptive signals in the

ANIMAL BEHAVIOUR, 2000, 59, 411–421
doi: 10.1006/anbe.1999.1310, available online at http://www.idealibrary.com on
Courtship role reversal and deceptive signals in the long-tailed
dance fly, Rhamphomyia longicauda
DAVID H. FUNK* & DOUGLAS W. TALLAMY†
*Stroud Water Research Center
†Department of Entomology and Applied Ecology, College of Agricultural and Natural Resources,
University of Delaware
(Received 2 March 1999; initial acceptance 29 June 1999;
final acceptance 27 September 1999; MS. number: A8423)
We examined the function of secondary sexual characters in the role-reversed, lekking behaviour of
female long-tailed dance flies, Rhamphomyia longicauda Loew (Empididae), to test the hypothesis that the
degree of abdominal distention is an honest female signal about the state of egg development. Female
Rhamphomyia cannot hunt for prey and they receive all of their protein from males by exchanging
copulations for nuptial prey gifts. Females compete for male gifts within leks that are organized for a brief
period each evening before dark. Before hovering within leks, females swallow air, inflating expandable
pouches on the pleural margins of the abdomen. The result is a large saucer-like abdomen which is further
exaggerated by wrapping scaled pro-, meso- and metathoracic legs along its pleural margins. Male
preference for an enlarged abdomen was confirmed by suspending plastic models of varying size from
monofilament lines and recording which models attracted the most males. There was a positive
relationship between egg development and abdominal distention in a related species, R. sociabilis
(Williston), which lacks inflatable abdominal pouches. Multiple regression showed that in R. longicauda,
abdominal inflation completely masks the state of egg development. We conclude that female R. longicauda deceive mate-seeking males with the unreliable message that eggs are nearing maturation in order
to obtain a protein meal in exchange for copulation. Males that fail to identify a female bearing mature
eggs risk near-certain cuckoldry and an increased probability that the female will die before oviposition.

should be skewed so that there are fewer males than
females available for mating, females should compete
through courtship behaviour for access to those males
and males should become more selective about which of
those females they mate with.
These predictions concerning courtship role reversal
have been upheld in a variety of vertebrate and invertebrate taxa (Gwynne 1991). Male reproductive investment
triggering female competition/courtship behaviour and
male choosiness comes in two forms: paternal care (vertebrates: Wells 1978; Reynolds 1985; Rosenqvist 1990;
belostomatid giant water bugs: Ichikawa 1988; Smith
1997; Zygophachylus harvestmen: Mora 1990; Rhinocoris
assassin bugs: Thomas 1995) and courtship feeding
through the capture (empidid dance flies: Svensson et al.
1989; Cumming 1994) or production (stomatopod crustaceans: Hatziolos & Caldwell 1983; several orthopteran
katydids: Gwynne & Simmons 1990; Simmons & Bailey
1990) of nutritious nuptial gifts. Paternal investment has
created sexual selection with enough strength and directionality to produce permanently enhanced secondary
Sexual selection is thought to operate when mating success is associated more with one particular phenotype
than with others (Darwin 1871). In theory, the sex with
the greatest investment in each offspring will have the
lower rate of offspring production (Thornhill 1986) and
the smaller number of sexually receptive individuals at
any one time, and thus will stimulate greater intrasexual
competition in the opposite sex (Williams 1966; Trivers
1972). Females are the more choosy, less competitive sex
in most species because they typically exceed males in
both pre- and postzygotic investment in offspring (Parker
et al. 1972; Trivers 1972). Reversal of this courtship norm
is predicted when reproductive investment by males
exceeds that of females (Gwynne 1991) or when males
control resources critical to female reproduction (Alcock
& Gwynne 1991). In such cases, the operational sex ratio
Correspondence: D. H. Funk, Stroud Water Research Center,
970 Spencer Road, Avondale, PA 19311, U.S.A. (email:
[email protected]). D. W. Tallamy is at the Department
of Entomology and Applied Ecology, University of Delaware,
216 Townsend Hall, Newark, DE 19717-1303, U.S.A.
0003–3472/00/020411+11 $35.00/0
2000 The Association for the Study of Animal Behaviour
411
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2000 The Association for the Study of Animal Behaviour
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ANIMAL BEHAVIOUR, 59, 2
Mating pairs
Courtship swarm
Hunting males
Stream
Figure 1. Diagrammatic depiction of hunting, courtship and mating interactions in R. longicauda.
sexual characters in the females of role-reversed birds
(Gill 1995), but such ornaments are rare among insects
with reversed courtship roles, having arisen only among
empidine dance flies (Cumming 1994). In Empis and
Rhamphomyia (Empidinae), 28% of 583 species examined
have developed some combination of enlarged wings,
pinnate leg scales and eversible abdominal sacs on
females alone. Although courtship behaviour has been
studied in only 18 empidines with female secondary
sexual characters, good evidence for role reversal has been
found in all but two (Cumming 1994).
What remains a puzzle is the function of secondary
sexual characters in female dance flies. The role of empidine secondary sexual characters has been examined
empirically only in Empis borealis, a dance fly in which
the posterior distal margin of female wings is considerably expanded (Svensson & Petersson 1987, 1988;
Svensson et al. 1989). In this species, males carrying prey
enter female leks where they discriminate among hovering females on the basis of female wing size. Apparently
wing size is an accurate index of both female size and
age. The most common secondary sexual characters on
female dance flies, however, are ventral eye facets that are
much larger than the dorsal facets, large pinnate scales on
the legs and bizarre eversible sacs on the pleural margins
of the abdomen (Newkirk 1970; Cumming 1994).
Although it has been presumed that pinnate scales and
eversible sacs are the result of sexual selection via male
choice (Cumming 1994), neither their role in female
courtship nor their effect on male choice has been delineated. Here we used the long-tailed dance fly, Rhamphomyia longicauda Loew (Empididae), and a congener,
R. sociabilis (Williston), to test the hypothesis that pinnate leg scales and eversible abdominal sacs increase the
apparent size of a lekking female’s abdomen and that
abdomen size is an honest signal of a female’s readiness to
oviposit.
Sex Role Reversal in Rhamphomyia
Empidid dance flies are a large group of predators with
some 3300 described species world-wide (Chvála 1976).
Cumming (1994) argues that the plesiomorphic mating
system of the largest subfamily, the Empidinae, is lek
polygyny wherein males present females with a nuptial
gift (a prey item) at the time of pair formation. Female
empidines, having lost the ability to hunt on their own,
rely for protein entirely on male-borne nuptial gifts
received during frequent copulations (Downes 1970). It is
because males control food resources critical to females
for the development of their eggs that an increase in the
frequency of sex role reversal is predicted in empidines
(Cumming 1994).
Role reversal in the form of female rather than male
leks has been reported in eight species of Rhamphomyia
(Cumming 1994). In R. longicauda, females gather at dusk
to form leks in which they hover until dark (Steyskal
FUNK & TALLAMY: RHAMPHOMYIA COURTSHIP REVERSAL
METHODS
Female Lekking Behaviour
Figure 2. Uninflated (top) and inflated (bottom) R. longicauda
females.
1941; Newkirk 1970). During this time males hunt and
capture small insects (Fig. 1). As soon as they succeed,
males individually fly with their nuptial gift into the
female swarm, approaching from below. Before attempting to copulate, males fly repeatedly beneath the swarm,
presumably to assess relative female quality. When a
potential mate is selected, a male rises beneath her and
hovers while the female drops to meet him. Prey
exchange is then negotiated and copulation occurs on the
wing. Males without nuptial gifts never enter female leks.
Females return nightly to the lek to mate and feed while
developing their eggs.
The most curious aspect of female courtship in R. longicauda is that prior to lekking, females expand the size of
their abdomen via pleural extensions of their integument
(Newkirk 1970). A lekking female bears a laterally
expanded abdomen three to four times the width of a
nonlekking female (Fig. 2). Females also have long pinnate scales arranged on a single plane along the lateral
margins of their legs and ventral eye facets that are larger
than dorsal facets. Male R. longicauda have none of these
traits. Because they collapse when punctured, Steyskal
(1941) suggested that lekking females inflate themselves
with air.
We observed and manipulated courtship swarms of
R. longicauda at 11 sites in deciduous hardwood edge
habitats between 25 May and 1 July from 1985 to 1990
in Avondale, Chester County, Pennsylvania, U.S.A. We
quantified sex ratios, mate selection by males, and the
number of unmated individuals of each sex remaining in
a swarm after the last successful pairing with a Panasonic
WV-1854 high-resolution video camera with extended
red and near-infrared sensitivity (<940 nm, usable illumination level 0.01 foot candles) fitted with a 50-mm f/1.8
lens. Supplementary illumination was used as needed,
provided by a single 15-W incandescent light bulb in a
darkroom safelight (Standard B&W safelight filter) at a
minimum of 3 m distance from subjects. We analysed
recordings on a Quasar VH5261 video cassette recorder.
To determine the mechanism by which lekking females
expand their abdomens, we performed dissections of
expanded females fixed either in alcoholic Bouin’s solution (Carolina Biological Supply Company, Burlington,
North Carolina, U.S.A.) or snap-frozen in flight within
95% ethanol cooled to approximately 80C with dry
ice. In both cases the preservative was placed in a shallow,
wide-mouthed (12-cm diameter) plastic jar. Females were
then collected from within swarms directly into the jar.
When females were snap-frozen, they were immediately
transferred to a freezer (80C) for 12 h, then warmed to
10C and transferred to alcoholic Bouin’s for an
additional 24 h before thawing to room temperature. This
procedure permanently hardened the pleural regions of
the abdomen in the expanded position. Females fixed
directly in Bouin’s solution deflated slightly before permanent fixation, but were still easily dissected in the
expanded position.
To determine the occurrence of virgin females in leks
over time, we sampled swarms periodically throughout
the mating season. We caught and fixed females (N=88)
in Bouin’s solution as before, and dissected and examined
the spermatheca of each for the presence or absence of
sperm. We also dissected females from one site (Buck’s
Corner) early (31 May 1987; N=23) and midseason (16
June 1987; N=26) to assess the stage of egg development
in lekking females over time. We arbitrarily chose six size
classes of eggs and assigned the eggs of each dissected
female to a single size class. Because Rhamphomyia displays gonotrophic concordance, all eggs of each clutch
mature simultaneously. Thus, the size of any given egg
can be used as an index of the stage of maturation of the
entire clutch. We measured 10 eggs from each female.
Male Mate Choice
We quantified the effect of female size on male mate
choice using two-dimensional models of inflated females.
We created accurate models by photographing parts of
inflated females that had been snap-frozen in flight as
they swarmed. Photographs were made in silhouette (i.e.
backlit) using Kodak Technical Pan film (2415) developed
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414
ANIMAL BEHAVIOUR, 59, 2
either accepted or rejected each model as a potential mate
after flying beneath it. A male was judged to have
accepted a model if it hovered no more than 3 cm under
it for several seconds. Males that did not pause beneath a
model were scored as having rejected it. To avoid problems from pseudoreplication, males that consecutively
returned to the same model were only scored once. To
achieve homogeneity of variance, we log transformed the
number of male acceptances of each model size and
compared them by analysis of variance (ANOVA). We
used Ryan’s Q multiple comparison procedure to separate
means.
Figure 3. Black and white composite print used as an artificial model
of an inflated R. longicauda female for quantifying the effect of
female size on male preference.
for highest contrast (Kodak developer D-19). We substituted wing outlines filled with 50% ‘grey’ computergenerated pattern for actual wing images. We combined
the various female parts (wings, legs, head, thorax, abdomen) in the darkroom into black and white composite
prints that represented an intact female in flight (Fig. 3).
We copied these using Technical Pan film, again developed for highest contrast. We then ‘printed’ negatives on
the same type of film using a slide duplicator, yielding
film positives. Printing was done at several magnifications including life size (i.e. actual size of average
field-collected females), 0.75, 1.5 and 2.0. We cut
the images from the film and trimmed them as closely as
possible. Clear areas of film were transparent to wavelengths between 314 and 900 nm; black image areas were
opaque at all wavelengths. We then glued (epoxy) models
to 25-cm pieces of fine monofilament nylon thread and
suspended them at approximately 5-cm intervals from
another section of monofilament strung across swarm
sites so that models hung at about 40 cm above the
ground amidst actual lekking females (Fig. 4). We
recorded activities on videotape as described above. We
used two models of each of the four sizes with positions
re-randomized each night data were collected. We quantified male response to these models during the entire
swarming period (about 45 min) each night (N=9). Males
Abdomen Size as an Honest Signal
We tested the hypothesis that abdomen size is an
honest signal of the state of egg maturation in Rhamphomyia. We examined the effect of body size, egg
number and egg size (egg maturity) on abdomen size in
female R. longicauda, which can misrepresent the actual
size of their abdomens both by inflating their guts with
air and by wrapping their scaled legs around their abdomens’ perimeter, and in female R. sociabilis, a western
North American species whose abdominal morphology is
argued to represent the unmodified ancestral condition
under which the early courtship dynamics between
R. longicauda males and females most likely developed;
that is, female R. sociabilis lack the ability to inflate the
abdomen and thus the ability to disguise the true size of
the abdomen over the course of egg development.
Although Evans (1988) refers to female R. sociabilis with
swollen abdomens and Cumming (1994) lists the species
as having extensive pleural membrane, our dissections
provide no evidence of inflation. Female R. sociabilis also
have pinnately scaled legs, but rather than position them
concentrically around the abdomen as in R. longicauda,
R. sociabilis females dangle them beneath their bodies
during courtship flights (H. Evans, personal communication). Rhamphomyia sociabilis also differs from
R. longicauda in that copulating pairs do not disperse from
the lek site but rather form a subswarm near the swarm of
unmated lekking females (Evans 1988). This feature of the
Figure 4. The pattern in which various-sized models of inflated R. longicauda females were suspended from monofilament line among actual
lekking females to quantify the effect of female size on male preference.
FUNK & TALLAMY: RHAMPHOMYIA COURTSHIP REVERSAL
First male observed hunting (N = 13)
Mating interaction
First male with prey swarming (N = 18)
First female swarming (inflated) (N = 31)
First mating pair observed (N = 5)
Swarm dispersed (N = 27)
–80
–60
–40
–20
0
Time relative to sunset (min)
20
40
60
Figure 5. The median and range of times at which mating interactions in R. longicauda began relative to sunset.
mating system of R. sociabilis enabled direct measures of
female traits associated with male preference.
We obtained copulating (N=30) and courting (N=30)
R. sociabilis females that had been fixed in Bouin’s
solution from populations near Livermore, Larimer
County, Colorado, U.S.A., with the help of Howard
Evans, Colorado State University. Inflated R. longicauda
females (N=30) were snap-frozen from swarms collected
in Avondale, Pennsylvania, in the latter part of the
swarming season. We measured 10 eggs from each ovary
from all females of both species as well as total egg
number and three measures of body size: head width
(frontal view), wing length (annular incision to apex) and
notal length (pronotum to tip of scutellum). We conducted a principal component analysis for both species to
create a single index of overall body size based on the
synthesized contribution of head width, wing length and
notal length to body size. We then used this index (PC1)
with the variables egg number and egg size in a stepwise
multiple regression to determine which accounted for the
majority of the variation measured in abdomen area. We
also compared egg size, egg number and body size
between R. sociabilis females from copulating swarms and
females from courting swarms using t tests.
We quantified total abdominal area when viewed two
dimensionally from the venter (the view afforded a discriminating male) using the image analysis software IP
Lab Spectrum 3.1.2a (Scanalytics, Inc., Fairfax, Virginia).
Before dissections, the two-dimensional image of the
abdomen of each female was video-captured on a Power
Macintosh 7500 using a Sony CCD-IRIS colour video
camera (model DSC-107A) mounted on a stereomicroscope.
RESULTS
Female Lekking Behaviour
At our study sites, lekking in R. longicauda began about
10 min prior to sunset (2025 hours) and lasted about
40 min (Fig. 5) every night with suitable weather during
the month of June. The first lek was observed on 25 May
and the last on 2 July. Lek sites shared no obvious swarm
marker on the ground, but all leks oriented directly under
light gaps in an otherwise complete canopy. At dusk such
gaps provided the essential ‘white’ background against
which females could hover as conspicuous silhouettes.
Leks varied in approximate size from 10 to 100 females,
with little variation per site over the course of the season.
Lek members slowly patrolled a horizontal plane about
0.5 m2 from 0.3–0.6 m above the ground or vegetation
with their abdomens inflated and their scaled legs held
concentrically around their abdomens. Females arrived at
the swarm site inflated or uninflated. Uninflated females
perched on nearby vegetation and proceeded to inflate
their abdomens, a process which took about a minute.
Dissection of snap-frozen, inflated females revealed that
inflation was accomplished by pneumatic expansion of
the midgut. Presumably females ‘swallow’ air to accomplish this. The hindgut remains uninflated, probably
either due to inelasticity or the closing of a sphincter
between it and the midgut. The result of this gut inflation
was to push the abdominal contents laterally into the
expandable pouches of the pleural membrane on segments two through seven (Fig. 2). The combination of gut
inflation and the lateral position of the legs gave hovering females the appearance of having abdomens much
415
ANIMAL BEHAVIOUR, 59, 2
25
20
15
10
5
0
5
10
15
20
25
0.5
31 May N = 23
0.4
0.3
0.2
1 June
16 June
Date
1 July
Figure 6. Presence of unmated individuals (by sex) in nightly
courtship swarms of R. longicauda following the last successful pairing in a given night. Combined observations from 1986, 1987, 1988
and 1990.
larger than they actually were, especially when viewed
from below as a silhouette against the sky.
One or more (up to 20) flies of either sex remained
unmated when courtship swarms dispersed (about
30 min after sunset) on the 21 nights on which such
observations were made (Fig. 6). Very early and very late
in the mating season there were more males with prey
than females to evaluate, but during most of the mating
season males with prey were in short supply and hovering
females were the only individuals remaining at the lek
site. Female behaviour at this time was marked by
repeated sudden descents similar to those initiating pair
formation in an apparent desperate attempt to secure a
mating with (nonexistent or no longer visible) males.
Only on two occasions were unmated members of both
sexes present in the same swarm when interactions were
terminated by darkness.
Dissections proved that throughout most of the courtship season leks were comprised entirely of inseminated
females; virgins were not found after the first week of
June and even on the earliest dates of dissection never
exceeded 4% of the females examined. As expected, eggs
of most females examined at the end of May were in the
early stages of vittelogenesis, but by mid-June all stages
of egg development were recorded in nearly equal
proportions (Fig. 7).
Male Mate Choice
Male R. longicauda began hunting up to an hour
(median 40 min) prior to sunset either in the vicinity of
courtship swarm sites or up to 30 m away (Fig. 5). While
hunting, flight was characterized by a fast patrolling,
often in a rough ‘figure of 8’ pattern. Males seemed to
take any prey they could capture and subdue, but typically sought other swarming insects, especially flies
(Diptera), mayflies (Ephemeroptera) and caddisflies
(Trichoptera). Males with captured prey immediately flew
to the swarm site (Fig. 5). If they arrived before females,
males flew several passes through the swarm area before
landing on nearby vegetation where they awaited the
arrival of females. Once the female lek was organized,
0.1
Frequency
Leftover individuals (by sex)
Female Male
416
0
I
II
III
IV
V
VI
III
IV
V
Egg developmental stage
VI
0.5
16 June N = 26
0.4
0.3
0.2
0.1
0
I
II
Figure 7. Frequency of various stages of R. longicauda egg development at one lek site (‘Buck’s Corner’) early (31 May 1987) and
midway (16 June 1987) through the mating season.
males bearing prey flew beneath the swarming females.
After several passes under the swarm, males would typically approach an individual female by ascending to a
position 1–2 cm directly beneath a female and hovering
briefly (0.5–2 s). A female thus approached would immediately drop to the male, whereupon the two would fly
away together as they negotiated the transfer of the
nuptial gift and the male climbed into the mating position above the female (Fig. 8). Detailed observation of
this process was impossible because it occurred as the
pairs flew rapidly away from the swarm, but during
negotiation of prey transfer individuals appeared to be
head to head. Occasionally pairs separated during this
phase, but the vast majority of pairings appeared to be
successful. Among pairs that separated, it was not clear
whether separation resulted from rejection by one partner or merely a failure to transfer prey. Successful pairing
usually took 10 s or less, after which the two flew slowly
in copula, often in a rough ‘figure of 8’ 1.5–3 m above
ground, directly beneath the lowest branch of a tree, and
2–10 m from the swarm site. Occasionally as many as four
pairs were seen together, but mating pairs generally did
not congregate and they were never observed to alight.
FUNK & TALLAMY: RHAMPHOMYIA COURTSHIP REVERSAL
5.0
(a)
4.5
4.0
2
Area of abdomen (mm )
3.5
Y = 0.005X + 2.356
r2 = 0.72 P ≤ 0.0001
3.0
300
200
400
(b)
16
14
Figure 8. Rhamphomyia longicauda in aerial copulation. Female
below, feeding on a nuptial gift (small tipulid crane fly).
12
During prey transfer, and even throughout copulation,
males maintained their grasp on the prey item with at
least their prothoracic legs (Fig. 8). Nuptial flights lasted
at least until it became too dark to see the pairs under
ambient light (about 40 min after sunset). Neither males
nor females returned to the swarm the same night of
a successful mating. Males without prey were never
observed in the courtship swarm.
When R. sociabilis females from courtship swarms were
compared to those from mating swarms the two groups
did not differ in body size nor in the number of eggs they
were carrying (Table 1). They did, however, differ in egg
length; females that had been selected as mates by males
carried eggs that were significantly larger (more mature)
than the eggs in females that had failed to attract mates.
A simple regression of abdominal area against egg length
in lekking R. sociabilis females revealed a highly significant (P≤0.0001) and relatively tight (r2 =0.72) relationship
(Fig. 9), suggesting that R. sociabilis males select mates
that are close to oviposition by discriminating against
females with unswollen abdomens. Manipulations with
plastic models clearly showed that abdomen size also
dictated male preference in R. longicauda. When given a
choice between models of four sizes, males approached
the largest model (twice life size) significantly more often
Y = 0.011X + 10.349
r2 = 0.23 P = 0.0068
225
300
375
Egg length (µm)
Figure 9. The effect of egg length on abdominal area in (a)
R. sociabilis, a dance fly incapable of inflating its abdomen, and (b)
R. longicauda, a species in which females disguise the actual size of
their abdomen by swallowing air prior to joining a lek.
than the other sizes (ANOVA: F3.24 =9.875: P=0.0002;
Fig. 10).
Abdomen Size as an Honest Signal
In contrast to R. sociabilis, a simple regression of
abdominal area on egg length in inflated R. longicauda
females showed that abdominal area was a poor indicator
of the state of egg maturation for mate-seeking males in
this species (Fig. 9). Although the relationship was significant (P=0.007), only 23% of the variation in abdomen
size was explained by egg length.
The difference in the effect of egg maturation on
abdominal size between R. sociabilis and R. longicauda was
Table 1. Comparison of females in Rhamphomyia sociabilis courting swarms with those in mating swarms
Trait
Swarm type
N
Mean±SE
t
P
PC1 (body size)
Mating
Courtship
Mating
Courtship
Mating
Courtship
20
20
19
17
30
30
−0.10±0.23
0.10±0.22
30.2±1.1
28.6±0.8
325.0±28.6
253.0±23.0
0.63
0.53
1.17
0.25
2.01
0.05
Egg number
Egg length (µm)
450
417
ANIMAL BEHAVIOUR, 59, 2
entirely (Table 2). Instead, body size explains 67.1% of
the variation in abdominal area.
7
Ln male approaches
418
6
5
A
309
DISCUSSION
AB
4
117
3
BC
26
2
C
12
1
0
2.0
0.75
1.5
1.0
Model size
Figure 10. The effect of female model size on male preference in R.
longicauda. Bars represent 95% confidence intervals. Untransformed
means to the right of log transformed means. Means sharing the
same letter did not differ significantly (Ryan’s Q multiple comparison
procedure; P=0.05).
Table 2. Partitioned stepwise multiple regression of abdominal area
against egg length, body size and egg number in Rhamphomyia
sociabilis and R. longicauda
Species
Independent variable
R. sociabilis
Egg length+
PC1 (body size)+
egg number
PC1 (body size)+
egg length+
egg number
R. longicauda
r2 (%)
P
72.4
81.2
82.3
67.1
67.4
67.8
<0.0001
0.0241
0.2224
<0.0001
0.5266
0.5499
Table 3. Eigen values for principal component analyses of head
width, notal length and wing length as measures of body size in
Rhamphomyia longicauda and R. sociabilis
Species
R. longicauda
R. sociabilis
e1
e2
e3
e1
e2
e3
Eigen values
Variance proportion
2.904
0.061
0.034
2.880
0.074
0.046
96.8
2.0
1.1
96.0
2.5
1.5
even more apparent when the relative effects of egg
length, body size and egg number on abdominal area
were examined via stepwise multiple regression (Table 2).
Principle component analyses of body size measures provided strong evidence for a single principal component
variable for size (PC1) in both R. longicauda and R. sociabilis (Table 3), which we used as our index of overall body
size in the multiple regression. In R. sociabilis, the dance
fly that is unable to inflate its abdomen, there was a
highly significant relationship (P<0.0001) between abdomen size and the state of egg maturation, with egg length
explaining 72.4% of the variation in abdomen size. This
was not the case in R. longicauda; when lekking females
artificially inflate their abdomens with air, the relationship between egg length and abdomen size disappears
Our observations and manipulations confirmed that
courtship roles in the long-tailed dance fly, R. longicauda,
are reversed. Females hover in small- to moderately sized
leks nightly where they compete with each other for
access to males bearing nuptial prey. Selection to attract
males is particularly intense because males provide the
only known protein source for adult females during the
nutritionally demanding period of oogenesis (Cumming
1994). Dissections showed that females become inseminated very early in the season, yet they apparently return
to the lek nightly, using males as a source of food as well
as sperm. Anecdotal evidence suggested that females
are site faithful and return to the same lek each night:
when females were removed from a lek for dissection,
the lek diminished in size on subsequent nights by
approximately the number of females removed.
The need to attract mate-seeking males in empidine
females has led to the evolution of three prominent
secondary sexual traits present in various combinations
and in a variety of species: broadened wings, long pinnate
scales on the margins of the legs, and eversible membranes on the pleural margins of the abdomen (Cumming
1994). Female R. longicauda have pinnately scaled legs
and pleural sacs on the abdomen and these work in
concert to enable the female to misrepresent the actual
size of her abdomen to males. Before joining a lek,
females sit on nearby vegetation and ‘swallow’ air into
their midgut. As a female inflates her gut, the normal
contents of her abdomen (hemolymph, ovaries, fat
bodies, malphighian tubules) are forced laterad into her
eversible pleural sacs. Expansion of the abdomen occurs
laterally rather than dorsoventrally, resulting in a round
saucer-like abdomen. A fully inflated female then takes
flight and hovers within the lek among her competitors.
To accentuate the size of her abdomen further, a lekking
female positions her scaled legs along the lateral margin
of the abdomen.
Such behaviour can only be appreciated when the
female is viewed from the perspective of a mate-seeking
male. Males that have succeeded in capturing a prey item
enter a lek of females from below and fly slowly beneath
the participants. Until this report, dipteran mating
swarms (typically comprised of males) as well as female
swarms in other sex-role-reversed empidines were
thought to orient exclusively over terrestrial lek markers
such as puddles, rocks, or distinctive vegetation (Sivinski
& Petersson 1997). In contrast, R. longicauda and probably
other Rhamphomyia with inflatable abdomens (Cumming
1994) use open patches of sky within an otherwise closed
canopy as lek-site markers. This unique choice of a
marker above the swarm rather than below it provides the
backlighting for hovering females to display their deceptive sexual signals to their greatest advantage. A backlit
hovering female appears only as a dark silhouette when
viewed from below (Fig. 3). Not only does this advertise
the inflated abdomen clearly, it also enables a female to
FUNK & TALLAMY: RHAMPHOMYIA COURTSHIP REVERSAL
deceive discriminating males about the actual size of her
abdomen by folding her fringed legs concentrically
around the abdomen’s perimeter. Under such conditions
it is very difficult or impossible for a male to distinguish a
female whose abdomen is full of mature eggs from one
whose abdomen contains only undeveloped ovaries and
air. The best strategy for a male would be to choose the
female with the largest abdomen.
Manipulations with two-dimensional models of varying size confirmed that R. longicauda males do, in fact,
prefer to mate with larger females. Several hypotheses,
some of which are not mutually exclusive, might explain
this preference. (1) Large females may be more capable of
laying larger egg clutches or clutches comprised of larger
eggs (Svensson & Petersson 1987). (2) Females with the
largest inflatable sacs may be preferred because they bear
‘good attractiveness’ genes (Eberhard 1996) and will thus
produce ‘sexy’ daughters. (3) Inflated abdomens may
compromise survivorship through lost manoeuvrability
and thus convey ‘good viability’ genes via the handicap
principle (Zahavi 1995; Zahavi & Zahavi 1997). (4)
Females with larger abdomens may be further along in
the gonotrophic cycle and thus be closer to oviposition
than females with smaller abdomens. There are two
reasons males might prefer females carrying eggs that are
nearly mature. First, if ‘last-male’ sperm precedence is as
important in R. longicauda as it is in a number of other
flies (Ito & Yamagishi 1989; Otronen 1989, 1990; Ridley
1989; Opp 1990; Lorch et al. 1993), the last male to mate
before oviposition has a distinct paternity advantage over
males that precede him. Second, females whose eggs are
mature are more likely to survive until oviposition
than are females whose eggs still require the nutrients
delivered by several additional matings.
Our data suggest that the stage of egg development is a
better predictor of male preference than is overall body
size in Rhamphomyia dance flies. In R. sociabilis, the empidine that is not able to inflate its abdomen, egg length
explained nine times more of the variation in abdomen
area than did body size. Furthermore, courting females
(those that had not yet attracted a prey-bearing male)
were not significantly smaller in body size than mating
females, but their eggs were significantly younger than
the eggs of copulating females. Thus, R. sociabilis provides
empirical support for the hypothesis that, in species
without inflatable abdomens, Rhamphomyia males that
prefer females with large abdomens couple with females
that are closer to oviposition.
Although confirmation must await reliable phylogenetic inferences, it seems likely male preference for
females with large abdomens pre-dates the evolution
of inflatable abdominal pouches in Rhamphomyia. Thus,
our data also suggest that the evolution of inflatable
abdominal pouches has enabled R. longicauda females
to capitalize on a pre-existing male bias (sensu Ryan &
Keddy-Hector 1992; Basalo 1990) towards egg-laden
abdomens while simultaneously concealing the state
of egg maturation in an extraordinarily effective way.
Partitioning the variables in our stepwise multiple regression showed that, in contrast to R. sociabilis, overall body
size rather than egg length accounted for most of the
variance in abdomen area. Inflated females completely
masked the effect that egg growth would otherwise have
had on abdominal distention. Egg length in inflated females explained only 0.3% of the variation in abdominal
area not accounted for by body size. A simple regression of
abdominal area on egg length in R. longicauda suggests
that egg length has a measurable effect on abdominal
area, but we believe this effect is a consequence of the
stronger relationship between overall body size and abdominal area in this species. As body size increases in
R. longicauda females, there is more pleural membrane to
inflate and thus larger females can inflate their abdomens
to a greater size than can smaller females. As our manipulations with models demonstrated, larger females attract
more males, each of which brings important food resources to the copulation. If larger females receive more
food than smaller females, their eggs will develop faster;
hence, larger females will, on average, carry larger eggs
(the relationship seen in the simple regression of Fig. 9),
not because the eggs distend the inflated abdomens of
these females, but rather because larger females have the
capacity to create larger abdomens and thus attract more
male-borne food. The sample of R. longicauda females
represented in Fig. 9 was taken about 3 weeks into the
season, when this effect might be expected to be most
pronounced.
This conclusion is somewhat at odds with that of
Svensson et al. (1989) who studied another dance
fly, Empis borealis. As in R. longicauda and R. sociabilis,
E. borealis displays complete sex role reversal, with
females competing for male favour within leks (Svensson
& Petersson 1987). But unlike Rhamphomyia species,
female E. borealis differ from males in wing morphology
alone; the distal margins of the female wing are greatly
expanded and correlate well with female size (Svensson &
Peterson 1988). Although Svensson et al. (1989) found
that males prefer to mate with the largest females (i.e.
those females with the largest wings), they also found
that mated females had less wing wear than unmated females and thus were probably younger. If male
E. borealis use wing size as a measure of female size when
selecting mates, older females with more wing wear and
thus smaller wings would be at a selective disadvantage.
Yet older females may be more likely to bear larger, more
mature eggs. It is also possible, however, that E. borealis
females regularly produce a second clutch, and that older
females with more wing wear are more likely to have
already laid their first clutch and to offer only immature
eggs of the second clutch to choosy males. More research
is needed to be able to make this distinction. In comparison, dissections of R. longicauda suggest that (1) either
some females are consistently rejected by males to the
extent that they go long periods without proteinaceous
food and consequently mature their first egg clutch very
slowly, or (2) a substantial proportion of the females in a
lek are seeking food for the development of their second
clutch.
Dishonest signalling about the state of egg development in R. longicauda can be labelled true behavioural
deception as defined by Semple & McComb (1996)
because the receiver of the signal, the mate-seeking male,
419
420
ANIMAL BEHAVIOUR, 59, 2
registers a situation that does not actually occur; that is,
males that approach inflated females because they have
swollen abdomens do not have the same probability of
mating with a female whose eggs are near oviposition as
do R. sociabilis males that approach females whose abdomens are distended with nearly mature eggs rather than
air. As a result of inflation, R. longicauda females benefit
from the acquisition of food, while males pay the cost of
having hunted for and fed a female with a lower likelihood of surviving to oviposition and which will almost
certainly cuckold him.
One might argue that abdominal inflation in R. longicauda is not a dishonest signal because a regression
indicates 23% of the variation in egg size is explained by
abdomen size after inflation. However, this does not
explain the evolution of abdominal inflation in the first
place; comparisons with R. sociabilis clearly show that
inflatable sacs could not have evolved to advertise egg
size honestly because inflation decreases the accuracy of
this signal over that conveyed by uninflated females by
49%! If signal accuracy drove selection of this trait, males
preferring uninflated abdomens would have been able to
identify females with mature eggs more often than males
with a preference for inflated abdomens, and thus would
have enjoyed the fitness advantages of higher paternity
levels and greater offspring survivorship. It is more parsimonious to argue that inflatable sacs evolved precisely
because males could not distinguish between abdomens
inflated with air and abdomens swollen with mature eggs;
that is, because inflatable sacs successfully deceived mateseeking males, females that bore them gained a considerable advantage over females that did not. Rather than
indicating that there is no deception imparted by
abdominal inflation, the fact that males continue to gain
a small advantage by attempting to select the largest
inflated abdomens instead suggests that the deception
from abdominal inflation is not perfect.
Deceptive sexual signals may carry important ecological costs for the Rhamphomyia females that employ them.
One obvious consequence of inflating the abdomen to a
flattened disc-like structure is to sacrifice aerodynamic
competence in comparison to flies with the uninflated
ancestral state. Inflated R. longicauda females do not
appear to fly or manoeuvre as quickly as uninflated
R. longicauda males or females of other sex-role-reversed
empidines that have not evolved inflatable abdominal
sacs. Inflated females, therefore, might be more vulnerable to bird predation. We suspect that, unlike
other empidines that typically lek for long periods
throughout the day (Aldrich & Turley 1899; Downes
1970; Svensson & Petersson 1987; Evans 1988; Cumming
1994), R. longicauda lek only during dusk as this is the
only time of daylight during which most avian predators
do not forage. Males of some empidine species have been
reported to be relatively scarce towards the end of the
swarming period (Laurence 1952; Chvála 1980, as cited in
Cumming 1994; Svensson & Petersson 1987). Cumming
(1994) suggests that this may be explained by a combination of protandry and a higher risk of mortality
associated with hunting (compared with the relatively
stationary, nonhunting females). However, Fig. 6
indicates that R. longicauda males predominate at lek sites
both early in the season and very late in the season,
suggesting both protandry and greater longevity in males.
This observation is consistent with the idea that females
of sex-role-reversed empidines might be at higher risk of
predation because of the burden of ornamentation.
Several hypotheses attempt to explain the evolution of
female secondary sexual characters in dance flies (reviewed by Cumming 1994). It has been proposed that
traits such as enlarged wings, pinnate leg scales and eversible abdominal sacs (1) enable lekking females to
fly more aerodynamically (Gruhl 1963; Svensson &
Petersson 1987), (2) act as premating isolating mechanisms (Downes 1970; Chvála 1990), or (3) evolved to
attract small moths to communal swarms where they
could be preyed upon by male dance flies (van der Goot &
de Vos 1988). We agree with Cumming (1994), however,
that secondary sexual traits in female dance flies function
in the same way that secondary sexual traits do in the
males of countless animal species; to signal, either honestly or deceptively, fitness while competing for mates.
We conclude that male control of all proteinaceous resources in concert with selection for males to favour
females with large abdomens has led to the reversal of
normal male–female courtship roles in R. longicauda and
intense intrasexual competition among females for access
to prey-bearing males. Such intense selection, in turn, has
favoured females with the ability to manipulate the size of
their abdomen at will, artificially inflating it before competing with other females in leks and further accentuating
its bizarre size with the judicious posture of fringed legs.
Because the misrepresentation of abdomen size is best
displayed in silhouette through backlighting, groundbased lek markers so common in other swarming Diptera
have been abandoned in R. longicauda in favour of distinct
patches of sky framed by dark canopy leaves. Against this
background hovering females repeatedly conceal the true
state of egg development from mate-seeking males. In so
doing, even females whose eggs are many days from
maturity acquire the protein required to complete oogenesis at least once before death. Thus, abdominal inflation
in female R. longicauda appears to be one of the most
successful dishonest sexual signals known.
Acknowledgments
We thank J. D. Newbold and E. L. White for statistical
advice, R. G. Weber for field assistance, Darryl Gwynne
and two anonymous referees for helpful comments on
the manuscript, and the Stroud Foundation for providing
facilities. We are especially grateful to Howard Evans for
supplying the necessary R. sociabilis females for dissection
and for helpful suggestions throughout the project.
Published as paper No. 1658 of the Delaware Agricultural
Experiment Station, contribution No. 716 of the Department of Entomology and Applied Ecology, University of
Delaware, Newark.
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