Download Multiple origins of a major novelty: moveable abdominal lobes in

EVOLUTION & DEVELOPMENT
3:3, 206–222 (2001)
Multiple origins of a major novelty: moveable abdominal lobes
in male sepsid flies (Diptera: epsidae), and the question
of developmental constraints
William G. Eberhard
Smithsonian Tropical Research Institute, and Escuela de Biología, Universidad de Costa Rica,
Ciudad Universitaria, Costa Rica
Correspondence (email: [email protected])
SUMMARY Contrary to the impression given by their extreme scarcity among extant species of flies, moveable processes on the abdomen are apparently of relatively simple
developmental origin, and they have evolved multiple times in
males of the small family Sepsidae. They are used to stimulate
the female during copulation in two groups, where they are
probably independently derived. Because female cuing of re-
productive decisions on particular types of stimuli will tend to
favor male abilities to elaborate such stimuli, sexual selection
by female choice may sometimes result in sustained selection
for certain types of innovations in males. The lack of moveable
appendages in most dipterans may be due not to developmental constraints, but to lack of selective advantages.
INTRODUCTION
able abdominal processes, the early stages of acquisition of
new abdominal appendages (“lateral lobes”) are relatively
common in males of the family Sepsidae (Fig. 1). This study
shows, using comparative morphology and direct observations of behavior, that the lateral lobes in two closely related
species are independently derived, and that in both cases
these structures are used during sexual interactions and are
probably under sexual selection by cryptic female choice.
The complex musculature associated with similar structures
in some other sepsids suggests that they are also moveable,
and that they may also have arisen independently under similar selection.
Phylogenetic uniformity in a trait is sometimes thought to
imply the existence of developmental constraints against alternative designs of that trait, and major innovations are
sometimes said to require substantial reorganization of the
phenotype (e.g., Müller and Wagner 1991). Constraint arguments of these sort run the risk of being tautological—whatever has not changed must have been constrained, and whatever has changed must not have been constrained. The basic
claim of constraint is potentially falsifiable, however, by
finding that repeated changes in a trait have occurred in an
otherwise unremarkable subgroup of a larger group in which
the trait is otherwise uniform. This is the situation documented here with respect to moveable abdominal appendages in flies.
Although abdominal appendages were present in the ancestors of adult insects (e.g., Snodgrass 1935; Birket-Smith
1984), all except those associated with the genitalia were lost
early in insect evolution. Subsequent evolution of new abdominal appendages or moveable processes has occurred
only rarely (e.g., Snodgrass 1935; Chapman 1999; Yen et al.
2000). In Diptera, aside from the dramatic and repeated fissions of genitalic sclerites (reviewed by Wood 1991; Sinclair
et al. 1994; Cumming et al. 1995), moveable abdominal processes are very rare (McAlpine et al. 1987). Thus, it might be
thought that such structures are developmentally difficult to
evolve. I will argue that this is not the case. Although adults
of most families of flies completely lack nongenitalic move© BLACKWELL SCIENCE, INC.
Specialized male morphology in sepsid flies
Sepsidae is a small family of flies of worldwide distribution
that includes about 240 species (Pont 1979). Adult males
have various sexually dimorphic traits that are often species-specific in form (Hennig 1949; Pont 1979; Steyskal
1987a), including a modified fourth abdominal sternite, the
subject of this study. In all sepsid genera in which the positions of copulating pairs have been determined, the male’s
fourth sternite touches or is very close to contacting the female during copulation, including Meroplius and Themira
(Cheligaster) (Šulc 1928) (Fig. 1), Sepsidimorpha sp. (Fig.
2), Sepsis (Parker 1972; Schulz 1999; Eberhard unpub. observation of S. neocynipsea), Archisepsis (Eberhard and
Pereira 1996), and Microsepsis (Eberhard 2001 in press). This
contact probably often occurs between the posterior portion
206
Evolutionary novelties in sepsid flies
Eberhard
207
Fig. 1. Schematic view of the long setae on the abdominal lobes of Themira ( Cheligaster) leachi, with the setae of the copulating male
(white) touching the female (stippled) (after Šulc 1928), and the relationships of Sepsidae (a member of the superfamily Sciomyzoidea)
and other groups of higher Diptera (Schizophora) (after McAlpine 1989).
of the male sternite and the female’s proctiger, which is
flexed dorsally to expose her vulva and permit intromission
(e.g., Fig. 2; see also Eberhard and Pereira 1996 on Archisepsis; Eberhard 2001 in press on Microsepsis).
MATERIALS AND METHODS
Copulating pairs of Palaeosepsis sp. (an apparently undescribed
species near P. chauliobrechma Silva) were observed in the field
near San Antonio de Escazu, San José Province, Costa Rica (el.
1400m). Each pair was aspirated into a plastic tube after copulation
had begun, and induced to walk into a clear glass vial where the
flies were observed using a 2 headband magnifier and 10 and
20 hand lenses. The bristles of the male’s fourth sternite were
clearly visible.
In addition, copulation behavior of both P. sp. and Pseudopalaeosepsis nigricoxa Ozerov was observed in captivity under a dissecting microscope, using flies raised in captivity from cow dung (P. sp.),
or from howler monkey dung (Alouatta palliata) on Barro Colorado
Island, Panama (P. nigricoxa). Copulating pairs of P. sp. were frozen
with ethyl chloride spray and fixed in 70% ethyl alcohol or FAA prior
to being prepared for examination with a scanning electron microscope. Drawings of specimens of these species and of Themira putris
Linn. and Nemopoda nitidula (Fallen), collected in Germany and preserved in 70% ethanol were made from preparations mounted in Euparol on microscope slides, using a camera lucida.
The nominal relations of Palaeosepsis sp. and P. nigricoxa are
not clear. Silva (1993) argued that the monotypic genus Pseudopalaeosepsis should be included in her newly erected genus Archisepsis.
Archisepsis, in turn, has classically been included in Palaeosepsis
(senus latu) (Duda 1925, 1926; also Meier 1995). The two species
thus belong to Palaeosepsis sensu latu, but the phylogenetic relations among the species in Palaeosepsis sens. lat. remain to be determined.
RESULTS
Morphology and movement of modified sternites
Palaeosepsis sp.
The fourth abdominal sternite of P. sp. is larger than the preceding sternites and has a brush of very long setae at each
posterior lateral corner (Figs. 3 and 4). The fifth sternite is
small (Fig. 4) and is hidden in an inward fold of the abdominal cuticle. The base of each brush is heavily sclerotized and
more or less circular (Fig. 4). When at rest, the long setae of
the brushes project posteriorly (Fig. 3). The cuticle of the
208
EVOLUTION & DEVELOPMENT Vol. 3, No. 3, May–June 2001
Fig. 2. Copulating pair of Sepsidimorpha sp. (A) The male (left)
grasps the lateral portions of the female’s fifth abdominal sternite
with his surstyli. (B) The thick setae on the male’s fourth abdominal sternite press forcefully against the female’s tergite.
fourth sternite just medial to the base of each brush is thin
and membranous (Figs. 3 and 4). The central portion of this
sternite is, in contrast, thicker and more rigid. Internally, the
central portion is invaginated to form a keel to which the central ends of a large bundle of muscle fibers are attached (Fig.
4). The other ends of these muscle fibers are attached to the
base of the brush. Thus, the contraction of these muscles
probably produces the ventral tapping movements of the setae that occur during copulation (below). A second, smaller
band of muscle fibers runs anteriorly from the base of the
brush to near the anterior margin of tergite 3 (Fig. 4). Contraction of these muscle fibers presumably moves the brush
anteriorly, causing the setae to project ventrally from the
male’s abdomen.
The male tapped the female’s abdomen rapidly with his
brushes in all copulating pairs of P. sp. (four in the field, four
Fig. 3. Scanning electron micrographs of Palaeosepsis sp. (A). Ventral view showing positions of male surstyli and fourth sternite
brushes at rest. (B) Lateral view of male abdomen (right) with
brush directed ventrally and contacting female abdomen during
copulation. (C) Close-up ventral view of base of brush at rest, showing thin, flexible portion of sternite proximal to base of brush.
Eberhard
Evolutionary novelties in sepsid flies
209
Fig. 4. Ventral view of fourth (sparse stippling) and fifth (dense stippling) abdominal sternites of Palaeosepsis sp. and Pseudopalaeosepsis
nigricoxa (above), and dorsal view of sternites and associated muscles of the same species.
210
EVOLUTION & DEVELOPMENT Vol. 3, No. 3, May–June 2001
in captivity). The brushes were flexed anteriorly, and the setae fanned out to assume a cupped form (Fig. 3B), and then
the brushes vibrated in an approximately dorsoventral direction an estimated 3–10 times/sec, so that the setae tapped the
sides of the female’s abdomen (Fig. 3C). In the most complete observation of a copulation, which lasted 104 min, the
brushes beat continuously on the female for at least 12 min
soon after copulation began, then became quiet. They resumed beating during six bursts of activity that lasted between about 10 and 100 sec during the next 38 min.
P. nigricoxa
The structure of the fourth abdominal sternite in P. nigricoxa
is very different. The central portion of the sternite is a thin,
transverse, dark band that is sharply pointed at either end
(Fig. 4). At each end of the central portion there is a long thin
lateral lobe, with two rows of long setae along its distal half.
The base of each lateral lobe is expanded, and the middle
portion of the base articulates with the sharp lateral point of
the central portion (Fig. 4). At rest the lateral lobes are directed posteriorly. The fifth sternite is much longer than the
fourth, and its anterior corners form small processes that extend anteriorly to nearly reach the articulation at the base of
each lateral lobe.
Internally, the fourth sternite has no keel, and there are no
muscle fibers joining the center of the sternite with the tips,
as in P. sp. Instead, there is a small internal keel on the posterior portion of sternite 5 (Fig. 4). A thin sheet of muscle fibers runs from the anterior edge of sternite 4 to sternite 5
(Fig. 4). Contraction of these fibers presumably causes the
entire central portion of the fourth sternite to rotate, and thus
move the lateral lobes anteriorly so that they are directed
ventrally (see below). A second thin sheet of muscles is attached to an invagination of the posterior margin of the fifth
sternite, and they converge in the area of the articulation at
the base of the lateral lobe (Fig. 4). Contractions of these
muscles undoubtedly move the lateral lobes.
In each of two pairs of P. nigricoxa observed while copulating, the male’s lateral lobes projected ventrally soon after intromission began, and tapped or swept repeatedly
across the female’s abdomen. In the most complete observation, the male began to tap the female 2:17 after copulation
began, moving his lateral lobes repeatedly forward so that
their long setae brushed against the posterior half of the female’s fifth abdominal tergite approximately 1.5–2 times/
sec. Tapping continued for at least 130 sec. The lateral lobes
seemed to vibrate as they swept the female. Later, the lateral
lobes were brought alongside the male’s genitalic surstyli,
and their setae tapped the female’s abdomen in this area with
an irregular rhythm about 1–3 times/sec. The lobes twisted
so the longest setae were parallel to the female’s longitudinal
axis at some times, while at others they were directed toward
her body at 20–30.
Themira putris
The strong and complex muscles associated with the lateral
lobes of T. putris (Fig. 5) indicate that the lobes in this species are also moveable. Ventral projection of the long setae
in T. putris is probably produced, at least in part, by contraction of the medium-strong band of muscles running dorsally
from the anterior margin of the sternite to tergite 4 (Fig. 5).
Medial and perhaps rotatory movements of the moveable
lobes probably also occur. Two moderate-sized bundles of
muscle fibers (A and B in Fig. 5) run from a small keel on
the central portion of sternite 4 to near the base of the long
setae of the lobe. Contraction of one of these (A), which is
attached on or near the dorsolateral surface of the internal
strut of the moveable lobe, apparently produced a rotatory
movement of the moveable lobe and the brush of setae with
respect to the central portion of sternite 4; rotation would be
around the tip of the strut (X in Fig. 5). Contraction of muscle B, which also ran dorsal to X but which was attached very
near the tip of the strut, may also produce rotation; its contraction would tend to hold the tip of the strut tight against
the point of rotation (X). The dorsal component of these rotatory effects (or posterior component, once the central portion of the sternite is rotated by the tergite muscles) would be
accentuated by the fact that muscles A and B were tightly encircled by a strong rigid band connected with the central portion of the sternite (an effect similar to that produced by the
pulley associated with the superior oblique muscles of the
human eye; Quain et al. 1842). At least some of the setae can
apparently be moved individually, as a few fibers were attached to internal extensions of the bases of at least two setae
(Fig. 5).
Sternite 5 is probably also moveable. A sheet of muscles
runs from the rear portion of sternite 5 to the posterior surface of sternite 4 (sternite 5 muscles in Fig. 5). Their contraction would cause sternite 5 to move at its articulation with
sternite 4, causing the pair of strong bristles on sternite 5 to
project more ventrally. Thus, these muscles may move the
bristles into contact with the female.
There are no descriptions of copulation behavior in
Themira, but the drawing of a copulating pair of T. ( Cheligaster) leachi (Meigen), in which the long setae of the
male’s fourth abdominal stenite are directed ventrally (Šulc
1928; see Fig. 1), indicates that the lobes of the fourth sternites are moveable.
Nemopoda nitidula
Sternite 4 and its associated muscles differed in many respects from those of the other species. The sternite’s ventral
surface was highly sculptured (Fig. 6), and dorsally a thick
keel projected inward (Fig. 6). There were two pairs of apparent lobes (A and B in Fig. 6), each of which bore an array
of long setae at its tip. The lobes on each side were connected
by strongly sclerotized cuticle, however, and probably could
Eberhard
Evolutionary novelties in sepsid flies
211
Fig. 5. Ventral and dorsal views (with muscles) of sternites 4 and 5 of a male Themira putris.
move very little relative to each other. The setae at the tip of
lobe A were thick and flattened, and formed three distinct
thick bundles. These bundles of setae were stiff when
touched. They thus contrasted with all the long setae of the
other species, which were flexible. The setae of lobe B were
thinner, rounder, and did not form bundles; aside from being
relatively shorter, they resembled the long setae of the other
species.
The musculature associated with sternite 4 was more
complex than that in the other species (Fig. 6), and was not
completely deciphered. Some muscles (X) probably caused
the distal portion of processes A and B to move laterally (to
open up), and others (V, W) probably closed them. Another
muscle band (Z) tilted sternite 4, causing the long setae to
project ventrally (as in T. putris, above). Some muscles (U, S)
were attached at both ends to the cuticle of the sternite, and
presumably caused it to flex and change shape.
Either sternite 5 was highly sculptured and more or less
fused with sternite 4 (see Fig. 6), or it was so reduced that I
could not find it. In either case, it was clear that, in contrast
to T. putris, there were no muscles that would move sternite
5 with respect to sternite 4.
212
EVOLUTION & DEVELOPMENT Vol. 3, No. 3, May–June 2001
Fig. 6. Ventral view of external surface of sternites 4 and
5 of a male Nemopoda nitidula
(above), and dorsal view of
the same sternites and their
associated muscles.
Eberhard
Modified male abdominal sternites in other sepsids
The male’s fourth abdominal sternite does not differ from
that of the female in the basal sepsid genus Orygma (Hennig 1958) (see Fig. 9)—or in the related families Sciomyzidae (Knutson 1987), Ropalomeridae (Steyskal 1987b), and
Coelopidae (Vockeroth 1987a)—so lack of sexual dimorphism
in sternite 4 is the likely plesiomorphic state for the family
Sepsidae. As is common in specialized non-genitalic contact courtship devices in many animals (Eberhard 1985),
sexually dimorphic modifications of the male sternites are
generally species-specific in form (Table 1). Thus, species
descriptions in sepsids often include drawings of male sternites, allowing an overview of the presence of the different
types of sternite modification throughout the family, though
data are lacking for some groups and many of the taxonomic drawings are not detailed enough to be used as reliable indicators of divisions between independent morphological processes (A. Pont, pers. comm., unreferenced; R.
Meier, pers. comm., unreferenced). A preliminary classification of derived, sexually dimorphic male sternite morphology includes three different types (Fig. 7), involving increas-
Evolutionary novelties in sepsid flies
213
ing degrees of apparent separation of potentially moveable
processes:
(A) Sternite shape only slightly dimorphic but posterior
setae thicker or longer (A. diversiformis, ecalcarata, and discolor in Fig. 7; Sepsis in Fig. 8). In some groups (e.g.,
Archisepsis, Microsepsis), the male’s fourth (or sometimes
third or second) sternite is more or less similar in size and
form to that of the female, but has more bristles or setae,
which are often somewhat longer than those of the female.
The modified setae usually originate on the posterior and lateral portions of the male sternite, where they are most likely
to contact the female during copulation. These setae are frequently species-specific in number and pattern of placement,
even in some groups of species such as Sepsis in which they
have not usually been employed in taxonomic descriptions
(Silva 1993) (Figs. 7 and 8);
(B) Modified setae arise on short extensions of the sternite (A. hirsutissima, T. lucida in Fig. 7). These setae are
nearly always much longer than those of type A sternites.
The sternite is extended, usually laterally and/or posteriorly,
and the long setae are nearly always inserted on the exten-
Fig. 7. Representatives of different types of secondary sexual modification of fourth abdominal sternites in Sepsidae
(all males unless otherwise
specified) (at different scales):
unmodified fourth abdominal sternite of female Archisepsis diversiformis Ozerov);
Type A. Sternite form little
modified, with species-specific
array of larger setae on posterior portion (Archisepsis diversiformis, ecalcarata, and A.
discolor); Type B. Elongate
setae originating on extensions of the sternite, which is
a single unit (A. hirsutisima
Silva, Themira lucida Staeger);
Type C. One or several independent sclerites at each end
of the sternite (Palaeosepsis
maculata Silva, T. superba Haliday, T. germanica Duda, A.
muricata Silva). (after Silva
1993 and Hennig 1949).
214
EVOLUTION & DEVELOPMENT Vol. 3, No. 3, May–June 2001
Fig. 8. Male and female sternites in different species of
Sepsis, illustrating differences
between males and females,
and the relatively greater interspecific differences between
males. All male fifth sternites
(sternites 4 are absent) are
type A.
sion. In some species, the cuticle in an area of the sternite between each extended corner and the rest is thinner (Fig. 3C);
(C) Separate lateral lobes that bear long setae (P. maculata, T. superba and germanica, A. muricata in Fig. 7). In
some species, there are one or more sclerites that are distinct
from the central portion of the sternite, and in at least some
cases they are separated from it by membranes (T. germanica). The drawings of some species do not allow distinction
of additional sclerites from an extension of the sternite with
an intervening thinner band of cuticle (e.g., Fig. 3C). In some
cases, however, asymmetrical positions of the lobes provide
direct evidence that the lobe can move with respect to the
other sclerites (A. muricata in Fig. 7).
DISCUSSION
Developmental constraints
The designs for moving the sternal lobes of Palaeosepsis sp.
and P. nigricoxa are very different, so it is likely that this
mobility has evolved independently. Both the ventral movement of the brush of long setae, which brings it into position
to tap the female, and the actual tapping movements are produced by novel muscles with substantially different points of
origin and insertion. In both Themira and Nemopoda ventral
movements of the brushes (a movement that has been confirmed by direct observation only in Themira—Fig. 1, Šulc
1928) are at least in part due to a set of muscles not seen in
the other species that attached at one end to tergite 4 and at
the other to the anterior portion of sternite 4. This suggests at
least one more independent derivation. Medial movements
of the long setae in Themira probably involve rotation around
a point at the base of the brush (X in Fig. 5). The sternite of
Nemopoda, in contrast, seems to have two different pairs of
lobes, which have more limited movement as a unit. Some
muscles apparently move portions of the sternite indirectly
by bending the cuticle, something not seen in the other three
genera. The complex ventral surface of the central portion of
the sternite suggests that it is pressed against the female.
There is at present no clear consensus regarding the phylogenetic relationships within Sepsidae. The one published
tree, based on larval characters (Meier 1995) (Fig. 9), has
some important disjunctions with a second, preliminary tree
based on adult characters (A. Pont and R. Meier, pers.
comm., unreferenced). Thus, it is not possible to confidently
trace all details of the probable evolution of abdominal processes within the family. It is also clear, however, from the
data in Table 1 that the moveable lobes documented here are
not unique within the family. The complexity of the musculature associated with the lobes of Themira and Nemopoda,
combined with the apparently different setal bases of T. putris, and the consistently basal position of Themira and derived position of Palaeosepsis sensu latu in trees using both
larva and adult characters (Fig. 9; R. Meier, pers. comm., unreferenced), suggest a total of at least three derivations of
moveable abdominal lobes.
The male sternites of P. sp. and P. nigricoxa suggest that
the early stages in the evolution of a moveable abdominal appendage are surprisingly easy to produce. A new cuticular
sclerite that articulates with a pre-existing sclerite can result
from nothing more than a thinning of an intermediate area of
a pre-existing sternite (e.g., Fig. 3C). Muscles to move the
Evolutionary novelties in sepsid flies
Eberhard
215
Table 1. Types of male sternites IV in sepsid flies. N denotes no sexual dimorphism; other categories are
described in the text, and in Fig. 7. Data are from taxonomic drawings, and interpretations are
subject to limitations discussed in the text. Species-specificity judged on basis of differences
between congeneric species. (WGE W. Eberhard, unpublished data)
SPECIES
Orygma luctuosum Meigen
Paratoxopoda depilis Wlkr.
crassiforceps Duda
akuminambili
akuminamoya
amonane
angolica
asaba
asita
baebata
depilis (Walker)
dudai Ozerov
frontalis Ozerov
kilinderensis Vanschuytbroeck
magna Ozerov
pilifemorata Soos
saegeri Vanschuytbroeck
similis Ozerov
straeleni Vanschuytbroeck
tenebrica Ozerov
tricolor (Walker)
villicoxa Duda
zuskai Ozerov
Themira
subgenus Enicita
annulipes Meigen
annulipes (Meigen)
bispinosa Melander and Spuler
mexicana Ozeov
subgenus Annamira
leachi (Meigen)
japonica Ozerov
notmani Curran
subgenus Enicomira
minor (Haliday)
kanoi Iwasa
paludosa Elberg
sabulicola Ozerov
subgenus Nadezhdamira
superba (Haliday)
pusilla (Zetterstedt)
latitarsata Melander and Spuler
malformans Melander and
Spuler
subgenus Themira
gracilis (Zetteerstedt)
nigricornis Meigen
putris Linn.
lucida Staeger
(athabasca Mangan)
germanica Duda
seticrus Duda
arctica Becker (dampfi
Becker)
biloba Andersson
bifida Zuska
flavicoxa Melander and Spuler
SEXUAL DIMORPHISM
TYPE
SPECIES-SPECIF.?
none
lobe?, mod. setae
more or less bare
v short setae st.5*
med setae st.5*
m-s setae st.5*
med setae thick st.5*
med set med st.5*
med setae fine st.5*
med set fine st.5*
med set fine st.5*
m-l setae strong st.5*
m-l setae strong st. 5*
med setae fine st.5*
m-s setae strong st.5*
s setae fine st.5*
m setae med thick st.5*
m set fine st.5*
m-l setae strong st.5*
m-l setae strong st.5*
m-l setae strong st.5*
m-s setae strong st.5*
m-s setae fine*
N
A/B?
A?
—
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Hennig 1958
Duda 1926
Duda 1926
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
Ozerov 1993
long setae
long setae
long setae (2 spines st.5)
long setae
B?
B/C
B
C
Y#
Y
Y
Y
Duda 1925
Pont 1979, Ozerov 1998a
Ozerov 1998a
Ozerov 1998a
long setae & keel
long setae plus keel
almost no setae!
C
B?
A
Y
Y
Y
Šulc 1928, Pont 1979, Ozerov 1998a
Ozerov 1998a
Ozerov 1998a
long setae §
long setae long setae
long setae
long setae (not on lobe!)
C
C
A/B
B/C
B
Y
Y
Y
Y
Y
Pont 1979, Ozerov 1998a
Hennig 1949, Ozerov 1998a
Ozerov 1998a
Ozerov 1998a
Ozerov 1998a
long setae
long setae §?
long setae
C
C
C
Y
Y
Y
Pont 1979, Ozerov 1998a
Pont 1979, Duda 1925, Ozerov 1998a
Ozerov 1998a
long setae
C
Y
Ozerov 1998a
long setae
mod. long setae¶
long setae
long setae
C
B
C
B
Y
Y
Y
Y
long setae §
long setae
C
B
Y
Y
Pont 1979, Ozerov 1998a
Pont 1979, Hennig 1949, Ozerov 1998a
Pont 1979, Duda 1925, Ozerov 1998a
Pont 1979, Duda 1925, Mangan 1976,
Hennig 1949, Ozerov 1998a
Pont 1979, Hennig 1949, Ozerov 1998a
Hennig 1949, Ozerov 1998a
long setae
long setae
long setae
long setae
C
Y
Y
Y
Y
Duda 1925, Ozerov 1998a
Ozerov 1998a
Ozerov 1998a
Ozerov 1998a
B
B
REF
Continued
216
EVOLUTION & DEVELOPMENT Vol. 3, No. 3, May–June 2001
Table 1. Continued
SPECIES
SEXUAL DIMORPHISM
TYPE
SPECIES-SPECIF.?
lutulenta Ozerov
mikiharai Iwasa
mesopleuralis Iwasa
mongolica Soos
saigusai Iwasa
shimai Iwasa
Susanomira caucasica Pont
short setae
short setae
long setae
long setae
long setae
long setae
long setae sternite 3 and
tergites 4,5 (sternite 4
not visible)
short setae
B
N/A
A
B
C
B
B
Y
Y
Y
Y
Y
Y
*
mod. setae
lobe, mod. long setae
lobe, mod. setae
lobe, mod. long setae
no modifications
lobe, short/long setae †
lobe, short/long setae †
lobe, short/long setae †
lobe, mod. short setae
A
C
C
C
N
C
C
C
C
?
Y
Y
Y
Y
Y
Y
Y
Y
Hennig 1949
Duda 1925, Zuska 1964
Duda 1925, Zuska 1964
Zuska 1964
Silva 1990
Zuska 1972
Zuska 1972
Zuska 1972
Hennig 1949
two parts, nearly no modif.
Long setae
Long setae
med-short setae
med-long setae
few, short setae
med long setae
med-long setae (Forked)
short setae
med-short setae
A?B?
B
C?
C?
B (nearly C)
C
B
B/C
A
B
Y
Y
Y
Y
Y
Y
Y
Y
Y
Ozerov 1999b
Ozerov 1999b
Ozerov 1999b
Ozerov 1999b
Ozerov 1999b
Ozerov 1999b
Ozerov 1999b
Ozerov 1999b
Ozerov 1999b
Ozerov 1999b
long setae
C
Y
Ozerov 1999b
long setae
short lobe, short setae
B
Y
Ozerov 1999b
lobe(?), mod. setae
lobe, long setae
lobe, long setae
lobe, long setae
lobe, long setae
lobe, long setae
short setae
mod. short setae
short setae
lobe, long setae
lobe, mod. long setae
short setae
short setae
short setae
lobe, long setae
lobe, long setae ¶
short setae
mod. setae
mod. setae
mod. setae
lobe, long setae
B?
B
C
B
B
B
A
A
A
B
B
A
A
A
B/C
C
A
A
A
A
C
*
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
*
Duda 1926
Silva 1993
Silva 1993
Silva 1993
Silva 1993
Silva 1991, 1993
Silva 1993
Silva 1993
Silva 1993, WGE
WGE
Silva 1993
Silva 1993
Ozerov 1993
Silva 1993
Silva 1993
Silva 1993
Silva 1993
Ozerov 1993
WGE
Ozerov 1993, WGE
Ozerov 1992a
short setae
A
Y
Silva 1993
Decachaetophora
aeneipes de Meijere
Saltella sphondylii Shrank
Nemopoda pectinulata Loew
nitidula (Fallen) (cylindrica)
speiseri Duda
Meroplius albuquerquei Silva
beckeri (Meijere)
sauteri (Meijere)
fasciculatus (Brun.)
minutus Wiedemann
( stercorarius Rob.-Desv.)
subgenus Meroplius
bispinifer Ozerov
africanus
trispinifer Ozerov
unispinifer Ozerov
hastifer Seguy
hastiferoides Ozerov
latispinifer Ozerov
madagascarensis Iwasa
pallidispinifer Ozerov
unispinifer Ozerov
subgenus Protomeroplius
trispinifer Ozerov
subgenus Xenosepsis
africanus Ozerov
sydneyensis
(Pseudomeroplius
acrosticalis Duda
Palaeosepsis chauliobrechma Silva
maculata (Duda)
dentata (Becker)
dentatiformis (Duda)
erythromyrma Silva
insularis (Williston)
laticornis (Duda)
pusio (Schiner)
n. sp.
Archisepsis hirsutisima Silva
armata (Schiner)
diversiformis (Ozerov)
excavata (Duda)
mirifica Silva
muricata Silva
priapus Silva
polychaeta
pleuralis (Coquillett)
discolor (Bigot) ( scabra)
Pseudopalaeosepsis
nigricoxa Ozerov
Microsepsis anomala Silva
A
REF
Ozerov 1998a
Ozerov 1998a
Ozerov 1998a
Ozerov 1998a
Ozerov 1998a
Ozerov 1998a
Pont 1987, pers. comm.
Hennig 1949
Continued
Evolutionary novelties in sepsid flies
Eberhard
217
Table 1. Continued
SPECIES
SEXUAL DIMORPHISM
TYPE
SPECIES-SPECIF.?
REF
armillata (Melander and Spuler)
furcata (Melander and Spuler)
inflexa (Becker)
mitis (Curran)
mystrion Silva
simplicula (Steyskal)
stenoptera Silva
eberhardi Ozerov
Sepsidimorphar¶¶ duplicata
(pilipes) (Wulp)
setulosa Duda§§
secunda
Nicarao rarus Silva
Dicranosepsis transita Ozerov
Sepsis tuberculata Duda
neocynipsea
duplicata
thoracica
punctum
cynipsea
alanica
Palaeosepsioides
grimaldii Ozerov
Zuskamira inexpectata Pont
lobe, mod. long setae
short setae
lobe, mod. setae
short setae
short setae **
lobe, mod. long setae
short setae
lobe, mod setae
B/C
A
A/B
A
A/B
B
A
B
Y
Y
Y
Y
Y
Y
Y
Y
Silva 1993, Duda 1925
Silva 1993 WGE
Silva 1993
Silva 1993
Silva 1993
Silva 1993
Silva 1993
Ozerov 1997, WGE
mod. setae on 3 and 5
mod. setae on 3 only
mod setae on 4 only
short setae
med setae
no*
short setae
short setae
short setae
short setae
short setae
short setae
A?
N
A
A?
A
Y
Y
Y
*
?
N?
A
A
A
A
A
A
Y
Y
Y
More or less Y
Y More/less
Duda 1925, Hennig 1949
Duda 1925
WGE
Silva 1995
Ozerov 1996
Duda 1926
WGE
WGE
WGE
WGE
WGE
Ozerov 1998b
long setae ‡‡
long setae, short
setae central area
hairy
very long and
elaborate, no setae
long setae, prob. keel
lobe, mod. setae
short setae
med long setae
Few mod long setae
One mod long seta
two long setae
long setae
long setae
long setae
C
*
Ozerov 1992
C
*
Pont 1987
Duda 1926
C?
B
B
A
B
A/B
B
B
B
B/C
C
Y
Y
Duda 1926
Ozerov 1992b
Silva 1992
Ozerov 1995
Ozerov 1999a
Ozerov 1999a
Ozerov 1999a
Ozerov 1999a
Ozerov 1999a
Ozerov 1995
Ozerov 1995
Parameroplius fasciculata Brun.
Perochaeta orientalis de Meijere
hennigi Ozerov
Meropliosepsis sexsetosa Duda
Dudamira abyssinica Duda
Afrosepsis sublataralis Vanschuytbroeck
camerounica Ozerov
quadrimaculata Ozerov
elongata Ozerov
lineata
Afromeroplius semlikiensis Vanschuytbroeck
watalingaensis Vanschuytbroeck
Y
Y
Y
Y
Y
Y
Y
* male tergite modified, may contact female
†
verbal description without drawings
‡
monotypic genus
#
varies between subspecies
§
additional sclerites at base of lobe
¶
asymmetrical positions in drawing suggest lobes are moveable
membrane at base of lobe suggest lobes are moveable
** drawing of Šulc show that setae touch female during copulation
††
extension of sternite without bristles, though others near its base
‡‡
apparent articulation base of lobe with central portion of sternite
§§
species dubia, known only from male; may be the same as Sepsis flavimana - A. Pont, pers. comm.
¶¶
This genus is often included in Sepsis; the sexual behavior of one species is, however, quite distinct.
sternite 4 is absent
new sclerite or lobe are probably recruited from the thin
sheets of muscle fibers that are attached to the abdominal
sternites and membranes of other segments. Such muscles
are associated with the sternites of other abdominal segments
in males and females of these and other species of sepsids
(Fig. 10), and indeed in many other insects (Snodgrass 1935,
1956; Birket-Smith 1984; Chapman 1999). The lack of sym-
metry in form and attachment sites of the muscles in Figure
10 suggests ample variation in the placement of these muscles in sepsids, which could be the starting point for selection
favoring modified morphology that allowed movement of
incipient sternal lobes.
Recruitment of nearby muscles for new functions is probably widespread in insects. Pass (2000) showed, using inner-
218
EVOLUTION & DEVELOPMENT Vol. 3, No. 3, May–June 2001
Fig. 9. Cladogram based on
larval characters of relations
between genera and species
for which information is available on male abdominal sternite form (after Meier 1995).
Letters refer to types of sternite (see text and Fig. 7).
vation and microstructure to determine homologies, that in
the formation of peripheral hemolymph pumps (”peripheral
hearts”), “any [nearby] muscle system is liable to become a
component of a [peripheral] circulatory pump” (Pass 2000).
Developmentally, myoblasts could move into areas where
re-patterning of the epidermis had already occurred (Gerhardt and Kirschner 1997). The possible recruitment of more
basic appendage producing mechanisms, such as distal-less
found in many animal groups (Panganiban et al. 1997), remains to be tested.
The repeated evolution of moveable abdominal lobes in
sepsids contrasts sharply with the lack of such structures in
other flies in the general taxonomic vicinity. For instance,
the book of McAlpine et al. (1987) illustrates sexually dimorphic modifications of the ventral surface of the male’s
abdomen in only 14 of the other 63 muscomorph families
(Table 2). Although their coverage is undoubtedly incomplete, it is clear that in some large families such as Phoridae
(B. Brown, pers. comm., unreferenced) and Drosophilidae,
such structures are apparently unknown: “To my knowledge,
there are no drosophilids where sternites have become fragmented. . .” (D. Grimaldi, pers. comm., unreferenced). In only
Rhinotoridae and Nycteribiidae do the descriptions or figures of McAlpine et al. (1987) suggest moveable lobes like
those of sepsids. To the best of my knowledge there are no
studies of copulatory behavior in either of these small families, which are very distantly related to Sepsidae and to each
other, or dissections to check for muscles that would allow
conclusions regarding the possibility that the lobes can be
moved independently.
The moveable abdominal lobes of sepsids illustrate the potential trap of supposing that phylogenetic uniformity implies
developmental constraints against alternative designs (Müller
and Wagner 1991). The moveable lateral lobes of male
sepsids fit many definitions of a novel trait (Müller and Wagner 1991), and the widespread absence of such structures in
other Diptera might suggest that they are developmentally
difficult to evolve. On the contrary, however, the observations reported here suggest that moveable lobes are developmentally easy to evolve. The abdomens of male sepsids with
moveable lobes are not obviously reorganized with respect to
those of conspecific females in other respects. A seemingly
more likely explanation of the absence of moveable processes
in other flies is that they have not been selectively advantageous; that is, there have been no courtship interactions of
comparable importance under sexual selection that favor
morphological innovation of this kind in males. This hypothesis is discussed further in the next section.
Why sepsids?
Why should it be that male sepsids have repeatedly evolved
the otherwise extremely rare trait of moveable nongenitalic
abdominal structures? A possible answer is suggested by the
link established in this study between the sternal lobes and
stimulation of the female during copulation, and thus the
probability that the lobes are under sexual selection. There
are two indications that female sepsids may have an otherwise unusual ability to sense stimuli from the male’s sternites during copulation. The genital morphology of female
sepsids is unusual among other flies in that the hypoproct
and cerci are displaced to a more dorsal position, and are thus
more exposed to the ventral surface of the mounted male
(Hennig 1949; Pont 1979). The hypoproct and cerci seem
likely to be relatively rich in sensory organs compared with
the usual dorsal structures of the ovipositor in other flies and
thus predispose females to be sensitive to male stimuli (R.
Eberhard
Meier, pers. comm., unreferenced). Another possibly contributing factor is that sepsids (other than Orygma, Pont
1979; Steyskal 1987a) are also unusual in lacking strong setae on the dorsal surface of the abdomen; this could allow
more intimate contact between the male’s ventral surface
and the female.
It seems inevitable that the sensory capabilities of females
will often have important evolutionary consequences for the
evolution of new male traits under sexual selection by female choice, because only those stimuli that a female can
sense can be expected to induce favorable female responses
Evolutionary novelties in sepsid flies
219
(West-Eberhard 1984; Andersson 1994; Ryan 1990). As a
result, when females evolve to use a particular male signal as
a mate choice criterion (to respond to it in a way that favors
the reproductive success of the male), the likelihood that additional male stimuli in that particular modality will be able
to elicit improved female responses probably often increases. In addition, female use of a particular type of stimuli
to filter males will often result in selection on females that favors an increase in female ability to discriminate among such
stimuli, through either modification of her sense organs or
changes at higher levels in her CNS. In other words, a “sen-
Fig. 10. Dorsal view of longitudinal and transverse muscles near the ventral abdominal wall of segments 4–6 of
a female Archisepsis diversiformis (tranverse muscles on
folded intersegmental membrane are omitted for clarity).
220
EVOLUTION & DEVELOPMENT Vol. 3, No. 3, May–June 2001
Table 2. Sexual dimorphism form and setation of male abdominal sternite structure reported or illustrated in
muscomorphan flies in 14 families in McAlpine et al. (1987). In the other 49 families there was no
indication of sexual dimorphism in abdominal sternites
Family
Micropezidae
Conopidae
Syrphidae
Lauxaniidae
Rhinotoridae
Sphaeroceridae
Scathophagidae
Anthomyiidae
Muscidae
Calliphoridae
Sarcophagidae
Tachinidae
Hippoboscidae
Nycteribiidae
Structure
Ref.
forceps-like extensions (frequent)
short spines and setae (frequent)
tubercles and keels (rare)
various modifications (some)
lobes on post-lat margins (some)
modified as genital pouch (frequent)
modified distinctive setae (some)
bilobate posteriorly
some very elaborate
strongly bilobate
bilobate
apical cleft
some with pair of sclerites
comb-like rows of spines, some with
postero-lateral lobes with spines
Steyskal 1987c
Smith and Peterson 1987
Vockeroth and Thompson 1987
Shewell 1987a
McAlpine 1987
Marshall and Richards 1987
Vockeroth 1987b
Huckett 1987
Huckett and Vockeroth 1987
Shewell 1987b
Shewell 1987c
Wood 1987
Maa and Peterson 1987
Peterson and Wenzel 1987
sory focus” by the female on some particular subset of stimuli, which is probably a widespread trait among insects (Bernays and Wcislo 1994), can have consequences for the
evolution male display traits. If the females of a species are
focusing one particular type of stimuli, then modifying or
elaborating these stimuli is especially likely to be advantageous for males (see also Wiley and Poston 1996).
This phylogenetic inertia argument regarding female sensory modes suggests that once female sepsids began to use
stimuli from the ventral surface of the male’s abdomen to cue
their reproductive decisions, the likelihood that a male could
further increase his chances of fertilizing eggs by further or
more effective stimulation of the female’s abdomen increases.
The probable relatively early origin of this female response in
sepsids (Table 1, Fig. 9) suggests that male sepsids have had a
relatively long evolutionary time to evolve novel mechanisms
with which to produce such stimuli. In the sense of Saether
(1979), female use of stimuli from the posterior portion of the
male’s abdomen to screen mates may have been an underlying
synapomorphy that has given male sepsids the evolutionary
tendency to evolve moveable lateral lobes on the abdomen.
Henry et al. (1999) mention a similar convergence in the mating songs of lacewing insects.
This argument suggests that a modification of the anatomy of the posterior portion of the abdomen of female
sepsids may have led to the evolution of the novel moveable
abdominal lobes in males. But the logic differs from that of
hypotheses based on developmental constraints. The claim is
not that modification of the female was necessary in overcoming developmental limitations in males, but rather that it
provided a new selective context in which such cuticular
variants were advantageous.
Evolutionary innovation in structures that are probably
under sexual selection also occurs in other structures in
Diptera. In particular, male genitalic structures are extremely
diverse; some structures have become divided and moveable, new points of articulation and muscles have arisen, new
sclerites have arisen from membranes, others have fused,
etc. (see Wood 1991, Sinclair et al. 1994, and Cumming et
al. 1995 for general reviews of the evolution of dipteran genitalia; Eberhard 2001 in press, for two new articulations in
the sepsid genus Microsepsis, for one of which there are behavioral data that strongly suggest a stimulatory function).
The evolution of the male abdominal sternal lobes in Sepsidae
may represent in miniature the evolution of male genitalia in
Diptera. Stimulation of the female by the male’s genitalia is
an almost inevitable consequence of internal insemination,
and cuing of female reproductive processes on these stimuli
is probably widespread (Eberhard 1985, 1996). Female responses to such stimuli have been demonstrated experimentally in flies of the families Glossinidae (Leegwater-van der
Linden and Tiggelman 1984), and Dryomyzidae (Otronen
1990; Otronen and Siva-Jothy 1991), and may also occur in
Drosophilidae (Coyne 1993). Sustained sexual selection on
males to stimulate females with their genitalia may thus have
resulted in the extraordinary evolutionary inventiveness seen
in male genitalic structures.
Acknowledgments
I thank Katja Schulz for kindly sending me specimens; Maribelle
Vargas for outstanding production of SEM images; Axel Retana,
David Wahl, and Andy Bennett for advice with regard to cladistic
analyses; and Rudolf Meier, Adrian Pont, and Mary Jane WestEberhard for comments on a preliminary version of the manuscript.
Financial support was provided by the Smithsonian Tropical Research Institute and the Vicerrectoría de Investigación of the Universidad de Costa Rica. Note added in proof: Andrej Ozerov kindly
identified the Palaeosepsis species of this study as dentatiformis
(Duda).
Eberhard
REFERENCES
Andersson, M. 1994. Sexual Selection. Princeton University Press, Princeton, NJ.
Bernays, E. A., and Wcislo, W. T. 1994. Sensory capabilities, information
processing, andresource specialization. Quart. Rev. Biol. 69: 187–204.
Birket-Smith, S. J. 1984. Prolegs, legs and wings of insects. Entomonograph
5: 1–128.
Chapman, R. F. 1999. The insects structure and function. Cambridge University Press, Cambridge.
Coyne, J. 1993. The genetics of an isolating mechanism between two sibling
species of Drosophila. Evolution 47: 778–788.
Cumming, J. M., Sinclair, B. J., and Wood, D. M. 1995. Homology and phylogenetic implications of male genitalia in Diptera - Eremoneura. Ent.
Scand. 26: 120–151.
Duda, O. 1925. Monographie der Sepsiden (Dipt.) I. Ann. Naturhist. Mus.
Wien. 39: 1–153.
Duda, O. 1926. Monographie der Sepsiden (Dipt.) II. Ann. Naturhist. Mus.
Wien. 40: 1–108.
Eberhard, W. G. 1985. Sexual Selection and Animal Genitalia. Harvard
University Press, Cambridge, MA.
Eberhard, W. G. 1996. Female Control: Sexual Selection by Cryptic Female
Choice. Princeton University Press, Princeton, NJ.
Eberhard, W. G. 2001. Species-specific genitalic copulatory courtship in
sepsid flies (Diptera: sepsidae). Evolution 55: 93–102.
Eberhard, W. G., and Pereira, F. 1996. Functional morphology of male
genitalic surstyli in the dungflies Archisepsis diversiformis and A. ecalcarata (Diptera: sepsidae). J. Kans. Ent. Soc. 69 suppl.: 43–60.
Gerhardt, J., and Kirschner, M. 1997. Cells, Embryos and Evolution. Blackwell Science,Malden, MA.
Hennig, W. 1949. Sepsidae. In E. Lindner (ed.). Die Fliegen der Palaearktischen Region. E. Schweizerbart’sche Verlagsbuchhandlung (Erwin
Nagele), Stuttgart, Germany, pp. 1–91.
Hennig, W. 1958. Die Familien der Diptera Schizophora ud ihre phylogenetischen Verwandtschaftsbeziehungen. Beit. Entomol. 8: 505–689.
Henry, C. S., Martinez Wells, M. L., and Simon, C. M. 1999. Convergent
evolution of courtship songs among cryptic species of the carnea group
of green lacewings (Neuroptera: chrysopidae: Chyrsoperla). Evolution
53: 1165–1179.
Huckett, H. C. 1987. Anthomyiidae. In J. F. McAlpine, B. V. Peterson,
G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.).
Manual of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 1099–1114.
Huckett, H. C., and Vockeroth, J. R. 1987. Muscidae. In J. F. McAlpine,
B. V. Peterson, G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M.
Wood (eds.). Manual of Nearctic Diptera, Vol 2. Monogr. Research
Branch Agriculture Canada, Ottawa, pp. 1130–1146.
Knutson, L. 1987. Sciomyzidae. In J. F. McAlpine, B. V. Peterson, G. E.
Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.). Manual
of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 927–940.
Leegwater-van der Linden, M. E., and Tiggelman, E. P. M. 1984. Multiple
mating and inseminating potential of Glossina pallidipes. Ent. Exp. Appl. 35: 283–294.
Maa, T. C., and Peterson, B. V. 1987. Hippoboscidae. In J. F. McAlpine,
B. V. Peterson, G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M.
Wood (eds.). Manual of Nearctic Diptera, Vol 2. Monogr. Research
Branch Agriculture Canada, Ottawa, pp. 1271–1292.
Mangan, R. L. 1976. Themira athabasca n. sp. (Diptera: sepsidae) with a revised key to North American Themira and notes on the sexual morphology of sympatric species. Ann. Ent. Soc. Am. 69: 1024–1028.
Marshall, S. A., and Richards, O. W. 1987. Sphaeroceridae. In J. F.
McAlpine, B. V. Peterson, G. E. Shewell, H. J. Teskey, J. R. Vockeroth,
and D. M. Wood (eds.). Manual of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 993–1006.
McAlpine, J. F. 1989. Phylogeny and classification of the Muscomorpha. In
J. F. McAlpine and D. M. Wood (eds.). Manual of Nearctic Diptera, Vol.
3. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 1397–
1518.
McAlpine, J. F. 1987. Rhinotoridae. In J. F. McAlpine, B. V. Peterson,
G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.).
Evolutionary novelties in sepsid flies
221
Manual of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 989–992.
McAlpine J. F., Peterson, B. V., Shewell, G. E., Teskey, H. J., Vockeroth,
J. R., and Wood, D. M. 1987. Manual of Nearctic Diptera, Vol 2.
Monogr. Research Branch Agriculture Canada, Ottawa.
Meier, R. 1995. Cladistic analysis of the Sepsidae (Cyclorrhapha: Diptera)
based on a comparative scanning electron microscopic study of larvae.
Syst. Ent. 20: 99–128.
Müller, G. B., and Wagner, G. P. 1991. Novelty in evolution: restructuring
the concept. Ann. Rev. Ecol. Syst. 22: 229–256.
Otronen, M. 1990. Mating behavior and sperm competition in the fly, Dryomyzaq anilis. Behav. Ecol. Sociobiol. 26: 349–356.
Otronen, M., and Siva-Jothy, M. 1991. The effect of postcopulatory male
behaviour on ejaculate distribution within the female sperm storage organs of the fly, Dryomyza anilis (Diptera: dryomyzidae). Behav. Ecol.
Sociobiol. 29: 33–37.
Ozerov, A. L. 1990. New data on the fauna and taxonomy of the African
dipterans of the family Sepsidae (Diptera). Vestn. zool. 2: 15–20.
Ozerov, A. L. 1992a. New data on the neotropical sepsids (Diptera:
sepsidae). Russ. Ent. J. 1: 81–86.
Ozerov, A. L. 1992b. On the taxonomy of flies of the family Sepsidae
(Diptera). Bull. Moscow Soc. Nat., Biol. Ser. 97: 44–47.
Ozerov, A. L. 1993. Six new species of the genus Palaeosepsis Duda
(Diptera: sepsidae). Russ. Ent. J. 2: 63–71.
Ozerov, A. L. 1995. To the fauna and taxonomy of African Sepsidae
(Diptera). Russ. Ent. J. 4: 127–144.
Ozerov, A. L. 1996. A revision of the genus Dicranopsis Duda, 1926
(Diptera, Sepsidae). Russ. Ent. J. 5: 135–161.
Ozerov, A. L. 1997. Two new species of Sepsidae (Diptera). Russ. Ent. J. 6:
83–85.
Ozerov, A. L. 1998a. A review of the genus Themira Robineau-Desvoidy,
1830 (Diptera: sepsidae of the world, with a revision of the North American species. Russ. Ent. J. 7: 169–208.
Ozerov, A. L. 1998b. A new species of the genus Sepsis Fallén (Diptera:
sepsidae) from North Ossetia. Russ. Ent. J. 7: 57–58.
Ozerov, A. L. 1999a. Studies of Afrotropical Sepsidae (Diptera). I. A revision of the genus Afrosepsis Ozerov. Int. J. Dipterol. Res. 10: 59–96.
Ozerov, A. L. 1999b. Two species of Sepsidae (Diptera) described by J. C. H.
de Meijere. Russ. Ent. J. 8: 51.
Panganiban, G., Irvine, S. M., Lowe, C., Roehl, H., Corley, L. S., Sherbon,
B., et al. 1997. The origin of animal appendages. Proc. Nat’l. Acad. Sci.
USA 94: 5162–5166.
Parker, G. A. 1972. Reproductive behaviour of Sepsis cynipsea (L.)
(Diptera: sepsidae). I. Preliminary analysis of the reproductive strategy
and its associated behaviour patterns. Behaviour 41: 172–206.
Pass, G. 2000. Accessory pulsatile organs: evolutionary innovations in insects. Ann. Rev. Entomol. 45: 495–518.
Peterson, B. V., and Wenzel, R. L. 1987. Nycteribiidae. In J. F. McAlpine,
B. V. Peterson, G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M.
Wood (eds.). Manual of Nearctic Diptera, Vol 2. Monogr. Research
Branch Agriculture Canada, Ottawa, pp. 1283–1292.
Pont, A. C. 1979. Sepsidae. Diptera Cyclorrhapha Acalyptrata. Handbook
for the Identification of British Insects 10, 5(c): 1–35.
Pont, A. C. 1987. Two new genera of West Palaearctic Sepsidae (Diptera).
Ent. Scandinav. 18: 265–272.
Quain, J., Wilson, W. J. E., and Pancoast, J. 1842. A Series of Anatomical
Plates; With References and Physiological Comments Illustrating the
Structures of Different Parts of the Human Body. Philadelphia: Carey
and Hart, Chestnut Street, for G. N. Loomis.
Ryan, M. J. 1990. Sexual selection, sensory systems, and sensory exploitation. Oxford Surv. Evol. Biol. 7: 157–195.
Saether, O. A. 1979. Underlying synapomorphies and anagenetic analysis.
Zool. Scripta 8: 305–312.
Schulz, K. 1999. The evolution of mating systems in black scavenger flies
(Diptera: sepsidae). PhD thesis, Univeristy of Arizona, Tucson, pp. 1–200.
Shewell, G. E. 1987a. Lauxaniidae. In J. F. McAlpine, B. V. Peterson, G. E.
Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.). Manual
of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 951–964.
Shewell, G. E. 1987b. Calliphoridae. In J. F. McAlpine, B. V. Peterson,
G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.).
222
EVOLUTION & DEVELOPMENT Vol. 3, No. 3, May–June 2001
Manual of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 1133–1146.
Shewell, G. E. 1987c. Sarcophagidae. In J. F. McAlpine, B. V. Peterson,
G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.).
Manual of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 1159–1186.
Silva, V. C. 1990. Revision of the family Sepsidae of the Neotropical region. I. The genus Meroplius Rondani (Diptera, Schizophora). Revta.
Bras. Ent. 34: 709–711.
Silva, V. C. 1991. Levantamento preliminar de Sepsidae (Diptera, Schizophora) em Roraima, projeto Maraca, com descricao de uma especie
nova. Acta Amazonica 21: 369–374.
Silva, V. C. 1992. Revision of the family Sepsidae of the Neotropical region. II. The genus Meropliosepsis Duda, 1926 (Diptera, Schizophora).
Revta. Bras. Ent. 36: 549–552.
Silva, V. C. 1993. Revisao da familia Sepsidae na regiao Neotropical. III.
Os generos Palaeosepsis Duda, 1926, Archisepsis genn. n. e Microsepsis
genn. n.; chave para os generos neotropicais (Diptera, Schizophora).
Iheringia, Ser. Zool. Porto Alegre 75: 117–170.
Silva, V. C. 1995. A new genus of Sepsidae (Diptera, Schizophora) from
Nicaragua. Stud. Dipt. 2: 203–206.
Sinclair, B. J., Cumming, J. M., and Wood, D. M. 1994. Homology and phylogenetic implications of male genitalia in Diptera - Lower Brachycera.
Ent. Scand. 24: 407–432.
Smith, K. G. V, and Peterson, B. V. 1987. Conopidae. In J. F. McAlpine,
B. V. Peterson, G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M.
Wood (eds.). Manual of Nearctic Diptera, Vol 2. Monogr. Research
Branch Agriculture Canada, Ottawa, pp. 749–756.
Snodgrass, R. E. 1935. Principles of Insect Morphology. McGraw-Hill, New
York.
Snodgrass, R. E. 1956. Anatomy of the Honey Bee. Comstock Publishing
Association, Ithaca, NY.
Steyskal, G. C. 1987a. Sepsidae. In J. F. McAlpine, B. V. Peterson, G. E.
Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.). Manual
of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 945–950.
Steyskal, G. C. 1987b. Ropalomeridae. In J. F. McAlpine, B. V. Peterson,
G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.).
Manual of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 941–944.
Steyskal, G. C. 1987c. Micropezidae. In J. F. McAlpine, B. V. Peterson,
G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.).
Manual of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 756–761.
Šulc, K. 1928. Biologische Bedeutung der Bewaffnung der männlichen
Voerderfusse bei den Sepsiden (Muscidae). Biol. Spisy Vysoké Š koly
Zvéroleka_ské Brno, sr. 7: 181–194.
Vockeroth, J. R. 1987a. Coelopidae. In J. F. McAlpine, B. V. Peterson, G.
E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.). Manual of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture
Canada, Ottawa, pp. 919–922.
Vockeroth, J. R. 1987b. Scathophagidae. In J. F. McAlpine, B. V. Peterson,
G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.).
Manual of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 1085–1098.
Vockeroth, J. R. and Thompson, F. C. 1987. Syrphidae. In J. F. McAlpine,
B. V. Peterson, G. E. Shewell, H. J. Teskey, J. R. Vockeroth, and D. M.
Wood (eds.). Manual of Nearctic Diptera, Vol 2. Monogr. Research
Branch Agriculture Canada, Ottawa, pp. 713–744.
West-Eberhard, M. J. 1984. Sexual selection, competitive communication
and species-specific signals in insects. In T. Lewis (ed.). Insect Communication. Academic Press, New York, pp. 283–324.
Wiley, R. H. and Poston, J. 1996. Indirect mate choice, competition for
mates, and co-evolution of the sexes. Evolution 50: 1371–1381.
Wood, D. M. 1987. Tachinidae. In J. F. McAlpine, B. V. Peterson, G. E.
Shewell, H. J. Teskey, J. R. Vockeroth, and D. M. Wood (eds.). Manual
of Nearctic Diptera, Vol 2. Monogr. Research Branch Agriculture Canada, Ottawa, pp. 1193–1270.
Wood, D. M. 1991. Homology and phylogenetic implications of male genitalia in Diptera. The ground plan. pp. 255–284 in Weismann, Orszàgh
and A. Pont. Proceedings of the Second International Congress of
Dipterology. The Hague.
Yen, S. H., Quickie, D. L., and Robinson, G. S. 2000. Evolutionary trends
on male genital structures of Chalcosiinae (Lepidoptera: Zygaenidae)
(Abstract). Abstract Book XXI International Congress of Entomology,
Brazil, August 20–26, 2000 1: 589.
Zuska, J. 1964. Notes on the Palearctic specis of the genus Nemopoda Robineau-Desvoidy (Diptera, Sepsididae). Acta. Ent. Bohemoslov. 62: 308–313.
Zuska, J. 1972. Revision of oriental and australasian species of Meroplius
and Xenosepsis (Diptera, Sepsidae). Acta Ent. Bohemoslov. 69: 60–68.