EVOLUTION & DEVELOPMENT 3:3, 206–222 (2001)

Multiple origins of a major novelty: moveable abdominal lobes in male sepsid (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 ex- productive decisions on particular types of stimuli will tend to treme scarcity among extant species of flies, moveable pro- favor male abilities to elaborate such stimuli, sexual selection cesses on the abdomen are apparently of relatively simple by female choice may sometimes result in sustained selection developmental origin, and they have evolved multiple times in for certain types of innovations in males. The lack of moveable males of the small family . They are used to stimulate appendages in most dipterans may be due not to develop- the female during copulation in two groups, where they are mental constraints, but to lack of selective advantages. probably independently derived. Because female cuing of re-

INTRODUCTION able abdominal processes, the early stages of acquisition of new abdominal appendages (“lateral lobes”) are relatively Phylogenetic uniformity in a trait is sometimes thought to common in males of the family Sepsidae (Fig. 1). This study imply the existence of developmental constraints against al- shows, using comparative morphology and direct observa- ternative designs of that trait, and major innovations are tions of behavior, that the lateral lobes in two closely related sometimes said to require substantial reorganization of the species are independently derived, and that in both cases phenotype (e.g., Müller and Wagner 1991). Constraint argu- these structures are used during sexual interactions and are ments of these sort run the risk of being tautological—what- probably under sexual selection by cryptic female choice. ever has not changed must have been constrained, and what- The complex musculature associated with similar structures ever has changed must not have been constrained. The basic in some other sepsids suggests that they are also moveable, claim of constraint is potentially falsifiable, however, by and that they may also have arisen independently under sim- finding that repeated changes in a trait have occurred in an ilar selection. otherwise unremarkable subgroup of a larger group in which the trait is otherwise uniform. This is the situation docu- mented here with respect to moveable abdominal append- Specialized male morphology in sepsid flies ages in flies. Sepsidae is a small family of flies of worldwide distribution Although abdominal appendages were present in the an- that includes about 240 species (Pont 1979). Adult males cestors of adult (e.g., Snodgrass 1935; Birket-Smith have various sexually dimorphic traits that are often spe- 1984), all except those associated with the genitalia were lost cies-specific in form (Hennig 1949; Pont 1979; Steyskal early in evolution. Subsequent evolution of new ab- 1987a), including a modified fourth abdominal sternite, the dominal appendages or moveable processes has occurred subject of this study. In all sepsid genera in which the posi- only rarely (e.g., Snodgrass 1935; Chapman 1999; Yen et al. tions of copulating pairs have been determined, the male’s 2000). In Diptera, aside from the dramatic and repeated fis- fourth sternite touches or is very close to contacting the fe- sions of genitalic sclerites (reviewed by Wood 1991; Sinclair male during copulation, including Meroplius and et al. 1994; Cumming et al. 1995), moveable abdominal pro- (Cheligaster) (Sˇ ulc 1928) (Fig. 1), Sepsidimorpha sp. (Fig. cesses are very rare (McAlpine et al. 1987). Thus, it might be 2), (Parker 1972; Schulz 1999; Eberhard unpub. ob- thought that such structures are developmentally difficult to servation of S. neocynipsea), Archisepsis (Eberhard and evolve. I will argue that this is not the case. Although adults Pereira 1996), and Microsepsis (Eberhard 2001 in press). This of most families of flies completely lack nongenitalic move- contact probably often occurs between the posterior portion

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Eberhard Evolutionary novelties in sepsid flies 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 Sˇ ulc 1928), and the relationships of Sepsidae (a member of the superfamily ) and other groups of higher Diptera () (after McAlpine 1989). of the male sternite and the female’s proctiger, which is Linn. and nitidula (Fallen), collected in Germany and pre- flexed dorsally to expose her vulva and permit intromission served in 70% ethanol were made from preparations mounted in Eu- (e.g., Fig. 2; see also Eberhard and Pereira 1996 on Archisep- parol on microscope slides, using a camera lucida. sis; Eberhard 2001 in press on Microsepsis). The nominal relations of Palaeosepsis sp. and P. nigricoxa are not clear. Silva (1993) argued that the monotypic genus Pseudopalae- osepsis should be included in her newly erected genus Archisepsis. Archisepsis, in turn, has classically been included in Palaeosepsis MATERIALS AND METHODS (senus latu) (Duda 1925, 1926; also Meier 1995). The two species thus belong to Palaeosepsis sensu latu, but the phylogenetic rela- Copulating pairs of Palaeosepsis sp. (an apparently undescribed tions among the species in Palaeosepsis sens. lat. remain to be de- species near P. chauliobrechma Silva) were observed in the field termined. 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 RESULTS flies were observed using a 2 headband magnifier and 10 and 20 hand lenses. The bristles of the male’s fourth sternite were Morphology and movement of modified sternites clearly visible. Palaeosepsis sp. In addition, copulation behavior of both P. sp. and Pseudopalae- The fourth abdominal sternite of P. sp. is larger than the pre- osepsis nigricoxa Ozerov was observed in captivity under a dissect- ceding sternites and has a brush of very long setae at each ing microscope, using flies raised in captivity from cow dung (P. sp.), or from howler monkey dung (Alouatta palliata) on Barro Colorado posterior lateral corner (Figs. 3 and 4). The fifth sternite is Island, Panama (P. nigricoxa). Copulating pairs of P. sp. were frozen small (Fig. 4) and is hidden in an inward fold of the abdom- with ethyl chloride spray and fixed in 70% ethyl alcohol or FAA prior inal cuticle. The base of each brush is heavily sclerotized and to being prepared for examination with a scanning electron micro- more or less circular (Fig. 4). When at rest, the long setae of scope. Drawings of specimens of these species and of the brushes project posteriorly (Fig. 3). The cuticle of the

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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 abdom- inal 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 cen- tral 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 se- tae 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). Con- traction of these muscle fibers presumably moves the brush Fig. 3. Scanning electron micrographs of Palaeosepsis sp. (A). Ven- anteriorly, causing the setae to project ventrally from the tral view showing positions of male surstyli and fourth sternite brushes at rest. (B) Lateral view of male abdomen (right) with male’s abdomen. brush directed ventrally and contacting female abdomen during The male tapped the female’s abdomen rapidly with his copulation. (C) Close-up ventral view of base of brush at rest, show- brushes in all copulating pairs of P. sp. (four in the field, four ing 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 se- Themira putris tae fanned out to assume a cupped form (Fig. 3B), and then The strong and complex muscles associated with the lateral the brushes vibrated in an approximately dorsoventral direc- lobes of T. putris (Fig. 5) indicate that the lobes in this spe- tion an estimated 3–10 times/sec, so that the setae tapped the cies are also moveable. Ventral projection of the long setae sides of the female’s abdomen (Fig. 3C). In the most com- in T. putris is probably produced, at least in part, by contrac- plete observation of a copulation, which lasted 104 min, the tion of the medium-strong band of muscles running dorsally brushes beat continuously on the female for at least 12 min from the anterior margin of the sternite to tergite 4 (Fig. 5). soon after copulation began, then became quiet. They re- Medial and perhaps rotatory movements of the moveable sumed beating during six bursts of activity that lasted be- lobes probably also occur. Two moderate-sized bundles of tween about 10 and 100 sec during the next 38 min. 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 P. nigricoxa setae of the lobe. Contraction of one of these (A), which is The structure of the fourth abdominal sternite in P. nigricoxa attached on or near the dorsolateral surface of the internal is very different. The central portion of the sternite is a thin, strut of the moveable lobe, apparently produced a rotatory transverse, dark band that is sharply pointed at either end movement of the moveable lobe and the brush of setae with (Fig. 4). At each end of the central portion there is a long thin respect to the central portion of sternite 4; rotation would be lateral lobe, with two rows of long setae along its distal half. around the tip of the strut (X in Fig. 5). Contraction of mus- The base of each lateral lobe is expanded, and the middle cle B, which also ran dorsal to X but which was attached very portion of the base articulates with the sharp lateral point of near the tip of the strut, may also produce rotation; its con- the central portion (Fig. 4). At rest the lateral lobes are di- traction would tend to hold the tip of the strut tight against rected posteriorly. The fifth sternite is much longer than the the point of rotation (X). The dorsal component of these ro- fourth, and its anterior corners form small processes that ex- tatory effects (or posterior component, once the central por- tend anteriorly to nearly reach the articulation at the base of tion of the sternite is rotated by the tergite muscles) would be each lateral lobe. accentuated by the fact that muscles A and B were tightly en- Internally, the fourth sternite has no keel, and there are no circled by a strong rigid band connected with the central por- muscle fibers joining the center of the sternite with the tips, tion of the sternite (an effect similar to that produced by the as in P. sp. Instead, there is a small internal keel on the pos- pulley associated with the superior oblique muscles of the terior portion of sternite 5 (Fig. 4). A thin sheet of muscle fi- human eye; Quain et al. 1842). At least some of the setae can bers runs from the anterior edge of sternite 4 to sternite 5 apparently be moved individually, as a few fibers were at- (Fig. 4). Contraction of these fibers presumably causes the tached to internal extensions of the bases of at least two setae entire central portion of the fourth sternite to rotate, and thus (Fig. 5). move the lateral lobes anteriorly so that they are directed Sternite 5 is probably also moveable. A sheet of muscles ventrally (see below). A second thin sheet of muscles is at- runs from the rear portion of sternite 5 to the posterior sur- tached to an invagination of the posterior margin of the fifth face of sternite 4 (sternite 5 muscles in Fig. 5). Their contrac- sternite, and they converge in the area of the articulation at tion would cause sternite 5 to move at its articulation with the base of the lateral lobe (Fig. 4). Contractions of these sternite 4, causing the pair of strong bristles on sternite 5 to muscles undoubtedly move the lateral lobes. project more ventrally. Thus, these muscles may move the In each of two pairs of P. nigricoxa observed while cop- bristles into contact with the female. ulating, the male’s lateral lobes projected ventrally soon af- There are no descriptions of copulation behavior in ter intromission began, and tapped or swept repeatedly Themira, but the drawing of a copulating pair of T. ( Che- across the female’s abdomen. In the most complete observa- ligaster) leachi (Meigen), in which the long setae of the tion, the male began to tap the female 2:17 after copulation male’s fourth abdominal stenite are directed ventrally (Sˇ ulc began, moving his lateral lobes repeatedly forward so that 1928; see Fig. 1), indicates that the lobes of the fourth stern- their long setae brushed against the posterior half of the fe- ites are moveable. male’s fifth abdominal tergite approximately 1.5–2 times/ sec. Tapping continued for at least 130 sec. The lateral lobes Nemopoda nitidula seemed to vibrate as they swept the female. Later, the lateral Sternite 4 and its associated muscles differed in many re- lobes were brought alongside the male’s genitalic surstyli, spects from those of the other species. The sternite’s ventral and their setae tapped the female’s abdomen in this area with surface was highly sculptured (Fig. 6), and dorsally a thick an irregular rhythm about 1–3 times/sec. The lobes twisted keel projected inward (Fig. 6). There were two pairs of ap- so the longest setae were parallel to the female’s longitudinal parent lobes (A and B in Fig. 6), each of which bore an array axis at some times, while at others they were directed toward of long setae at its tip. The lobes on each side were connected her body at 20–30. 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 the distal portion of processes A and B to move laterally (to lobe A were thick and flattened, and formed three distinct open up), and others (V, W) probably closed them. Another thick bundles. These bundles of setae were stiff when muscle band (Z) tilted sternite 4, causing the long setae to touched. They thus contrasted with all the long setae of the project ventrally (as in T. putris, above). Some muscles (U, S) other species, which were flexible. The setae of lobe B were were attached at both ends to the cuticle of the sternite, and thinner, rounder, and did not form bundles; aside from being presumably caused it to flex and change shape. relatively shorter, they resembled the long setae of the other Either sternite 5 was highly sculptured and more or less species. fused with sternite 4 (see Fig. 6), or it was so reduced that I The musculature associated with sternite 4 was more could not find it. In either case, it was clear that, in contrast complex than that in the other species (Fig. 6), and was not to T. putris, there were no muscles that would move sternite completely deciphered. Some muscles (X) probably caused 5 with respect to sternite 4.

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Fig. 6. Ventral view of exter- nal surface of sternites 4 and 5 of a male Nemopoda nitidula (above), and dorsal view of the same sternites and their associated muscles.

Eberhard Evolutionary novelties in sepsid flies 213

Modified male abdominal sternites in other sepsids ing degrees of apparent separation of potentially moveable The male’s fourth abdominal sternite does not differ from processes: that of the female in the basal sepsid genus Orygma (Hen- (A) Sternite shape only slightly dimorphic but posterior nig 1958) (see Fig. 9)—or in the related families Sciomyz- setae thicker or longer (A. diversiformis, ecalcarata, and dis- idae (Knutson 1987), (Steyskal 1987b), and color in Fig. 7; Sepsis in Fig. 8). In some groups (e.g., (Vockeroth 1987a)—so lack of sexual dimorphism Archisepsis, Microsepsis), the male’s fourth (or sometimes in sternite 4 is the likely plesiomorphic state for the family third or second) sternite is more or less similar in size and Sepsidae. As is common in specialized non-genitalic con- form to that of the female, but has more bristles or setae, tact courtship devices in many (Eberhard 1985), which are often somewhat longer than those of the female. sexually dimorphic modifications of the male sternites are The modified setae usually originate on the posterior and lat- generally species-specific in form (Table 1). Thus, species eral portions of the male sternite, where they are most likely descriptions in sepsids often include drawings of male stern- to contact the female during copulation. These setae are fre- ites, allowing an overview of the presence of the different quently species-specific in number and pattern of placement, types of sternite modification throughout the family, though even in some groups of species such as Sepsis in which they data are lacking for some groups and many of the taxo- have not usually been employed in taxonomic descriptions nomic drawings are not detailed enough to be used as reli- (Silva 1993) (Figs. 7 and 8); able indicators of divisions between independent morpho- (B) Modified setae arise on short extensions of the stern- logical processes (A. Pont, pers. comm., unreferenced; R. ite (A. hirsutissima, T. lucida in Fig. 7). These setae are Meier, pers. comm., unreferenced). A preliminary classifica- nearly always much longer than those of type A sternites. tion of derived, sexually dimorphic male sternite morphol- The sternite is extended, usually laterally and/or posteriorly, ogy includes three different types (Fig. 7), involving increas- and the long setae are nearly always inserted on the exten-

Fig. 7. Representatives of dif- ferent types of secondary sex- ual modification of fourth ab- dominal sternites in Sepsidae (all males unless otherwise specified) (at different scales): unmodified fourth abdomi- nal sternite of female Archi- sepsis diversiformis Ozerov); Type A. Sternite form little modified, with species-specific array of larger setae on pos- terior portion (Archisepsis di- versiformis, ecalcarata, and A. discolor); Type B. Elongate setae originating on exten- sions of the sternite, which is a single unit (A. hirsutisima Silva, Themira lucida Staeger); Type C. One or several inde- pendent sclerites at each end of the sternite (Palaeosepsis maculata Silva, T. superba Hal- iday, T. germanica Duda, A. muricata Silva). (after Silva 1993 and Hennig 1949).

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Fig. 8. Male and female stern- ites in different species of Sepsis, illustrating differences between males and females, and the relatively greater in- terspecific 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 be- of the long setae in Themira probably involve rotation around tween each extended corner and the rest is thinner (Fig. 3C); a point at the base of the brush (X in Fig. 5). The sternite of (C) Separate lateral lobes that bear long setae (P. macu- Nemopoda, in contrast, seems to have two different pairs of lata, T. superba and germanica, A. muricata in Fig. 7). In lobes, which have more limited movement as a unit. Some some species, there are one or more sclerites that are distinct muscles apparently move portions of the sternite indirectly from the central portion of the sternite, and in at least some by bending the cuticle, something not seen in the other three cases they are separated from it by membranes (T. german- genera. The complex ventral surface of the central portion of ica). The drawings of some species do not allow distinction the sternite suggests that it is pressed against the female. of additional sclerites from an extension of the sternite with There is at present no clear consensus regarding the phy- an intervening thinner band of cuticle (e.g., Fig. 3C). In some logenetic relationships within Sepsidae. The one published cases, however, asymmetrical positions of the lobes provide tree, based on larval characters (Meier 1995) (Fig. 9), has direct evidence that the lobe can move with respect to the some important disjunctions with a second, preliminary tree other sclerites (A. muricata in Fig. 7). 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 pro- DISCUSSION cesses within the family. It is also clear, however, from the data in Table 1 that the moveable lobes documented here are Developmental constraints not unique within the family. The complexity of the muscu- The designs for moving the sternal lobes of Palaeosepsis sp. lature associated with the lobes of Themira and Nemopoda, and P. nigricoxa are very different, so it is likely that this combined with the apparently different setal bases of T. pu- mobility has evolved independently. Both the ventral move- tris, and the consistently basal position of Themira and de- ment of the brush of long setae, which brings it into position rived position of Palaeosepsis sensu latu in trees using both to tap the female, and the actual tapping movements are pro- larva and adult characters (Fig. 9; R. Meier, pers. comm., un- duced by novel muscles with substantially different points of referenced), suggest a total of at least three derivations of origin and insertion. In both Themira and Nemopoda ventral moveable abdominal lobes. movements of the brushes (a movement that has been con- The male sternites of P. sp. and P. nigricoxa suggest that firmed by direct observation only in Themira—Fig. 1, Sˇ ulc the early stages in the evolution of a moveable abdominal ap- 1928) are at least in part due to a set of muscles not seen in pendage are surprisingly easy to produce. A new cuticular the other species that attached at one end to tergite 4 and at sclerite that articulates with a pre-existing sclerite can result the other to the anterior portion of sternite 4. This suggests at from nothing more than a thinning of an intermediate area of least one more independent derivation. Medial movements a pre-existing sternite (e.g., Fig. 3C). Muscles to move the Eberhard Evolutionary novelties in sepsid flies 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 SEXUAL DIMORPHISM TYPE SPECIES-SPECIF.? REF

Orygma luctuosum Meigen none N — Hennig 1958 Paratoxopoda depilis Wlkr. lobe?, mod. setae A/B? Y Duda 1926 crassiforceps Duda more or less bare A? Y Duda 1926 akuminambili v short setae st.5* Y Ozerov 1993 akuminamoya med setae st.5* Y Ozerov 1993 amonane m-s setae st.5* Y Ozerov 1993 angolica med setae thick st.5* Y Ozerov 1993 asaba med set med st.5* Y Ozerov 1993 asita med setae fine st.5* Y Ozerov 1993 baebata med set fine st.5* Y Ozerov 1993 depilis (Walker) med set fine st.5* Y Ozerov 1993 dudai Ozerov m-l setae strong st.5* Y Ozerov 1993 frontalis Ozerov m-l setae strong st. 5* Y Ozerov 1993 kilinderensis Vanschuytbroeck med setae fine st.5* Y Ozerov 1993 magna Ozerov m-s setae strong st.5* Y Ozerov 1993 pilifemorata Soos s setae fine st.5* Y Ozerov 1993 saegeri Vanschuytbroeck m setae med thick st.5* Y Ozerov 1993 similis Ozerov m set fine st.5* Y Ozerov 1993 straeleni Vanschuytbroeck m-l setae strong st.5* Y Ozerov 1993 tenebrica Ozerov m-l setae strong st.5* Y Ozerov 1993 tricolor (Walker) m-l setae strong st.5* Y Ozerov 1993 villicoxa Duda m-s setae strong st.5* Y Ozerov 1993 zuskai Ozerov m-s setae fine* Y Ozerov 1993 Themira subgenus Enicita annulipes Meigen long setae B? Y# Duda 1925 annulipes (Meigen) long setae B/C Y Pont 1979, Ozerov 1998a bispinosa Melander and Spuler long setae (2 spines st.5) B Y Ozerov 1998a mexicana Ozeov long setae C Y Ozerov 1998a subgenus Annamira leachi (Meigen) long setae & keel C YSˇ ulc 1928, Pont 1979, Ozerov 1998a japonica Ozerov long setae plus keel B? Y Ozerov 1998a notmani Curran almost no setae! A Y Ozerov 1998a subgenus Enicomira minor (Haliday) long setae § C Y Pont 1979, Ozerov 1998a long setae C Y Hennig 1949, Ozerov 1998a kanoi Iwasa long setae A/B Y Ozerov 1998a paludosa Elberg long setae B/C Y Ozerov 1998a sabulicola Ozerov long setae (not on lobe!) B Y Ozerov 1998a subgenus Nadezhdamira superba (Haliday) long setae C Y Pont 1979, Ozerov 1998a pusilla (Zetterstedt) long setae §? C Y Pont 1979, Duda 1925, Ozerov 1998a latitarsata Melander and Spuler long setae C Y Ozerov 1998a malformans Melander and Spuler long setae C Y Ozerov 1998a subgenus Themira gracilis (Zetteerstedt) long setae C Y Pont 1979, Ozerov 1998a nigricornis Meigen mod. long setae¶ B Y Pont 1979, Hennig 1949, Ozerov 1998a putris Linn. long setae C Y Pont 1979, Duda 1925, Ozerov 1998a lucida Staeger long setae B Y Pont 1979, Duda 1925, Mangan 1976, (athabasca Mangan) Hennig 1949, Ozerov 1998a germanica Duda long setae § C Y Pont 1979, Hennig 1949, Ozerov 1998a seticrus Duda long setae B Y Hennig 1949, Ozerov 1998a arctica Becker (dampfi Becker) long setae C Y Duda 1925, Ozerov 1998a biloba Andersson long setae Y Ozerov 1998a bifida Zuska long setae B Y Ozerov 1998a flavicoxa Melander and Spuler long setae B Y Ozerov 1998a Continued 216 EVOLUTION & DEVELOPMENT Vol. 3, No. 3, May–June 2001

Table 1. Continued SPECIES SEXUAL DIMORPHISM TYPE SPECIES-SPECIF.? REF

lutulenta Ozerov short setae B Y Ozerov 1998a mikiharai Iwasa short setae N/A Y Ozerov 1998a mesopleuralis Iwasa long setae A Y Ozerov 1998a mongolica Soos long setae B Y Ozerov 1998a saigusai Iwasa long setae C Y Ozerov 1998a shimai Iwasa long setae B Y Ozerov 1998a Susanomira caucasica Pont long setae sternite 3 and B * Pont 1987, pers. comm. tergites 4,5 (sternite 4 not visible) Decachaetophora short setae A Hennig 1949 aeneipes de Meijere sphondylii Shrank mod. setae A ? Hennig 1949 Nemopoda pectinulata Loew lobe, mod. long setae C Y Duda 1925, Zuska 1964 nitidula (Fallen) (cylindrica) lobe, mod. setae C Y Duda 1925, Zuska 1964 speiseri Duda lobe, mod. long setae C Y Zuska 1964 Meroplius albuquerquei Silva no modifications N Y Silva 1990 beckeri (Meijere) lobe, short/long setae † C Y Zuska 1972 sauteri (Meijere) lobe, short/long setae † C Y Zuska 1972 fasciculatus (Brun.) lobe, short/long setae † C Y Zuska 1972 minutus Wiedemann lobe, mod. short setae C Y Hennig 1949 ( stercorarius Rob.-Desv.) subgenus Meroplius bispinifer Ozerov two parts, nearly no modif. A?B? Y Ozerov 1999b africanus Long setae B Ozerov 1999b trispinifer Ozerov Long setae C? Y Ozerov 1999b unispinifer Ozerov med-short setae C? Y Ozerov 1999b hastifer Seguy med-long setae B (nearly C) Y Ozerov 1999b hastiferoides Ozerov few, short setae C Y Ozerov 1999b latispinifer Ozerov med long setae B Y Ozerov 1999b madagascarensis Iwasa med-long setae (Forked) B/C Y Ozerov 1999b pallidispinifer Ozerov short setae A Y Ozerov 1999b unispinifer Ozerov med-short setae B Y Ozerov 1999b subgenus Protomeroplius trispinifer Ozerov long setae C Y Ozerov 1999b subgenus Xenosepsis africanus Ozerov long setae B Y Ozerov 1999b sydneyensis short lobe, short setae (Pseudomeroplius acrosticalis Duda lobe(?), mod. setae B? * Duda 1926 Palaeosepsis chauliobrechma Silva lobe, long setae B Y Silva 1993 maculata (Duda) lobe, long setae C Y Silva 1993 dentata (Becker) lobe, long setae B Y Silva 1993 dentatiformis (Duda) lobe, long setae B Y Silva 1993 erythromyrma Silva lobe, long setae B Y Silva 1991, 1993 insularis (Williston) short setae A Y Silva 1993 laticornis (Duda) mod. short setae A Y Silva 1993 pusio (Schiner) short setae A Y Silva 1993, WGE n. sp. lobe, long setae B Y WGE Archisepsis hirsutisima Silva lobe, mod. long setae B Y Silva 1993 armata (Schiner) short setae A Y Silva 1993 diversiformis (Ozerov) short setae A Y Ozerov 1993 excavata (Duda) short setae A Y Silva 1993 mirifica Silva lobe, long setae B/C Y Silva 1993 muricata Silva lobe, long setae ¶ C Y Silva 1993 priapus Silva short setae A Y Silva 1993 polychaeta mod. setae A Y Ozerov 1993 pleuralis (Coquillett) mod. setae A Y WGE discolor (Bigot) ( scabra) mod. setae A Y Ozerov 1993, WGE Pseudopalaeosepsis lobe, long setae C * Ozerov 1992a nigricoxa Ozerov Microsepsis anomala Silva short setae A Y Silva 1993 Continued Eberhard Evolutionary novelties in sepsid flies 217

Table 1. Continued SPECIES SEXUAL DIMORPHISM TYPE SPECIES-SPECIF.? REF

armillata (Melander and Spuler) lobe, mod. long setae B/C Y Silva 1993, Duda 1925 furcata (Melander and Spuler) short setae A Y Silva 1993 WGE inflexa (Becker) lobe, mod. setae A/B Y Silva 1993 mitis (Curran) short setae A Y Silva 1993 mystrion Silva short setae ** A/B Y Silva 1993 simplicula (Steyskal) lobe, mod. long setae B Y Silva 1993 stenoptera Silva short setae A Y Silva 1993 eberhardi Ozerov lobe, mod setae B Y Ozerov 1997, WGE Sepsidimorphar¶¶ duplicata (pilipes) (Wulp) mod. setae on 3 and 5 A? Y Duda 1925, Hennig 1949 setulosa Duda§§ mod. setae on 3 only N Y Duda 1925 secunda mod setae on 4 only A Y WGE Nicarao rarus Silva short setae A? * Silva 1995 Dicranosepsis transita Ozerov med setae A ? Ozerov 1996 Sepsis tuberculata Duda no* N? Duda 1926 neocynipsea short setae A WGE duplicata short setae A Y WGE thoracica short setae A Y WGE punctum short setae A Y WGE cynipsea short setae A More or less Y WGE alanica short setae A Y More/less Ozerov 1998b Palaeosepsioides grimaldii Ozerov long setae ‡‡ C * Ozerov 1992 Zuskamira inexpectata Pont long setae, short setae central area C * Pont 1987 Parameroplius fasciculata Brun. hairy Duda 1926 Perochaeta orientalis de Meijere very long and elaborate, no setae C? Y Duda 1926 hennigi Ozerov long setae, prob. keel B Y Ozerov 1992b Meropliosepsis sexsetosa Duda lobe, mod. setae B Silva 1992 Dudamira abyssinica Duda short setae A Ozerov 1995 Afrosepsis sublataralis Vanschuytbroeck med long setae B Y Ozerov 1999a camerounica Ozerov Few mod long setae A/B Y Ozerov 1999a quadrimaculata Ozerov One mod long seta B Y Ozerov 1999a elongata Ozerov two long setae B Y Ozerov 1999a lineata long setae B Y Ozerov 1999a Afromeroplius semlikiensis Vanschuytbroeck long setae B/C Y Ozerov 1995 watalingaensis Vanschuytbroeck long setae C Y Ozerov 1995 * 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 Sˇ ulc 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 metry in form and attachment sites of the muscles in Figure sheets of muscle fibers that are attached to the abdominal 10 suggests ample variation in the placement of these mus- sternites and membranes of other segments. Such muscles cles in sepsids, which could be the starting point for selection are associated with the sternites of other abdominal segments favoring modified morphology that allowed movement of in males and females of these and other species of sepsids incipient sternal lobes. (Fig. 10), and indeed in many other insects (Snodgrass 1935, Recruitment of nearby muscles for new functions is prob- 1956; Birket-Smith 1984; Chapman 1999). The lack of sym- ably 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 avail- able on male abdominal stern- ite form (after Meier 1995). Letters refer to types of stern- ite (see text and Fig. 7). vation and microstructure to determine homologies, that in and Wagner 1991). The moveable lateral lobes of male the formation of peripheral hemolymph pumps (”peripheral sepsids fit many definitions of a novel trait (Müller and Wag- hearts”), “any [nearby] muscle system is liable to become a ner 1991), and the widespread absence of such structures in component of a [peripheral] circulatory pump” (Pass 2000). other Diptera might suggest that they are developmentally Developmentally, myoblasts could move into areas where difficult to evolve. On the contrary, however, the observa- re-patterning of the epidermis had already occurred (Ger- tions reported here suggest that moveable lobes are develop- hardt and Kirschner 1997). The possible recruitment of more mentally easy to evolve. The abdomens of male sepsids with basic appendage producing mechanisms, such as distal-less moveable lobes are not obviously reorganized with respect to found in many groups (Panganiban et al. 1997), re- those of conspecific females in other respects. A seemingly mains to be tested. more likely explanation of the absence of moveable processes The repeated evolution of moveable abdominal lobes in in other flies is that they have not been selectively advanta- sepsids contrasts sharply with the lack of such structures in geous; that is, there have been no courtship interactions of other flies in the general taxonomic vicinity. For instance, comparable importance under sexual selection that favor the book of McAlpine et al. (1987) illustrates sexually di- morphological innovation of this kind in males. This hypoth- morphic modifications of the ventral surface of the male’s esis is discussed further in the next section. abdomen in only 14 of the other 63 muscomorph families (Table 2). Although their coverage is undoubtedly incom- Why sepsids? plete, it is clear that in some large families such as Why should it be that male sepsids have repeatedly evolved (B. Brown, pers. comm., unreferenced) and , the otherwise extremely rare trait of moveable nongenitalic such structures are apparently unknown: “To my knowledge, abdominal structures? A possible answer is suggested by the there are no drosophilids where sternites have become frag- link established in this study between the sternal lobes and mented. . .” (D. Grimaldi, pers. comm., unreferenced). In only stimulation of the female during copulation, and thus the Rhinotoridae and do the descriptions or fig- probability that the lobes are under sexual selection. There ures of McAlpine et al. (1987) suggest moveable lobes like are two indications that female sepsids may have an other- those of sepsids. To the best of my knowledge there are no wise unusual ability to sense stimuli from the male’s sterni- studies of copulatory behavior in either of these small fami- tes during copulation. The genital morphology of female lies, which are very distantly related to Sepsidae and to each sepsids is unusual among other flies in that the hypoproct other, or dissections to check for muscles that would allow and cerci are displaced to a more dorsal position, and are thus conclusions regarding the possibility that the lobes can be more exposed to the ventral surface of the mounted male moved independently. (Hennig 1949; Pont 1979). The hypoproct and cerci seem The moveable abdominal lobes of sepsids illustrate the po- likely to be relatively rich in sensory organs compared with tential trap of supposing that phylogenetic uniformity implies the usual dorsal structures of the ovipositor in other flies and developmental constraints against alternative designs (Müller thus predispose females to be sensitive to male stimuli (R. Eberhard Evolutionary novelties in sepsid flies 219

Meier, pers. comm., unreferenced). Another possibly con- (West-Eberhard 1984; Andersson 1994; Ryan 1990). As a tributing factor is that sepsids (other than Orygma, Pont result, when females evolve to use a particular male signal as 1979; Steyskal 1987a) are also unusual in lacking strong se- a mate choice criterion (to respond to it in a way that favors tae on the dorsal surface of the abdomen; this could allow the reproductive success of the male), the likelihood that ad- more intimate contact between the male’s ventral surface ditional male stimuli in that particular modality will be able and the female. to elicit improved female responses probably often in- It seems inevitable that the sensory capabilities of females creases. In addition, female use of a particular type of stimuli will often have important evolutionary consequences for the to filter males will often result in selection on females that fa- evolution of new male traits under sexual selection by fe- vors an increase in female ability to discriminate among such male choice, because only those stimuli that a female can stimuli, through either modification of her sense organs or sense can be expected to induce favorable female responses changes at higher levels in her CNS. In other words, a “sen-

Fig. 10. Dorsal view of longi- tudinal and transverse mus- cles near the ventral abdom- inal wall of segments 4–6 of a female Archisepsis diversi- formis (tranverse muscles on folded intersegmental mem- brane 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 Structure Ref.

Micropezidae forceps-like extensions (frequent) Steyskal 1987c short spines and setae (frequent) Smith and Peterson 1987 Syrphidae tubercles and keels (rare) Vockeroth and Thompson 1987 various modifications (some) Shewell 1987a Rhinotoridae lobes on post-lat margins (some) McAlpine 1987 modified as genital pouch (frequent) Marshall and Richards 1987 modified distinctive setae (some) Vockeroth 1987b bilobate posteriorly Huckett 1987 some very elaborate Huckett and Vockeroth 1987 strongly bilobate Shewell 1987b Sarcophagidae bilobate Shewell 1987c apical cleft Wood 1987 some with pair of sclerites Maa and Peterson 1987 Nycteribiidae comb-like rows of spines, some with Peterson and Wenzel 1987 postero-lateral lobes with spines

sory focus” by the female on some particular subset of stim- Diptera. In particular, male genitalic structures are extremely uli, which is probably a widespread trait among insects (Ber- diverse; some structures have become divided and move- nays and Wcislo 1994), can have consequences for the able, new points of articulation and muscles have arisen, new evolution male display traits. If the females of a species are sclerites have arisen from membranes, others have fused, focusing one particular type of stimuli, then modifying or etc. (see Wood 1991, Sinclair et al. 1994, and Cumming et elaborating these stimuli is especially likely to be advanta- al. 1995 for general reviews of the evolution of dipteran gen- geous for males (see also Wiley and Poston 1996). italia; Eberhard 2001 in press, for two new articulations in This phylogenetic inertia argument regarding female sen- the sepsid genus Microsepsis, for one of which there are be- sory modes suggests that once female sepsids began to use havioral data that strongly suggest a stimulatory function). stimuli from the ventral surface of the male’s abdomen to cue The evolution of the male abdominal sternal lobes in Sepsidae their reproductive decisions, the likelihood that a male could may represent in miniature the evolution of male genitalia in further increase his chances of fertilizing eggs by further or Diptera. Stimulation of the female by the male’s genitalia is more effective stimulation of the female’s abdomen increases. an almost inevitable consequence of internal insemination, The probable relatively early origin of this female response in and cuing of female reproductive processes on these stimuli sepsids (Table 1, Fig. 9) suggests that male sepsids have had a is probably widespread (Eberhard 1985, 1996). Female re- relatively long evolutionary time to evolve novel mechanisms sponses to such stimuli have been demonstrated experimen- with which to produce such stimuli. In the sense of Saether tally in flies of the families Glossinidae (Leegwater-van der (1979), female use of stimuli from the posterior portion of the Linden and Tiggelman 1984), and (Otronen male’s abdomen to screen mates may have been an underlying 1990; Otronen and Siva-Jothy 1991), and may also occur in synapomorphy that has given male sepsids the evolutionary Drosophilidae (Coyne 1993). Sustained sexual selection on tendency to evolve moveable lateral lobes on the abdomen. males to stimulate females with their genitalia may thus have Henry et al. (1999) mention a similar convergence in the mat- resulted in the extraordinary evolutionary inventiveness seen ing songs of lacewing insects. in male genitalic structures. This argument suggests that a modification of the anat- omy of the posterior portion of the abdomen of female Acknowledgments sepsids may have led to the evolution of the novel moveable I thank Katja Schulz for kindly sending me specimens; Maribelle abdominal lobes in males. But the logic differs from that of Vargas for outstanding production of SEM images; Axel Retana, hypotheses based on developmental constraints. The claim is David Wahl, and Andy Bennett for advice with regard to cladistic not that modification of the female was necessary in over- analyses; and Rudolf Meier, Adrian Pont, and Mary Jane West- coming developmental limitations in males, but rather that it Eberhard for comments on a preliminary version of the manuscript. provided a new selective context in which such cuticular Financial support was provided by the Smithsonian Tropical Re- search Institute and the Vicerrectoría de Investigación of the Uni- variants were advantageous. versidad de Costa Rica. Note added in proof: Andrej Ozerov kindly Evolutionary innovation in structures that are probably identified the Palaeosepsis species of this study as dentatiformis under sexual selection also occurs in other structures in (Duda). Eberhard Evolutionary novelties in sepsid flies 221

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