Behavioral Ecology Vol. 14 No. 4: 526-530
© 2003 International Society for Behavioral Ecology
Courtship in long-legged flies (Diptera: Dolichopodidae): function and evolution of signals
Institut für Neurobiologie–AG Zoologie und Didaktik der Biologie, Heinrich-Heine-Universität, Universitätsstr. 1, D-40225 Düsseldorf, Germany
Address correspondence to M. Zimmer, who is now at Zoologisches Institut: Limnologie, Biologiezentrum der Christian-Albrechts-Universität, Olshausenstr. 40, D-24098 Kiel, Germany. E-mail: mzimmer{at}zoologie.uni-kiel.de.
Received 16 May 2001; revised 17 September 2002; accepted 1 October 2002.
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ABSTRACT |
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Analyzing the courtship behavior of long-legged flies (Diptera: Dolichopodidae), we focus on the evolutionary development of courtship signals. Long-legged flies may serve as a model for this evolutionary process, because males of some species present sexually dimorphic badges during courtship, whereas others do not exhibit such conspicuous signals but present lavish courtship behavior, including dynamic flight maneuvers. A comparison of these two groups within a single taxonomic family provides insight into the evolution of courtship signals and the corresponding behavior. Males of the closely related Empididae do not possess such badges. Within the super-family Empidoidea, we propose an evolutionary shift from dynamically courting and mating on the wing (in Empididae) to courting and mating on ground (in Dolichopodidae), accompanied by signaling through badge-waving. By comparing previously published data and observations on courtship behavior in Dolichopodidae, we present the hypothesis that the latter replaced the former energetically expensive behavior as a case of automimicry and sensory trap.
Key words: courtship, Dolichopodidae, habitat selection, long-legged flies, mate choice, mimicry, sexual selection, signal evolution.
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INTRODUCTION |
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Our knowledge about courtship signals has rapidly increased during the past decades. Theoretical and behavioral studies have revealed information on receiver psychology and the respective evolution of signals (for review, see Endler and Basolo, 1998
; Rowe, 1999; Ryan and Rand, 1993). Despite our poor knowledge of phylogenetic relationships within this family (Ulrich H, personal communication), long-legged flies (Diptera: Dolichopodidae) might serve as a good model for further understanding these topics of sexual selection. The males of some species present sexually dimorphic badges during courtship, whereas others do not exhibit such conspicuous signals. Males of the closely related Empididae do not possess such badges. A comparison of these two groups of dolichopodid flies provides insight into the evolution of courtship signals and the corresponding behavior.
The lavish courtship behavior of some long-legged flies has been described in detail recently (Land, 1993a,b; Lunau, 1992, 1996; Zimmer, 2000). Males show dynamic flight maneuvers and/or display their badges by waving them in front of, or behind, the potential mate. In both cases–presenting sexually dimorphic badges or showing dynamic flight maneuvers–courting males invest in advertisement (Zahavi, 1981). Only if the costs for the signaler are high enough that advertising reliably demonstrates the signaler's constitution can the receiver use the submitted information for decision processes (Zahavi, 1975, 1977). In the present article, we discuss sexually dimorphic badges of dolichopodid flies with respect to (1) their function as signals in courtship behavior and (2) possible pathways of their evolutionary implementation by comparing existing data on courtship behavior in a variety of species of long-legged flies. Within the family Dolichopodidae, we propose an evolutionary shift from courting and mating on the wing to courting and mating on ground.
Visual communication in courtship: sexually dimorphic badges as signals
When communicating, a receiver perceives and uses information submitted by a sender (Hinde, 1972; Otte, 1974). Reception of potential mates, courtship, and mate choice frequently involve visual communication. Visual signals display individual differences of senders by using standardized information that can be used in decision processes (Zahavi, 1981). According to Zahavi (1975, 1977), the signal display allows for estimation of the sender's constitution and, thus, for information input, only if sending signals is costly for the sender ("honest signal" sensu; Hamilton and Zuk, 1982). Honest signals, however, need not be costly if there is no sender-receiver conflict, because both share a common interest and the sender does not gain from deceiving the receiver (see Maynard-Smith 1991, 1994). Zahavi (1993: 227), in turn, argued that "it is difficult to imagine any social interaction in which there is no potential for some conflict." This is certainly true for courtship behavior, because males may deceive females by pretending to be better mates than they are.
A simple measure for estimating a mate's quality may be its size. Courtship in long-legged flies involves display behavior that would allow for size estimation (cf. Lunau, 1992, 1996). By comparing the average size of all males in a given population with the average size of successfully courting males, Lunau (1992) showed that male size is at least one cue for female mate choice in Poecilobothrus nobilitatus. Both winners of male-male combats (wing length, 6.03 ± 0.31 mm) and males in copula (6.02 ± 0.33 mm) were significantly larger than were average males (5.71 ± 0.35 mm). Data for other dolichopodid species are scarce. In species with sexually dimorphic badges, however, those male appendages carrying the badges are significantly prolonged in relation to others (Lunau, 1996; Figure 1). An involvement of these badges in signaling size is likely, and they may facilitate the evaluation of male size by the female. Male size, in turn, can serve as a measure of quality, because adult size reflects the former nutritional status of the developing larva. By contrast, the current physiological status of a male would be advertised best by some dynamic action (see below).
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= 0.05) prolongation of sexually dimorphic badge-carrying (filled symbols) versus nonmodified (open symbols) legs (squares) and wings (circles). Forelegs and wings do not differ in length in species without sexually dimorphic badges (p >.2). Data are mean values of 5–10 individuals, each (after Lunau, 1996Possibly, displayed badges act in amplifying a signal that already a uniformly colored wing will exhibit when in motion (Figure 2). Because the wing is rigid and narrow at its tip, the apical region occurs lighter than the basal region when the wing is rapidly moved up and down (Figure 2a). White spots at the tip of the wing (Figure 2b) and additional black subapical contrasts (Figure 2c) result in an amplified signal even in front of a dark shady background, as given in many courtship habitats of long-legged flies. Black-and-white wing tips are realized in males of some long-legged flies (cf. Lunau, 1996
), and many species—even those without wing badges—display wing-waving during courtship (Land, 1993a; Lunau, 1992, 1996; Lunau and Diestelhorst, 2000; Zimmer, 2000). Comparing species without and those with ornamented wing tips, an increase in signal contrast is obvious (cf. Figure 2).
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Contrast amplification of courtship signals is particularly significant in species courting under canopy (Lunau, 1992
, 1996; Zimmer, 2000), in which the light intensity is low and the light spectrum is strongly green-biased (Endler, 1993). Colored cornea lenses, producing the characteristic colors of red and green eyes in many species of the Dolichopodidae (Lunau and Knüttel, 1995), prevent the prevailing wavelength of these habitats from reaching the photoreceptors, hence increasing the contrast of black-and-white signals compared with the background (Bernard, 1971). Based on this observation, Lunau and Knüttel (1995) propose that the corneal filter mechanism optimizes signal perception in courting Dolichopodidae. Many species that do not exhibit sexually dimorphic badges court in direct sunlight (Zimmer, 2000), whereas those displaying signals frequently prefer shady courtship habitats (Lunau, 1996). Even the former species, however, have red- or green-colored eyes. Thus, cornea filters must have evolved in another context (e.g., photoreconversion; Lunau and Knüttel, 1995) but may have been a predisposition for signal display in shady habitats.
Badge display during courtship appears to be related to a species-specific distance to the female. Courting males of P. nobilitatus (2.5 cm; 22% deviation) and Liancalus virens (1.0 cm; 10 % deviation) show small variations in their distance to the potential mate (Figure 3a,b). The former even keep this distance when the female comes closer (Zimmer M, unpublished observations). The estimation of distance may be achieved by motion parallax: In P. nobilitatus, males show tiny fluctuating side-ward movements while displaying their spread wings (cf. Lunau, 1996). Comparing the visual information of both positions may reveal distance information. Land (1993b) points out that males of P. nobilitatus do not come too close when chasing a female in order not to provoke her escape. Males of Tachytrechus consobrinus follow their potential mates on ground in a distance of 1.5 cm (60% deviation) (Figure 3c), but do not display badges nor wing span (Zimmer, 2000).
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Species-specific differences in courtship distance correspond with badge size. The quotients of badge size and its distance to the female's eye during wing-waving is equal in P. nobilitatus and L. virens (Zimmer M, unpublished video analyses), both displaying white wing tips (Lunau, 1992
). In the species Neurigona quadrifasciata and Dolichopus nigricornis, tiny black pretarsae are waved in front of the female's eye in a distance of only few millimeters (Lunau, 1996). Keeping a species-specific badge size–related distance may make an accurate comparison of body size among various males by females possible.
Criteria for mate choice
Assuming that courtship and copulation take place in the same habitat (of course, we cannot exclude the possibility that the majority of copulation takes place in different habitats than those we studied), the small number of observed copulations in relation to the number of observed courtship interactions (Gruhl, 1924; Land, 1993b; Lunau, 1992, 1996; Zimmer, 2000) indicates strong female choice (Lunau, 1992). However, we know little about which criteria females use to choose their mate(s)—at least in part, because copulation has been observed rarely, so that in most cases, we cannot tell what renders a male successful. As mentioned above, male size appears to matter in P. nobilitatus (Lunau, 1992) and possibly in other species.
The size of an adult holometabolous insect, however, does only allow for estimating the nutritive conditions during larval development (see above), but not the present physiological constitution. The latter can be presented through costly dynamic movements (cf. Lunau, 1992; Zahavi, 1977). A predator may display his suitability for foraging by performing sportive flight action. Tracking a female on ground (T. consobrinus; Zimmer, 2000) or on the wing (P. nobilitatus; Land, 1993a) may present common suitability. However, Land (1993b) argues that although females may be selecting for some aspects of physiological constitution (e.g., speed or maneuverability) being of some value to the offspring, predation on soft-bodied, mud-dwelling prey, as in long-legged flies, does not require a particular degree of agility. On the other hand, mud-dwelling long-legged flies also feed on enchytraeid worms, which they tear out of the mud. In some cases, the dolichopodids did so even with the aid of their wings and started flying (Lunau K, unpublished observation)
Courtship in long-legged flies consists of two main components (cf. Table 1). A static element with males presenting and waving spread appendages displays male size, while a dynamic element presents the male's physiological constitution. In many species with males carrying and displaying sexually dimorphic badges, the dynamic element lost its significance in favor of the static element of waving badges that is predominant in most of these species (Table 1).
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Evolution of courtship signals: outlook
Often structures with signal character develop through mimicking existing signals that are already responded to by the receiver in another context ("sensory bias" sensu Ryan, 1990
; Ryan and Rand, 1993; Wickler, 1965). Weldon and Burghardt (2001) recently discussed the importance of mimicry in the evolution of sexual signals and came to conclude that "mimicry is widespread in sexual signaling." According to this statement and Wickler's (1965) early hypothesis, badge-waving during courtship—those badges situated on appendages other than wings are also waved during display (see Lunau, 1996)—could be interpreted as the mimic of another (courtship) signal using the females' sensory bias (cf. Christy, 1995; Ryan, 1990; Ryan and Rand, 1993). It is obvious that courting on the wing (lavish flight maneuvers or hovering) is much more costly than is courting on ground by waving appendages. Given that the costly dynamic elements of courtship display the male's physiological constitution (see above; Lunau, 1992), waving of signals might represent a case of automimicry or a sensory trap (sensu Christy, 1995): Signaling males may mimic their own dynamic display through much less costly waving of badges to their potential mate, and females are trapped by responding to this signal in the same way as to dynamic flight maneuvers.
Even if sexually dimorphic badges are located on appendages other than the wings, males show wing-waving during courtship (Crossley, 1988; Lunau, 1996; Stubbs, 1988), evidently being a rudimentary remnant of the evolutionarily older courtship on the wing (Lunau, 1992). We hypothesize that hovering in front of or above a female (e.g., D. nigricornis) may have been evolutionarily replaced by less costly wing-waving on ground or by waving of badges on any given appendage. Bickel (1990) provided morphological evidence for the shift from mating on the wing to mating on ground. Recent courtship behavior within the superfamily Empidoidea may present an evolutionary trend (cf. Lunau, 1996), beginning with courtship and mating on the wing (in the common ancestor of Dolichopodidae and Empididae), showing intermediate situations of dynamic courtship with single static elements (e.g., D. acuticornis, "pendulum flight" and wing-waving; Zimmer, 2000), equal representation of dynamic and static elements (e.g., T. consobrinus, circular flight and "tandem walk"; Zimmer, 2000), or mainly static courtship with single dynamic elements (e.g., P. nobilitatus, wing-waving and "fly-over"; D. nigricornis, badge-waving and hovering; Lunau, 1996), and finally leading to courtship taking place solely on the ground (e.g., L. virens, wing-waving; N. quadrifasciata, badge-waving; Lunau, 1996).
It is impossible to confirm or reject our hypothesis on phylogenetic grounds, because our knowledge of dolichopodid phylogeny is scarce (Ulrich H, personal communication), and sexually dimorphic badges on different appendages evolved in several subfamilies and genera of long-legged flies independently, and even twice in a single species (see Lunau, 1996). The proposed relation between courtship behavior and badge-display, however, is corroborated by Lunau's (1996) comparison of a total of 23 species of dolichopodid flies. Of nine species with white or black-and-white badges, six show static courtship with badge-waving in shady habitats. Of seven species that do not possess badges, Lunau (1996) presented only one (Medetera sp.) that shows static courtship including wing-waving. In coincidence, those long-legged flies presented herein may be classified (Table 1) as species without badges, predominantly exhibiting dynamic courtship elements (but see Medetera spp.); and those with badges, mainly courting by waving signals.
Further, there seems to be correlation between the display of badges and the courtship habitat (see Lunau, 1996: Table 1). Both D. acuticornis and T. consobrinus court at sunny places and do not display badges, whereas D. nigricornis and N. quadrifasciata, both showing ornamented pre-tarsea, court in shaded habitats under the canopy. Both P. nobilitatus and L. virens are intermediate, displaying their ornamented wing tips in partially shaded places. Males of Medetera jacula and M. truncorum do wave their wings while statically courting in shaded habitats but do not possess badges (Lunau and Diestelhorst, 2000), seemingly opposing the proposed trend in courtship behavior (cf. Table 1). However, light intensity is a key factor initializing courtship behavior in these species (Lunau and Diestelhorst, 2000), and even uniformly gray-colored wings appear fair-tipped when waved rapidly (cf. Figure 2). As is obvious, not all species of Dolichopodidae accord with the proposed evolutionary pathway from courting on wing to displaying badges on ground, but this may be owing to evolutionary convergence between several subfamilies and genera with respect to the existence of badges (see above). The many open questions regarding the relative significance of dynamic and static courtship elements warrant further behavioral and sensory-physiological investigations.
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