Bending for love: losses and gains of sexual dimorphisms are strictly correlated with changes in the mounting position of sepsid flies (Sepsidae: Diptera)
© Puniamoorthy et al; licensee BioMed Central Ltd. 2008
Received: 05 February 2008
Accepted: 21 May 2008
Published: 21 May 2008
Sexually dimorphic structures contribute the largest number of morphological differences between closely related insect species thus implying that these structures evolve fast and are involved in speciation. The current literature focuses on the selective forces that drive these changes, be it 'sexual conflict' or 'female choice'. However, there are only few studies examining the function of sexual dimorphisms and even fewer that investigate how functional changes influence dimorphisms. This is largely due to the paucity of taxa for which the morphology, behavior, and phylogenetic relationships for multiple species are known. Here we present such data for sepsid flies. Sepsids have starkly dimorphic forelegs whose function can be documented under laboratory conditions. We use data from 10 genes to reconstruct the phylogenetic relationships for 33 species and test whether mounting positions are correlated with the presence and absence of sexual dimorphisms in the forelegs.
The phylogenetic tree fully resolves the relationship with 29 of the 31 nodes of the tree having a posterior probability of 1.0. Twenty-eight of the 31 sepsid species have sexually dimorphic forelegs. All 28 species with such forelegs have the same mounting technique whereby the male uses his modified forelegs to grasp the female wingbase. Mapping mounting behavior and foreleg morphology onto the tree reveals that the wing grasp evolved once and was reduced twice. All changes in the mounting behavior are strictly and statistically significantly correlated with the origin and losses of sexually dimorphic legs (concentrated changes test: P < 0.001); i.e., the two species that have independently lost the wing grasp have both also re-evolved monomorphic legs. The wing grasp in these species is replaced with a novel but very similar mounting technique not involving the forelegs: the males bend their abdomens forward and directly establish genital contact to the female. In addition, one of the secondarily monomorphic species, Sepsis secunda, has evolved a new sexual dimorphism, a 'bump' on the dorsal side of the 4th tergite, which is now touching the ventral side of the female abdomen.
Our study reveals that the evolution of sexually dimorphic legs in Sepsidae can only be understood once the function of the legs during mating is considered and the relationships of species with and without sexual dimorphisms are known. We demonstrate that homoplasy in sexually dimorphic structures can be due to homoplasy in mating behavior. We furthermore document that the two species with secondarily monomorphic legs have independently replaced the typical sepsid wing grasp with very similar, new mounting techniques. This suggests that convergent evolution may be common in mating behaviors.
Most closely related species of insects differ exclusively or predominantly with regard to sexually dimorphic traits [1, 2]. This observation implies that these traits evolve fast and are likely to be involved in speciation. Understanding the evolution of sexual dimorphisms is thus crucial for understanding the impressive species diversity of the Insecta, the most speciose clade of multicellular animals . This has made the study of sexual dimorphisms also one of the most important goals of modern evolutionary biology.
Much of the literature focuses on the theoretical issues that drive the sexual selection that is responsible for the origin and maintenance of sexual dimorphisms. Traditionally, the fast evolution of male ornaments had been attributed to selection via female choice . Some empirical data and genetic models had shown that this choice could be driven by direct benefits that increase survivorship [5, 6] or indirect genetic benefits that could improve viability and/or the attractiveness of the offspring [7–12]. However, there is an alternative explanation for the fast evolution of sexual dimorphisms. The unequal investments in gametes by males and females leads to a conflict of interest between the sexes ("sexual conflict" [13, 14]). Males have a higher interest in multiple matings than females and may thus try to coerce females into being polygamous. As a result both sexes can become involved in a sexually antagonistic arms race and evolve mechanisms to gain control over reproduction, regardless of the costs to the other sex [15, 16]. Evidence for such morphological coevolution between male and female reproductive characters has been found across a number of insect groups like Coleoptera (e.g.: Bruchidae and Dytiscidae), Hemiptera (e.g.: Gerridae) and Diptera (e.g.: Empididae and Scathophagidae) [17–25].
However, comparatively little is known about the function of many sexually dimorphic structures and even less is known about how the function of these structures changes over evolutionary time. One reason for this gap in our knowledge is that studying the evolution of function requires concurrent information on the morphology, behavior and phylogeny of multiple species. Only then can functional changes be mapped onto a phylogenetic hypothesis. Unfortunately, for many sexually dimorphic features, only the morphology has been documented in detail and it is often unclear how they are being used. This is particularly so for male genitalia whose function is difficult to study because they interact with internal elements of the female reproductive tract [26, 27]. Even if the function for a particular structure has been studied in great detail, information is usually only available for one or a few species  and if there is information for several species, the phylogenetic relationships are frequently unknown. As a consequence there are only few studies that have documented the evolution of the function of sexually dimorphic structures [18, 29–33]. Here, we use a wealth of information on the morphology and function of the male forelegs for 31 species of Sepsidae (Diptera: Cyclorrhapha) to document how sexual dimorphisms are correlated with mating behavior over evolutionary time.
Sexually dimorphic forelegs are found in the vast majority of sepsid species. However, monomorphic legs are known for six species: Orygma luctuosum Meigen 1830, three species of Perochaeta Duda 1926, Sepsis duplicata Haliday 1838, and S. secunda (Melander et Spuler 1917). Here, we document the foreleg morphology and mounting behavior for two outgroup species, 3 species of Sepsidae with monomorphic legs and 28 species of Sepsidae with sexually dimorphic legs. We reconstruct the phylogenetic relationships among all species based on sequence data for 10 genes, map foreleg morphology and mounting behavior onto the phylogenetic tree, and use a concentrated change test  to establish whether the gains and losses of dimorphic forelegs are correlated with changes in how the forelegs are used during mounting.
The forelegs of ethanol-preserved males and females for the 33 species were removed from the thorax and both the anterior and posterior views of the femur, tibia and trochanter were documented at 200× and 400× magnification using a Hirox microscope and the software Digi-Scale. Drawings of the anterior view of the male femur and trochanter were prepared based on these digital images and comparisons with additional specimens of the same species. The morphology of the male foreleg was then compared to the morphology of the female foreleg. Legs were regarded as sexually monomorphic when male and female forelegs could not be differentiated from each other upon removal from the thorax. For certain select species, a Jeol JSM-7220A Scanning Electron Microscope was used to document additional dimorphic structures.
Rearing and Mating experiments
Laboratory cultures were established for 30 sepsid species based on females collected in the field. The parental cultures were maintained under controlled conditions in incubators and supplied regularly with dung and sugar water. Mating experiments involved virgin flies that were obtained by sexing newly emerged flies within 24 hours of eclosion, keeping males and females as virgins in separate containers. Mating trials were carried out approximately four days after separation. A male and a female were introduced into a small Petri dish and their interaction was recorded using a Leica MZ16A Microscope camera and a VCR. The recording started upon the introduction of both flies into the Petri dish and ended after a successful copulation or after 25 minutes if the males did not attempt to mount. The analog recordings were digitized using the non-linear editing software, Final Cut Pro, and studied frame by frame (1 frame = 1/25 seconds) in order to document the mounting behavior of the different species in detail. The number of recordings per species is listed in the results section. Information on the mating behavior of Saltella sphondylii was obtained from an earlier study by Martin and Hosken .
We reconstructed the relationships among the 33 species based on 10 genes (18S, 28S, AATS, EF1a, Histone 3, 12S, 16S, COI, COII, CYB; for details see ; for Genbank accession numbers [see Additional file 1]). The data set was subjected to a Bayesian analysis as implemented in MrBayes 3.1 . We used MrModeltest  to establish that the GTR + I + G model was favored for all genes by both the Akaike information criterion and hierarchical likelihood ratio testing. The data set was analyzed for 3,000,000 generations and a tree was sampled every 300 generations (=10,000 trees) with a subsequent burn-in of 2500 trees.
Character mapping and concentrated change test
Sexual dimorphism (SD) was scored as a presence/absence character (sexually dimorphic legs absent = 0; present = 1). With regard to the mounting behavior (MB), we used the role of the forelegs to define two character states. State 0 was used to code those species where the male foreleg is not used to grasp the female wing base. Presence of the grasp was coded as character state 1. To test whether changes in behavior and morphology are correlated, we mapped both binary characters onto the phylogenetic tree and used the concentrated change test  as implemented in MacClade 4  using the Sepsidae node as the target clade.
Out of the 31 sepsid species included in this study, the following 28 have sexually dimorphic forelegs. The number of mating trials with successful mountings is listed after the species names: Australosepsis frontalis (Walker, 1860), n = 15; A. niveipennis (Becker, 1903), n = 17; Decachaetophora aeneipes (de Meijere, 1913), n = 10; Dicranosepsis emiliae (Ozerov, 1992), n = 13; D. hamata (de Meijere, 1911), n = 9; Meroplius fukuharai (Iwasa, 1984), n = 5; Nemopoda nitidula (Fallen, 1820), n = 8; Parapaleosepsis plebeia Duda, 1926, n = 15; Saltella sphondylii (Schrank, 1803), Sepsis biflexuosa Strobl, 1893, n = 3; S. cynipsea (Linnaeus, 1758), n = 20;S. dissimilis Brunetti, 1910, n = 20; S. flavimana Meigen, 1826, n = 5; S. fulgens Meigen, 1826, n = 10;S. (Allosepsis) indica Wiedemann, 1824, n = 20; S. monostigma Thomson, 1869, n = 5; S. neocynipsea Melander et Spuler, 1917, n = 5;S. nitens Wiedemann, 1824, n = 7; S. orthocnemis Frey, 1908, n = 6;S. punctum (Fabricius, 1794), n = 10; Themira annulipes (Meigen, 1826), n = 4; T. biloba Andersson, 1975, n = 3; T. flavicoxa Melander et Spuler, 1917, n = 10;T. leachi (Meigen, 1826), n = 3;T. lucida (Staeger, 1844), n = 15;T. minor (Haliday, 1833), n = 15;T. putris (Linnaeus, 1758) n = 15; and T. superba (Haliday, 1833) n = 20. The forelegs of N. nitidula may at first sight appear almost monomorphic, but this is due to the fact that the dimorphic elements are very small. They are thus here documented in a separate micrograph [see Additional file 2]. The three species with sexually monomorphic forelegs in our study were Orygma luctuosum, n = 14, Perochaeta dikowi Ang et al., 2008, n = 20 and Sepsis secunda, n = 8. The two outgroups, Gluma nitida McAlpine, 1991 and Willistoniella pleuropunctata (Wiedemann, 1824) also have monomorphic forelegs (see Figure 2).
Additional file 3: Video A1 (Themira + Nemopoda). Compiled video of mounting clips and foreleg drawings for eight Themira species and Nemopoda nitidula, all with sexually dimorphic forelegs. (MP4 18 MB)
Additional file 4: Video A2 (Australosepsis + Sepsis). Compiled video of mounting clips and foreleg drawings for two Australosepsis species and 10 Sepsis spp., all with sexually dimorphic forelegs. (MP4 19 MB)
Additional file 5: Video A3 (Five genera of sepsid species). Compiled video of mounting clips and foreleg drawings for Decachaetaphora aeneipes, Meroplius fukuharai, Allosepsis indica, Parapaleosepsis plebeia, and two Dicranosepsis species, all with sexually dimorphic forelegs. (MP4 16 MB)
Additional file 6: Video B1 (Orygma luctuosum). Video of mounting clips and foreleg drawing for Orygma luctuosum with sexually monomorphic forelegs. (MP4 8 MB)
Additional file 7: Video B2 (Perochaeta dikowi). Video of mounting clips and foreleg drawing for Perochaeta dikowi with sexually monomorphic forelegs. (MP4 9 MB)
Additional file 8: Video B3 (Sepsis secunda). Video of mounting clips and foreleg drawing for Sepsis secunda with sexually monomorphic forelegs. (MP4 7 MB)
Phylogeny and character evolution
The dataset was subjected to a Bayesian analysis and three independent analyses resulted in similar tree topologies, comparable clade probabilities and substitution model parameters. This suggested that consistent estimates of the posterior probability (PP) distributions had been obtained. Our analysis yielded a very well resolved tree placing Orygma luctuosum as sister group to all the remaining sepsids. All but two nodes had PP values of 1.00 (see Figure 2). The dimorphism and behavior characters were mapped onto the phylogenetic hypothesis. The presence of a sexually dimorphic foreleg is strictly correlated with a mating position involving the wing grasp (concentrated changes test using all of Sepsidae as target clade: two losses in SD with two losses in MB, P = 0.000742). All three changes in the sexual dimorphism character occur on the same branches as the changes in mounting behavior (see Figure 2).
However, the monomorphic legs of Perochaeta dikowi and Sepsis secunda are due to the convergent loss of the male leg armature in two distantly related clades of Sepsidae. A study of the mating behavior reveals that in both species, the forelegs are no longer used for grasping the female wingbase. One can imagine many different ways of replacing the typical sepsid mounting position with a new mounting technique. Yet, P. dikowi and S. secunda have convergently invented near identical, new behaviors. In both species, the male approaches the female from behind. In both species, the males curl their abdomens forward in order to touch the female abdomen with their claspers. In both species, it is only afterwards that the male legs play a minor role in mating: in P. dikowi, males rest their fore tarsi on the female postpronotal callus whilst the males of S. secunda rest their fore tarsi mid-way along the female wing margin. Convergence in morphology is often driven by similarities in habitat and environment. However, there are no aspects of the known autecology of these two species that could explain the convergent evolution of the mounting behavior. Both are typical scavenger flies that use cow dung as breeding substrate. Sepsis secunda is mostly found on open pastures in hot and dry areas of North America, while P. dikowi is only known from forests at mid-elevation sites in the tropics . Furthermore, both species co-occur in the same habitat with other sepsid species that have the "normal" wing grasp.
Evolutionary biologists have long predicted and documented convergence in sexually dimorphic structures . Some authors attribute the convergent evolution of correlated traits to highly conserved patterns of pleiotropy as a potential mechanism for channeling sexual shape dimorphism in Diptera . These hypotheses address the proximate causes for the convergent evolution of sexual dimorphisms and should be complemented with studies that can address the ultimate causation. We suggest that the ultimate reasons for why similar genetic architecture may be utilized to produce convergent dimorphisms are convergent changes in mating behavior. In our case the convergent loss of the wing clamp leads to the convergent loss of the leg dimorphisms. Yet, more intriguing is our finding of convergent evolution of a very specific new mounting behavior which may suggest that highly conserved patterns of pleiotropy and a conserved genetic architecture may also exist for behavior.
We had previously outlined that there is only scant information on how the function of sexually dimorphic traits change over time. Our study helps to fill the void. In the sepsid outgroups and Orygma luctuosum the fore femora and tibiae of the males function like the same structure in most flies. However, in most species of Sepsidae the male forelegs acquire an additional function, i.e., the clamping of the females' wingbase and as a result a new sexual dimorphism evolves. Subsequently, the male forelegs undergo extensive and fast modification as revealed in Figure 1 where all 28 species with sexually dimorphic legs have species-specific modifications. However, as P. dikowi and S. secunda document sexual dimorphisms can also disappear once a structure loses its role in mating behavior.
There are still relatively few studies that document how a behavioral change is correlated with a morphological change [18, 29, 31, 32]. However, a similar case is also known from seaweed flies (Diptera: Coelopidae) where the male foretarsus touches the female antenna during mating . A new morphological structure, a thumbnail-like process, evolved on the basitarsus of males and it must be evolving rapidly because it differs between the different species of Coelopidae . The antlered flies in the genus Phytalmia (Diptera: Tephritidae) provide another example. Males have cuticular projections on the head (antlers) that are used in male-male combat for territory and the complexity of the antler shapes differs quite drastically between species . Species with complex antlers have simple behavioral repertoires whilst those with simpler antlers evolved more complex behaviors involving the fore, mid and hind legs (e.g.: 'wing-locking' and 'stilting' ).
Throughout the discussion, we often implicitly assumed that the change in behavior preceded the loss of the sexual dimorphism although technically the strict correlation between the two traits could also imply the reverse order. However, based on functional considerations it appears unlikely that the reduction of the male leg armature preceded the behavioral change given that the leg armature has been experimentally shown to be important for successful mating in sepsids [37, 44, 51, 76]. Reversing the order of events would also not alter our finding of a strict correlation between mounting behavior and the losses and gains of sexual dimorphisms in Sepsidae.
Several groups of Diptera are important models for investigating sexual conflict. A number of studies have documented coevolution between male and female reproductive characters. For instance, Minder et al. (2005) show that the sperm length in males evolves with the length of spermathecal ducts in females across several species of yellow dung flies (Scathophagidae) . In Drosophila melanogaster (Drosophilidae) female resistance evolves in response to the harm caused by male accessory gland proteins that reduce female fitness and are transferred during copulation [77–80]. Furthermore, Bonduriansky and Rowe (2005) argued that intralocus sexual conflict reduces the heritability of sexual traits in Prochyliza xanthostorna (Piophilidae) and Otronen (1994) suggested that inter-sexual conflict over mating patterns led to repeated copulations in Dryomyza anilis (Dryomyzidae) . In Sepsidae, some authors argued for sexual conflict [38, 47, 82] while others claimed that the evolution of sexual dimorphisms is driven by female choice [35, 37].
In our study, we have identified several elements that are characteristic of an arms race: morphological variation among close relatives as well as a correlation between morphology and behavior. However, we only documented this coevolution within the male sex and in order to document sexual conflict, we would also need to document coevolutionary responses in the females (see ). In the absence of this evidence, we cannot attribute the diversity of male foreleg armature to sexually antagonistic coevolution.
One of the most powerful indirect techniques in evolutionary biology is using the comparative method to investigate convergent evolution . By combining behavioral, morphological, and phylogenetic data, we are here able to show that sexual dimorphisms evolve fast and convergently in Sepsidae. Homoplasy is not restricted to sexual dimorphisms, but also affects mounting behavior. Our study furthermore documents how important it is to study the function of sexually dimorphic structures.
The authors thank numerous colleagues who made intellectual and material contributions for this study. In particular, we would like to mention Torsten Dikow, Michael von Tschirnhaus, Thomas Pape, Guanyang Zhang, Michael Balke, and Wei Song Hwang. This study was financially supported by grant R-154-000-256-112 from the Ministry of Education in Singapore and the US National Science Foundation Grant No. 0334948.
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