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Diptera) and the Cost of Male Copulations in Saltella Sphondylii

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Diptera) and the Cost of Male Copulations in Saltella Sphondylii Org Divers Evol (2011) 11:253–261 DOI 10.1007/s13127-011-0054-2 ORIGINAL ARTICLE New information on the evolution of mating behaviour in Sepsidae (Diptera) and the cost of male copulations in Saltella sphondylii Denise Siew Hoong Tan & Sheng Rong Ng & Rudolf Meier Received: 24 December 2010 /Accepted: 26 July 2011 /Published online: 13 August 2011 # Gesellschaft für Biologische Systematik 2011 Abstract Here we describe the hitherto unknown Introduction details of the highly unusual mating behaviour of Saltella sphondylii—a widely cited model for male TheSepsidae(“black scavenger flies”)are,withap- longevity costs caused by multiple copulations. When proximately 320 described species, a moderately large compared to the known mating behaviour of 28 sepsid family of acalyptrate flies (Diptera: Cyclorrhapha: species, we find five unique behavioural elements based Schizophora) occurring in all zoogeographic regions on frame-by-frame analyses of video-recordings. These (Ozerov 2005). Many species are attracted in large new behaviours are documented with video clips. We numbers to dung, carrion, and other decaying organic suggest that the male longevity costs could be due to substrates where they can be recognized readily based on copulation bouts that involve multiple insertions of a an ant-like habitus that is caused by the constriction of the comparatively membranous phallus into the female. We first two abdominal segments (Pont and Meier 2002). At compare the phallus of the Saltella sphondylii to those the substrate, the females will feed and oviposit while the from three other species (Themira putris, Parapaleosepsis males attempt to copulate with females. Many sepsid plebeia, Sepsis punctum). species are common and breed under laboratory con- ditions, which have made them attractive study objects for Keywords Sepsidae . Mating cost . Mating behaviour . biologists working in different fields ranging from the Longevity. Polyandry. Sexual conflict evolution of sexual dimorphisms (Ang et al. 2008; Blanckenhorn et al. 2007;Eberhard2001a, b, 2002a, b; Ingram et al. 2008; Puniamoorthy et al. 2008), over behaviour (Parker 1972a, b), systematic theory (Laamanen et al. 2005;Meier1997) to developmental biology (Bowsher and Nijhout 2007, 2009), and genomics (Hare Electronic supplementary material The online version of this article et al. 2008). (doi:10.1007/s13127-011-0054-2) contains supplementary material, Many species are strongly sexually dimorphic with which is available to authorized users. regard to forelegs and sternites. The forelegs of males are ’ D. S. H. Tan : S. R. Ng : R. Meier modified for grasping the females wings before and/or Department of Biological Sciences, during copulation (Eberhard 2001b; Ingram et al. 2008; National University of Singapore, Puniamoorthy et al. 2008) while the 4th sternites are often 14 Science Drive 4, modified into brushes that are used to stimulate females. Singapore 117543, Singapore The study of sepsid behaviour started with Hammer (1941) R. Meier (*) who described an “elegant minuet-like” dance in Sepsis University Scholars Programme, duplicata, and Parker (1972a, b) who described an unusual National University of Singapore, precopulatory guarding behaviour for Sepsis cynipsea. This 14 Science Drive 4, Singapore 117543, Singapore species subsequently became widely studied (Blanckenhorn e-mail: [email protected] et al. 2000, 2002; Martin and Hosken 2002; Muhlhauser 254 D.S.H. Tan et al. and Blanckenhorn 2002, 2004; Ward et al. 1992) but it was Materials and methods not until 20 years later that the behaviour of several additional species was described (Eberhard 1999, 2001a, Virgin S. sphondylii flies were separated by sex within 24 h 2002a, c, 2003, 2005; Eberhard and Pereira 1996; of eclosion from a laboratory culture established using Puniamoorthy et al. 2009). This comparative research females collected in Kevelaer (Germany) and maintained as was supported by a better understanding of the phyloge- described in Puniamoorthy et al. (2009). In order to obtain netic relationships within the family (Meier 1995a, b, sexually mature flies, the sexes were housed separately for 1996;Suetal.2008). a period of 5 days before being used for mating trials. Due For several decades, behavioural research on Sepsidae to high mortality in the parental culture, only a relatively was based largely on macroscopic observations although small number of virgins were available for experiments (n= most species are too small (<5 mm) and move too fast 14 individuals) that involved one male and one female. to observe the details without the use of a microscope. Note that, based on previous experience (see Puniamoorthy Recently, observing and/or video-taping mating behav- et al. 2009), a small number of successful mating trials is iour through microscopes has revealed new insights sufficient for describing the qualitative elements of sepsid (Ang et al. 2008;Eberhard2001a, b, 2002a, b, c, 2003), mating behaviour. Recordings began upon the introduction and demonstrated that the behaviour of sepsids is of both flies into the same Petri dish and were terminated surprisingly diverse (Puniamoorthy et al. 2009). Many after the male voluntarily dismounted from the female and insects rely heavily on olfactory and auditory species- the pair remained separate for more than 1 min. The specific cues (Doi et al. 2001;Freyetal.1992; Henry et recordings were analysed frame-by-frame (1 frame=1/25th al. 2002), but Puniamoorthy et al. found that in sepsids of a second) and behavioural elements were noted, even the visible male courtship behaviour was species- categorized and described. We coded known behaviours as specific. Saltella sphondylii (Schrank 1803)wasnot in Puniamoorthy et al. (2009), while new behaviours were included in Puniamoorthy et al.’s studies although Martin either coded as new states or new characters. We then and Hosken’s(2004) and Schulze’s(1999)macroscopic mapped the 33 characters (Table 1, and see character observations suggested that the mating behaviour of this descriptions in Appendix) on the molecular phylogenetic species might be very unusual. They noticed postcopula- hypothesis in Puniamoorthy et al. (2008) with the exception tory guarding, a lack of female resistance to mating, no of Toxopoda sp., which was missing in this analysis and overt courtship behaviour, and short and intermittent whose position was based on Su et al. (2008). Character copulations (Martin and Hosken 2004:358:“i.e., males optimisation procedures follow Puniamoorthy et al. (2009). engage and disengage genitalia”). This contrasts sharply In order to determine levels of homoplasy, we recorded tree with other sepsid species that lack postcopulatory guarding, length and consistency index with and without S. sphondylii. have strong female resistance, extensive courtship In addition to the behavioural research, we also extracted behaviour, and engage genitalia only once in a copulation the phallus of male S. sphondylii, Themira putris (Lin- bout (Puniamoorthy et al. 2009). Here, we describe the naeus, 1758), Parapaleosepsis plebeia (de Meijere, 1906), behaviour in detail and update a matrix of behavioural and Sepsis punctum (Fabricius, 1794) and studied their characters published in Puniamoorthy et al. (2009) morphology under a scanning electron microscope (SEM). Additional information on S. sphondylii is particularly These species represent major branches on the sepsid tree important because life history costs related to courtship (Fig. 1) and copulation have been extensively documented and quantified mostly for females while fewer authors have investigated male costs (but see Burton-Chellew et al. Results and discussion 2007; Cordts and Partridge 1996; Ferkau and Fischer 2006; Kotiaho and Simmons 2003; Oliver and Cordero The mating behaviour of S. sphondylii is very unusual for 2009; Paukku and Kotiaho 2005; Prowse and Partridge sepsids in that males in all mating trials copulated 2–3 1997; South et al. 2009). One prominent exception is times over a period of 10–18 minutes without dismounting Martin and Hosken’s(2004) demonstration of a negative the female. The copulation duration is the shortest (3– correlation between the number of copulations and 4 mins) known for any sepsid species. Note that we only longevity in S. sphondylii males. On average, virgin males count periods of genital contact that lasted for more than lived 28 days while a single copulation reduced longevity 2 mins as proper copulations. In between these copulations by4days,twoby6,fourby8,andsixby12days. up to five more sporadic and short instances of genital However, Martin and Hosken’s(2004) description lacks contact occurred that lasted from a few seconds to just over information on behavioural details that can be observed 1 min. At least some of these interactions included the only under a microscope. insertion of male genitalia into the female. Martin and Cost of male copulations in Table 1 Behavioural character matrix modified from Puniamoorthy et al. (2009) with new information for Saltella sphondylii List of Species Behavioural characters 123456789101112131415161718192021222324252627282930313233 Saltella sphondylii Allosepsis indica 0000221220 –– –000 00000 0– 00– 00– 00 00 Australosepsis frontalis 10001– 10–– – – – 000 10000 0– 02– 00– 00 00 Australosepsis niveipennis 10001– 0101 02 0000 00000 11 02– 0100000 Dechaetaphora aeneipes 0000201102 – 2 1200 ?0003 10&102– 0100100 Dicranosepsis sp.1 10001– 1 1 0 0&1 0 0 0 0 0 1&3 0 0 0 0 0 1 1 1 0 – 0100000 Dicranosepsis
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