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Orthoptera: Caelifera: Acrididae) Zoologica Scripta Evolution of acoustic communication in the Gomphocerinae (Orthoptera: Caelifera: Acrididae) ROMAIN NATTIER,TONY ROBILLARD,CHRISTIANE AMEDEGNATO,ARNAUD COULOUX,CORINNE CRUAUD &LAURE DESUTTER-GRANDCOLAS Submitted: 6 January 2011 Nattier, R., Robillard, T., Amedegnato, C., Couloux, A., Cruaud, C. & Desutter-Grandc- Accepted: 2 June 2011 olas, L. (2011). Evolution of acoustic communication in the Gomphocerinae (Orthoptera: doi:10.1111/j.1463-6409.2011.00485.x Caelifera: Acrididae). — Zoologica Scripta, 40, 479–497. We used a phylogenetic analysis to study the communication behaviour in the Gompho- cerinae (Insecta, Orthoptera, Acrididae), which are characterised by their stridulatory appa- ratus and a diversified acoustic repertoire. Song-emitting behaviour, together with the general description, temporal dimension and amplitude of signals were used to describe the calling song of 34 species, resulting in a matrix of 39 acoustic characters. A phylogeny using 59 gomphocerine species and two outgroups was built based on four mitochondrial markers and the acoustic characters. Based on acoustic character optimisations, ancestral calling song was reconstructed and the evolution of calling song is discussed, with a com- parison to courtship behaviours. Our results show a dynamic process of calling song evolu- tion and underline a balance between calling and courtship diversity leading to two mating strategies corresponding to two major clades in the phylogeny. Corresponding author: Romain Nattier, Departement Systematique et Evolution, Museum National d’Histoire Naturelle, UMR 7205 CNRS (OSEB), Case postale 50 (Entomologie), 75231 Paris Cedex, France. E-mail:[email protected] Tony Robillard, Christiane Amedegnato (deceased), and Laure Desutter-Grandcolas, De´partement Syste´matique et Evolution, Muse´um National d’Histoire Naturelle, UMR 7205 CNRS (OSEB), Case postale 50 (Entomologie), 75231 Paris Cedex, France. E-mails: [email protected], amedeg@ mnhn.fr, [email protected] Arnaud Couloux and Corinne Cruaud, Genoscope, Centre National de Sequencage, 2, rue Gaston Cremieux, CP5706, 91057 Evry Cedex, France. E-mails: [email protected], cruaud@ genoscope.cns.fr Introduction could be mostly under the influence of sexual selection For animals communicating using sounds, acoustic signals (Shaw & Herlihy 2000; Robinson & Hall 2002). In con- usually play a major role in the process of pair formation trast, singing Caelifera (grasshoppers) perform more (Bradbury & Vehrencamp 1998). Among the rich behav- diverse behaviours prior to mating. In the subfamily Gom- iours commonly used during reproduction, calling and phocerinae (Acrididae) more specifically, many species courtship songs are of special interest, as they precede emit calling songs, which are sufficiently specific to be copulation and are directly involved in species recogni- used for species identification in the field (Faber 1953; von tion and mate choice. Calling song allows individuals of Helversen 1986; Ragge et al. 1990; Ragge & Reynolds one sex, usually the male, to attract individuals of the 1998; Savitsky 2007), but they also perform very complex, other sex at long range, whereas courtship song is per- often multimodal, courtship behaviours involving formed when potential mates are close together to initi- sequences of acoustic, vibrational and ⁄ or visual signals ate mating sensu stricto (Alexander 1967; Robinson & (Jacobs 1953; Otte 1970, 1972; Elsner 1974a; Bull 1979; Hall 2002). Riede 1983, 1986; Elsner & Wasser 1995; Vedenina & The process of acoustic communication in reproduction von Helversen 2003; Vedenina et al. 2007). Although other is amply documented in ensiferan insects (crickets and prereproductive isolation mechanisms such as habitat katydids) (Gerhardt & Huber 2002): Males of singing choice or phenology have been documented in Gompho- Ensifera emit specific calling songs used for species recog- cerinae (Blondheim 1990; Savitsky 2000; Bailey et al. nition, while courtship songs are generally less specific and 2004), the different contributions of calling and courtship ª 2011 The Authors d Zoologica Scripta ª 2011 The Norwegian Academy of Science and Letters, 40, 5, September 2011, pp 479–497 479 Evolution of acoustic communication in the Gomphocerinae d R. Nattier et al. songs may represent a major factor of species isolation in steppe, savannah and meadow (Otte 1981), but reach their this clade (Vedenina & von Helversen 2003). maximal taxonomic diversity in the Palearctic and Afro- This is however far from homogeneous within Gompho- tropical areas (Otte 1995). The taxonomy used in the pres- cerinae (Faber 1953; von Helversen 1986; Berger 2008): In ent paper follows the online version of the Orthoptera Chorthippus species, for example, the most specific behav- Species File (Eades & Otte 2008), except for the genus iours are the calling songs, which tend to be very complex; Megalacobothrus, which is considered a subgenus of Chor- the courtship songs are generally not much distinct from thippus by most authors (e.g. Jago 1971). the calling song and have no original components of their Two molecular phylogenetic hypotheses have been pro- own (Faber 1953; von Helversen 1986; Savitsky 2000). In posed recently for the Gomphocerinae, based on limited contrast, Stenobothrus species produce rather unspecific taxonomic samples: Bugrov et al. (2006) considered 25 spe- calling songs, but each species shows a unique and usually cies (11 genera, six tribes) from Eurasian origin only, while complex courtship song associated with multimodal signals Contreras & Chapco (2006) used 32 species (21 genera, (Berger 2008). Except for a hypothesis of gradual transfor- eight tribes) from North America and Europe. mation that was proposed without a phylogenetic reference In the present study, the choice of species was designed (von Helversen & von Helversen 1994), the evolution of to combine these previous analyses and to improve the gomphocerine acoustic communication has never been sampling according to gomphocerine diversity. We sam- analysed in a phylogenetic framework. Their acoustic com- pled all the species documented by Bugrov et al. (2006) munication, however, is well known in terms of neurophys- and Contreras & Chapco (2006) and added four species iology (Elsner 1974a,b), ethology (Otte 1970; Reinhold belonging to poorly represented genera (Euchorthippus dec- et al. 2002) and bioacoustics (Stumpner & von Helversen livus, Myrmeleotettix maculatus, Omocestus rufipes and Steno- 1994; von Helversen et al. 2004), and phylogenetic hypoth- bothrus stigmaticus). We also considered Stethophyma eses have recently been proposed for the subfamily (Bugrov grossum because its position within the Acrididae is uncer- et al. 2006; Contreras & Chapco 2006). As suggested by tain (Otte 1981; Vickery & Kevan 1985; Storozhenko & Berger (2008), who studied the evolution of courtship Otte 1994; Contreras & Chapco 2006). The ingroup con- behaviour in Stenobothrus, it is necessary to study the sists of 59 species (Table 1) from Palearctic and Nearctic behavioural repertoire of each species in a comparative way areas, representing 29 genera and nine tribes. Although to consider the evolution of calling and courtship songs at more extended studies are necessary to address the broad the scale of the whole subfamily. relationships within the Acrididae and define the precise In the present study, we reconstruct the most extended outlines of the Gomphocerinae, our study involves the phylogeny of gomphocerine grasshoppers performed up to most extended sampling ever gathered for this group. now, using both molecular and acoustic data sets. Our Following previous studies, we use Locusta migratoria main purpose is to study the evolution of the calling songs (Caelifera, Acrididae) and Ruspolia nitidula (Ensifera, Tet- in this subfamily. We focus on the calling signals, which tigonidae) as outgroups for the phylogenetic analyses. constitute the cornerstone of the acoustic system in these insects and are sufficiently known and documented to be Character sampling included in a phylogenetic matrix. We address the follow- Molecular characters. The molecular matrix includes ing questions to characterise the patterns of evolution and sequences from four fragments of coding mitochondrial main evolutionary trends: Were calling songs ancestrally genes: Cytochrome b (cytb, 900 bp), Cytochrome c Oxidase 1 elaborate or simple? Did they evolve progressively toward (CO1, 750 bp), Cytochrome c Oxidase 2 (CO2, 380 bp) complexity, once or multiple times? Finally, based on a NADH dehydrogenase 5 (ND5, 650 bp). All newly generated broad comparison of calling songs with courtship behav- sequences are deposited in GenBank (Table 1). iours, we propose a general pattern for the evolution of mating behaviour related to acoustic communication. Acoustic characters. We analysed recordings of male calling songs for 34 ingroup species from various sources that Materials and methods were fully documented for recording conditions (Table 1). Sampling The acoustic sampling is representative of the acoustic Taxon sampling. Gomphocerinae is the second largest sub- diversity in the Gomphocerinae (R. Nattier personal family of Acrididae (Orthoptera, Caelifera), with about observation). We analysed a sample of songs emitted by 2000 species, 190 genera and 19 tribes (Eades & Otte 1–5 different individuals per species (mean = 3.25 individ- 2008). They are distributed worldwide, except in Australia uals per species), for a total of 104 individual
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