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Araneae: Salticidae) Biological Journal of the Linnean Society, 2012, 105, 522–547. With 13 figures Orchestrating the score: complex multimodal courtship in the Habronattus coecatus group of Habronattus jumping spiders (Araneae: Salticidae) DAMIAN O. ELIAS1*, WAYNE P. MADDISON2, CHRISTINA PECKMEZIAN3, MADELINE B. GIRARD1 and ANDREW C. MASON3 1Department of Environmental Science, Policy and Management, University of California, Berkeley, Berkeley, CA 94720, USA 2Departments of Zoology and Botany, University of British Columbia, Vancouver, BC V6T 1Z4, Canada 3Integrative Behaviour and Neuroscience Group, University of Toronto Scarborough, Toronto, ON, M1C 1A4, Canada Received 21 July 2011; revised 28 September 2011; accepted for publication 28 September 2011bij_1817 522..547 Jumping spiders in the genus Habronattus use complex multimodal signals during courtship displays. In the present study, we describe multimodal displays from the Habronattus coecatus clade, comprising a diverse group of 23 described species. Habronattus coecatus group displays are made up of sex-specific ornamentation and temporally coordinated combinations of motion displays and vibratory songs. Vibratory songs are complex, consisting of up to 20 elements organized in functional groupings (motifs) that change as courtship progresses. This temporal structuring of displays is analogous to a musical composition. Vibratory elements are associated with movement displays involving coloured and patterned ornaments on the male body. We describe general patterns of multimodal displays for 11 species including one, Habronattus borealis, which appears to have lost complex display behaviour. Habronattus coecatus group courtship is one of the most complex communication systems yet described in arthropods and this group may reveal important factors driving the evolution of complex signals. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 522–547. ADDITIONAL KEYWORDS: antagonistic coevolution – behaviour – female choice – seismic communication – sexual selection – substrate-borne vibration. INTRODUCTION display behaviour is generally considered to be simple, sexual signalling in some taxa rivals their Complex sexual displays have long stimulated the vertebrate counterparts. In one of the most spectacu- imagination of naturalists and been the focus of bio- lar examples of complex signalling, mantis shrimp logical research. Classic examples include the ornate males signal using combinations of colourful, polar- plumage and ‘dances’ of male birds-of-paradise (Frith ized ornaments, and water-borne vibrations (Patek & & Beehler, 1998; Irestedt et al., 2009), the elaborate Caldwell, 2006; Marshall, Cronin & Kleinlogel, 2007; bowers used by male bowerbirds (Borgia, 1995; Chiou et al., 2008; Kleinlogel & Marshall, 2009). In Doucet & Montgomerie, 2003; Frith & Frith, 2004; the present study, we document elaborate signalling Endler et al., 2005), and the dance ‘struts’, vocaliza- in jumping spiders, rivalling that of bird groups such tions, and plumage of sage grouse males (Gibson, as the birds-of-paradise. 1996; Krakauer et al., 2009). Although arthropod Numerous adaptive hypotheses for complexity in sexual displays have been proposed, including mul- tiple sources of quality information (‘multiple mes- sages’), compensation for environmental variation, *Corresponding author. E-mail: [email protected] and increased efficacy of signal transmission and 522 © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 522–547 MULTIMODAL COURTSHIP IN HABRONATTUS 523 reception (Guilford & Dawkins, 1993; Rowe, 1999; one species, Habronattus dossenus, produce complex Hebets & Papaj, 2005; Partan & Marler, 2005). These multicomponent substrate-borne signals (Elias et al., hypotheses, however, do not adequately address the 2003). In addition, unique, independently produced evolution of highly complex displays because, under visual signals are precisely coordinated with distinct most conditions, highly complex signals are predicted substrate-borne signals (Elias et al., 2006d). Displays not to evolve (Pomiankowski & Iwasa, 1993; Iwasa & in H. dossenus follow sets of stereotyped patterns that Pomiankowski, 1994). For example, as the value of change and progress through time. Courtship initially new information in signals reaches an asymptote (in starts several body lengths away as males produce terms of each information bit’s contribution to the visual motion displays. As males approach females, reduction of uncertainty), the theoretical costs of they begin to perform multimodal displays (visual producing/decoding new information continues to plus vibration) and males gradually add new multi- accelerate, leading to the prediction that economi- modal display elements, ramping up the complexity cally, communication systems have severe constraints (i.e. number of different elements used) and intensity (Ay & Polani, 2008). In addition, the physiology of (i.e. rate at which different elements are presented) of sensory neurones (i.e. habituation, adaptation), as the display (Elias et al., 2003). well as the memory capabilities of receivers, may set Phylogenetic analyses have resolved Habronattus limits to the amount of information that animals are into a series of discrete species groups (Griswold, able to effectively detect and process (Rowe, 1999; 1987; Hedin & Maddison, 2001; Maddison & Hedin, Hillis et al., 2002; Mishra, Martinez & Hillyard, 2003; Hedin & Lowder, 2009). One of the major sup- 2008). In a recent meta-analysis, it was shown that, ported phylogenetic clades is the Habronattus coeca- across taxa, selection for shorter duration signals was tus group, consisting of at least 23 described taxa stronger than longer duration signals, suggesting the (Griswold, 1987; Maddison & Hedin, 2003). Mono- existence of constraints for evaluating complex phyly of this group is strongly supported and males of signals (Reinhold, 2011). The factors driving the evo- this group include the most elaborate ornamentation lution of highly complex displays remain an open of all Habronattus species groups, as well as the question. highest number of nominal species (Griswold, 1987; Jumping spiders use visual and vibratory signals Maddison & Hedin, 2003). Previous studies of court- during courtship. Jumping spiders have visual ship signals indicated the presence of substrate-borne systems with high spatial acuity (Land, 1985) and vibrations in one H. coecatus group species, Habr- well developed colour vision (Forster, 1982a, b; Land, onattus schlingerii (Elias et al., 2005) and in another 1985; Koyanagi et al., 2008). Not unexpectedly, species, Habronattus borealis, distinct populations jumping spiders use vision as the dominant sense in differed in the number of stereotyped displays used a variety of contexts (predation: Harland & Jackson, (Richman & Cutler, 1998). 2002; Nelson & Jackson, 2009; navigation: Hill, 1979; In the present study, we characterized in detail the Hoefler & Jakob, 2006; communication: Uhl & Elias, multimodal courtship displays of 11 species in the 2011). In some jumping spiders, males use substrate- H. coecatus group (male substrate-borne vibrations borne vibration signals (Jackson, 1980; Edwards, and accompanying motion displays). We observed that 1981; Maddison & Stratton, 1988a, b; Noordam, 2002; the majority of species had multiple elaborate visual Elias et al., 2003, 2006b, 2008) that are crucial to ornaments, complex multicomponent vibratory songs, mating success (Elias et al., 2005, 2010; Elias, Hebets and coordinated multimodal displays. Courtship & Hoy, 2006a; Sivalinghem et al., 2010). signals in the H. coecatus group are quintessential Among the best studied jumping spiders are those examples of terrestrial arthropod sexual displays and of the genus Habronattus. These small (body length are among the most highly complex displays found in 5–8 mm) jumping spiders live on sticks, rocks, and the entire animal kingdom. The present study sets dry leaves on exposed open ground. Habronattus is the stage for future work on signal evolution and one of the most diverse genera in jumping spiders behaviour in the group. (approximately 100 described species) and includes species with some of the most elaborate visual orna- mentation described (Peckham & Peckham, 1889, MATERIAL AND METHODS 1890; Griswold, 1987; Maddison & McMahon, 2000; Maddison & Hedin, 2003). Sexual selection on male SPECIES SAMPLING secondary characteristics has been implicated as an Habronattus coecatus group members were sampled important driver of diversification throughout the throughout North America (see Supporting informa- group (Maddison & McMahon, 2000; Masta, 2000; tion, Doc. S1). In total, we report on complete court- Masta & Maddison, 2002; Hebets & Maddison, 2005; ship displays from 11 different species representing Elias et al., 2006a; Hedin & Lowder, 2009). Males in the majority of fauna found in the USA. We measured © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 522–547 524 D. O. ELIAS ET AL. displays from two to seven individuals per species and were placed in the freezer. Female models were typi- each individual was sampled once. Additionally, we cally used for a maximum of 3 days (Girard et al., report visual displays for four other species (see Sup- 2011). porting information, Table S1). Voucher specimens The general progression of courtship in the are currently housed in the personal collection H. coecatus
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