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 multiple sources of quality information (‘multiple messages’), 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 ornamentation 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 group is highly stereotyped, with indi- of D.O.E. and will ultimately be deposited at the vidual variation mainly occurring in the number of California Academy of Sciences. repeated elements, motifs, and movements (see below). The main variation across species occurs in the types of elements used. The present study COURTSHIP RECORDING AND ANALYSIS aimed to describe courtship in the entire H. coecatus All courtship behaviour was videotaped ‘face on’ group and we report on idealized ‘typical’ courtship (30 frames/s; Navitar Zoom 7000 lens, JAI CV-S3200 and focus on between species differences in signal CCD camera) and substrate-borne vibrations elements and not on individual variation in displays recorded using a Laser Doppler Vibrometer (LDV) within species. (Polytec OFV 3001 controller, OFV 511 sensor head). Only displays that progressed to the male mounting Video and substrate-borne vibrations were recorded the female model were analyzed. Male displays were on a digital VCR (Sony DVCAM DSR-20 digital VCR; scored first by qualitatively assigning all distinct sampling rate of 48 100 kHz). behaviours to signal element categories and recording Mating recordings were conducted on a custom- the order of all courtship elements (timeline) for each made arena consisting of a piece of nylon fabric individual male. Next, each individual timeline was stretched on a circular wooden needlepoint frame condensed by coding repeated elements to produce an (diameter 27 cm). The arena was positioned firmly at annotated description for each individual (see below). the center of a larger circular (diameter 35 cm) rotat- The reported descriptions describe ‘typical’ displays ing platform on wooden dowels (height 7.5 cm). Glued produced by the majority of individuals. Finally, each to the top of the larger platform was a belt-pulley qualitative signal element was quantified. For quan- system with one drum attached at the center of the tification of vibratory displays, five to ten signals for platform. On top of the centrally placed drum, we every individual were averaged and the average attached a small piece of cork to which female models signal properties are reported for individuals. All could be attached (see below). At the outermost part signal analyses were performed using custom written of the larger platform, we placed the second drum of scripts in MATLAB, version 7 (Mathworks Inc.) and the belt-pulley system and, by rotating the outermost SOUNDFORGE (Sony). Vibratory traces are pre- drum, we were able to turn the innermost drum. sented as RMS waveforms (2.1 kHz sampling) for Small pieces of reflective tape (1 mm2) were placed at clarity. Vibratory display measurements are reported the center of the arena to serve as measurement in the Supporting information (Table S2–S8). points for the LDV. Nylon fabric passes all relevant Our experimental set-up made recording early por- frequencies with no significant distortion (Elias et al., tions of courtship display challenging and several of 2006e). Arenas were cleaned with 75% ethanol our recordings had shortened or missing Intro por- between trials. tions (see below). In the field, males approach females Female models were used to entice males to court. from longer distances and likely always include intro- Conspecific female models were first prepared by ductory portions. The close proximity at which dis- taking freshly dead females and waxing them to an plays began may be the reason that many of the insect pin ventrally on the cephalothorax. The insect courtship displays began with Introductory Bursts pin was inserted into the cork glued to the central (In; see below) or Ticks (Ti; see below). We report any drum of the belt-pulley system. This arrangement Intro elements observed, even if the majority of males allowed us to move female models in a ‘lifelike’ did not produce this behaviour. manner, which helped to entice males to court. Males were dropped into the arena and allowed to freely wander. Females were rotated until males noticed NOMENCLATURE them and began to approach. When males began to To describe complex displays, we have adopted approach, we positioned the female as if she was aspects of mathematical and musical nomenclature in observing the courting male. Using the larger rotat- our descriptions. Displays should be read as algebraic ing platform, we rotated the arena to provide a equations. We refer to complete courtship displays as ‘female’s eye view’ of the male to the regular speed display compositions. Display compositions are made camera. If males stopped courting for 30 s, females up of movements comprising stereotyped motifs that were rotated slightly to draw the male’s attention repeat in each movement. Motifs are made up of once again. At the end of each day, female models signal element ‘notes’. Signal elements are produced

(a)

40 20 144 4 3 17 12 8 2 4 3 (b) TiEv Ti EvTi EvRd Rd Rd Rd Fl Ti Ev Ti Ev Ti Ev Rd Rd Rd Rd Fl sw sw 3 sw sw 3 (c) Ti** Ev Ti** Ev Ti** Ev Rd Rd* Fl ** Ti** Ev ** Rd Rd* Fl Rdsw Rd* sw Ti Ev Ti EvRdsw Rd* sw

3 3 (d) (Rd Rd*)* (Ti**Ev)* (Rdsw Rd*)* Fl (Ti**Ev)* sw Fl

3 3 (e) (Ti**Ev)* (Rd Rd*)* Fl (Ti**Ev)* (Rd Rd*)* Fl sw sw

3 (f) ((Ti**Ev)* (Rd Rd*)* Fl )* sw

Figure 1. Nomenclature of spider displays. Example of notation of a jumping spider vibratory display. Row A, vibration waveform (RMS amplitude versus time) of a ‘typical’ 2nd movement. The sequence of vibrational display elements can be transcribed as a list of element identifiers (letter codes) with superscripts representing the number of repetitions for each element. Rows B–F, repeating patterns are iteratively reduced until a simplified overall description of the entire sequence is constructed (F). Low numbers of repetitions (2–9) are indicated by a single asterisk (*); higher numbers of repetitions (10–30) are indicated by a double asterisk (**). Numerals represent stereotyped number of repetitions. Display summaries should be read as algebraic equations. by males in the context of courtship behaviour and higher in frequency and typically have a broadband are defined by unique combinations of vibrational structure (see below). energy and/or visual motions. Superscripts in display compositions denote how often signal elements occur; for example, an integral number (x) describes the RESULTS typical repetition of the signal element; a single Habronattus coecatus group male multimodal dis- asterix (*) denotes a small variable repetition number plays consisted of visual ornaments, motion displays, typically in the range 2–9; and a double asterix (**) and substrate-borne vibratory songs. Below, we denotes a large variable repetition number typically describe motion and vibratory displays; we also in the range 10–30. For example, the notation: describe the ornamentation of one species (H. coeca- (((A**B)*(CD*)*)**E3)* should be read as a display tus). Descriptions of vibratory songs include average motif where the A element is first repeated many dominant frequencies (± SD), as well as minimum times (10–30) [A**] followed by a single B element and maximum frequencies (10 dB below peak ampli- [B]. This set of A and B elements is repeated two to tude) (Table S2–S8). The majority of spider songs eight times [(A**B)*] and is then followed by a single were broadband (i.e. broad frequency spectrum) and C element followed by two to nine repetitions of the D the range of frequencies is probably the most salient element [D*]. This set of C and D elements is then feature of spider signals. Some signals are relatively repeated two to nine times [(CD*)*] and is followed tonal in structure and, for those signals, we included by the E element which is repeated three times [E3]. average fundamental frequency (see Supporting infor- The entire set of elements is then repeated again two mation Table S2–S8). For edited courtship recordings to nine times [((A**B)*(CD*)*E3or4)*]. An example of of select H. coecatus group species, see http://nature. this process is provided in Figure 1. berkeley.edu/eliaslab/coecatusgroup.html. If an integral superscript (x) contains a comma, this denotes a gap between signal element repetitions; for example, the superscript ‘2,1’ would denote two ele- MULTIMODAL DISPLAYS (MOTION DISPLAYS AND ments in rapid succession followed by a pause, fol- SUBSTRATE-BORNE VIBRATIONS) lowed by one element repetition. Subscripts denote Overall display progression (movements) signal elements which are distinct but variations on a In general, H. coecatus group display compositions theme; for example, both Walo and Wahi denote a occurred in 4–5 movements. Introductory Movements multimodal behaviour where the male extends its (Intro) started the entire display composition. Post- forelegs forward, waving them rapidly at the same mount (PM) movements were the finale of the time as producing a sustained vibratory signal. Walo display, just before a copulation attempt. Between displays are low in frequency and typically have a the Intro and PM were movements consisting of spe- relatively tonal structure, whereas Wahi displays are cific motifs (or sets of motifs). In general, the second

Introductory Concluding Movement 1: x x:y y:z Movement

Intro Tick-Rev Motif 3rd leg Motif Foreleg Wave Motif Pre-Mount Motif 3 Ou Et In (Ti** Ev )** Bo lo (Rdsw Rd* )* (Rdsw po Rd* )* )** * * Ra (Sflo Wa lo (Sfhi Cosi Comu Wa lo)** Pr

2 3 3 3 Fl Fl Ba Rd sw Fl Thump Burst Bridge Thump Burst Bridge Reprise Bridge

Figure 2. Summary of idealized display of a typical coecatus group member. Displays consist of several movements punctuated by one of two bridges [Thump Burst (TB) Bridge, Green double bold line; Reprise Bridge (RB), yellow double bold line]. Repeat sign notation (double bar with dots) indicates the beginning (dots on right of double bar, almost always the Tick-Rev Motif) and end of a movement (dots on left of the double bar, always a TB or RB). The number of repeated movements is highly variable between individuals but more motifs are added as courtship progresses. If a display composition is made up of 1 to z movements, then the 1st movement is always the Intro movement. This is followed by a number of movements made up of Tick-Rev Motifs alone (movement 2 to movement x + 1) punctuated by a single TB Bridge. These sets of movements would then be followed by a number of movements made of Tick-Rev Motifs and 3rd Leg Motifs (movement x + 1 to movement y) punctuated by a single TB Bridge. These sets of movements would then be followed by a number of movements made up of Tick-Rev Motifs, 3rd Leg Motifs, and Foreleg Wave Motifs (movement y + 1 to movement z), punctuated by a single RB Bridge. The concluding movement is always a series of Tick-Rev Motifs, 3rd Leg Motifs, Foreleg Wave Motifs, concluded by a single Pre-Mount Motif. Different colours represent different motifs or bridges. 1st Row, RMS amplitude of vibrational song motifs; 2nd row, song ‘score’ of display composition with notations. movement was comprised of one motif and, in each transitional period. Below, we describe typical motifs subsequent movement, more motifs were added until and signal elements. the ﬁnal PM movement. In total, there were seven Figure 2 shows an example of an idealized complete motifs that comprised display compositions, with two display, demonstrating several movements with their of these motifs serving as bridges. The seven motifs associated motifs. The number of movements in each in order were: Introductory Motif (Intro), Tick-Rev display composition was variable between males of Motif (Tick-Rev), 3rd Leg Motif (3rd-Pop, 3rd-Shake), the same species. It is highly likely that this would Thump Burst Bridge (TB), Foreleg Wave Motif have been even more variable if females were alive (S-Wave-Reach), Reprise Bridge (RB), and Post- and allowed to interact with males. Regardless, as a mount Motif (PM). Introductory Motifs only occurred general rule, motif and movement order was stereo- in the introductory movement of the display compo- typed (Fig. 2) (with the exception of H. borealis; see sition. PM Motifs only occurred in the ﬁnale of the below) and more variation occurred in the length and display composition. Tick-Rev Motifs were the most number of movements, as well as the repetition rate common motif in H. coecatus group displays and were of signal elements within motifs, than in the overall included in most of the movements (excluding the order and make-up of motifs. In our scoring of display Introductory and PM movements). TBs bridged mul- compositions, we found that early movements had tiple Tick-Rev Motifs with each other and 3rd Leg fewer motifs. Motifs with Tick-Rev Motifs. RBs bridged Foreleg Wave Motifs with Tick-Rev Motifs. As a general rule, INTRODUCTORY MOTIF (FIG.3) the repetition of motifs was greater in earlier movements. Within each motif, transitions between signal Intro Motifs were made up of three display elements, ‘notes’ (elements) were not abrupt and, instead, Bounces (Ou), Settles (Et), and Introductory Flicks included a short period where properties of both (IF). The order of a typical complete introductory signal elements were evident (typically between two motif was: to four notes). For the purposes of the present Introductory Motif: Ou* Et IFx (where x is an study, we did not analyze any elements from this integral number)

The first signal element was a Bounce (Ou). Ous Tick-Rev Motifs) and were a major part of all move- begin at a long distance when the male first detected ments, with the exception of introductory and PM the presence of a female and consisted of stereotyped movements. Tick-Rev Motifs consisted of two signal combinations of ‘dance’ motions and no associated element types, Ticks (Ti) and Revs (Ev). The order of substrate-borne vibrations. As the male approached a typical Tick-Rev Motif was: the female, he moved (bounced) his body up and down Tick-Rev Motif: (Ti** Ev)** repeatedly, at the same time as alternately waving his palps diagonally (as they were held above the The first signal type was a Tick (Ti; Fig. 4). Ti dis- femora of the first legs), his forelegs up and down and plays had no associated motions and consisted of his 3rd legs back and forth in synchrony (Fig. 3.1a). short, broadband vibrations (see Supporting informa- Ous were repeated until the male got within two body tion, Table S3). Ti displays were produced repeatedly lengths of the female, after which he performed the for long periods of time. At the end of a long bout of Settle (Et) display. Et displays occurred when the Ti displays, males produced a Rev (Ev) display male moved his entire body upwards, ‘standing’ at its element. Ev displays had both vibratory and visual highest point. Next, the male folded his 3rd legs components (Fig. 4). Associated Ev vibrations were towards his body until the patellas were almost longer than Ti vibrations (see Supporting informa- touching each other and, at the same time, extended tion, Table S3, Fig. 4). Coordinated with these vibra- his pedipalps upwards (Fig. 3.2a). Several species per- tions, a male flicked the tips of his forelegs formed a variation of this Et display, the ‘subtle’ Eto downwards and slightly vertically (Fig. 4). Three display. Eto display elements differed in that the body variations of Ev displays occurred (Table 2), Evlo,Evhi, of the male was not held at its highest point but, and Ev0:Evlo foreleg movements were subtle, Evhi instead, was a simple transition from Ous to IFs with foreleg movements were much stronger and in Ev0 no exaggerated movements. Et displays were always foreleg movements and vibrations were very subtle followed by Introductory Flick (IF) displays. IF and often undetectable. A single Ev display occurred display elements were made up of several foreleg after a Ti series (Fig. 4). As the Tick-Rev Motifs were flicks. The first flick of an IF display consisted of the repeated, the male’s forelegs gradually moved down entire body of the male moving down into regular during each Ev display (Fig. 4). In general, there were courtship posture when his pedipalps were moved more Ti displays in early Tick-Rev Motifs than later into forward position (the typical position during most motifs within a movement (Fig. 4). After several Tick- of the display composition), and his legs were arched Rev Motifs, there was often a Thump Burst Bridge upwards so that the tips of his forelegs were pointing (TB) which demarcated the ending of a movement towards the female (with the femurs almost com- (see below; Fig. 6). pletely vertical) (Fig. 3.3a). During this movement, males produced a high intensity broadband ‘thump’ that was coordinated with movements of the forelegs 3RD LEG MOTIFS (FIGS 5, 6) but slightly advanced relative to his foreleg move- 3rd Leg Motifs usually followed Tick-Rev Motifs. ments (Fig. 3.3a; see also Supporting information, There were several variations of 3rd Leg Motifs. Some Table S2). In subsequent flicks, the male arched his species used different 3rd Leg Motifs in different forelegs up and then down (Fig. 3.3b, c). During this movements and in these cases, 3rd Leg Motifs in period, the 3rd legs were slightly lowered so that they early movements were simpler (had less motifs) than were positioned closer to his body (Fig. 3.3c). Less in later movements. 3rd Leg Motifs were made up of intense substrate-borne thumps were also coordi- 4 different signal types: 3rd leg switches (Rd ), 3rd nated with these leg flicks. Vibrations and leg motions sw leg slides (Rd), Body pops (Bo ), and Body shakes were coordinated but substrate-borne vibrations po (Bo ) (Table 3). The order of the three 3rd Leg Motif were produced by abdominal movements, similar to sh variations were: other Habronattus species (Elias et al., 2003). Flick numbers in IF displays appeared to be species specific 3rd Leg Motif variation 1: (Rdsw Rd*)**

(Table 1). We did not record Ous or Ets for all species, 3rd Leg Motif variation 2: ((Rdsw Rd*)* (Bopo Rdsw potentially as a result of differences in the starting Rd*)*) position of male displays. When males started dis- 3rd Leg Motif variation 3: ((Rdsw Rd*)* (Bosh Rdsw playing close to females, they often proceeded directly Rd*)*) to Et or IF displays. The ﬁrst signal type was a 3rd leg switch (Rdsw). Rdsw always began a 3rd Leg Motif and consisted of motion TICK-REV MOTIF (FIG.4) and vibratory components. Rdsw occurred when a male Tick-Rev Motifs were the most common motif in in typical courtship posture, moved one of his 3rd legs H. coecatus group displays (all species examined used up in a diagonal direction so that his 3rd leg was

(1) Intro Tick-Rev 3rd-Leg TB S- Wave-Reach PM

3,1 Ou* Et In (2) 0.2

Vibration Amplitude −0.2 (3) 50

30 Right 1st leg Left 1st leg 10 Relative Pixel Relative Location −10 (4) 15

5 Right 3rd Leg Left 3rd Leg Relative Pixel Relative Location −5 0 5 10 15 Time (sec)

3,1 1. Ou 2. Et 3. If (5) (a) (a) (a) (b) (c)

0.8 3 (a)(a) (b)(c) (6) (a) 0.6 2 Substrate-borne vibrations

RMS 0.4 1 0.2 0 0 (7) 8 45 6 35 1st Leg 4 25 Vertical 15

Y Location 2 5 0 1 (8) 10 0.6 1st Leg 0.2 0 Horizontal

−0.2 X Location X −0.6 −10 −1 12 (9) 4 8 3 3rd Leg Vertical 2 4

Y Location 1 0 0 6 6 (10) 2 3rd Leg 2 Horizontal −2 −2

X Location X −6 −6 0.7 0.9 1.1 1.3 1.5 7891011 Time (sec)

Figure 3. Introductory Motif. Intro Motifs begin all displays and consist of three display elements (Ou, Et, If). 1st Row, overall timeline of display. Enlarged tab (in this case, Intro) represents the motif described in detail in the remaining panels (in this and subsequent ﬁgures). 2nd Row, oscillogram of entire Intro Motif. 3rd row, 1st leg position (red) during entire Intro Motif. Solid lines represent right 1st leg, dashed lines represent left 1st leg. 4th Row, 3rd leg position (blue) during the Intro Motif. Solid lines represent right 3rd leg, dashed lines represent left 3rd leg. 5th Row, drawings and video stills from courtship recordings. Each number represents a signal element (1–3) and each letter (a–c) represents a component of each signal element. Arrows show the direction of motion and thicknesses of arrows indicate the relative amplitude of motion. Grey bars indicate the times within the display that are represented by the drawings (5th row) and the corresponding details of substrate-borne vibrations (6th row), vertical (7th row) and horizontal (8th row) 1st leg movements, and horizontal (9th row) and vertical (10th row) 3rd leg movements. Display quantiﬁed from Habronattus coecatus. ᭣

Table 1. Introductory Motif band and had the properties of percussive signals. Males alternated the legs that they used in successive

Species Motif order displays (Fig. 5). Body shake (Bosh), was the fourth

type of signal. Bosh occurred after Rd displays Habronattus anepsius In3,1 (Fig. 6.1a) and began when the raised 3rd leg was Habronattus borealis Simple Form: Ou lowered down. During this movement, the male began 3or4 Complex Form: Ou Et In to pivot his entire body back and forth repeatedly by 4,1 Habronattus brunneus Ou Et In approximately 30° (Fig. 6.2a). After his 3rd leg was 4 Habronattus coecatus Ou Et In lowered tightly against his body, the male continued Habronattus cuspidatus Ou Et In3 to ‘shake’ his body by pivoting it back and forth. The Habronattus festus Ou Et In3,1 shakes were produced along with a low intensity Habronattus klauserii Ou Et In4,1 broadband vibration (Fig. 6; see also Supporting Habronattus mexicanus Ou Et In2 o information, Table S4). After several 3rd Leg Motifs, Habronattus pyrrithrix Ou Et In2 Habronattus schlingerii Ou Et In3,1 there was often a Thump Burst Bridge (TB), which 3 punctuated the ending of a movement (see below; Habronattus virgulatus Eto In Fig. 7). positioned higher than the tips of his forelegs THUMP BURST BRIDGE (FIG.7) (Fig. 5.1a). During these 3rd leg motions, males Thump Burst Bridges (TB) served as the bridge produced a relatively long broadband vibration between most movements. TB displays occurred after (Fig. 5.1a; see also Supporting information, Table S3). Tick-Rev, 3rd Leg displays, and Reprise Bridges (see

Rdsw vibrations were similar to Rd vibrations in spec- below). TB displays bridged these displays to new tral content (see below) but were longer in duration Tick-Rev Motifs. In our scoring of displays, TBs (Fig. 5.1a; see also Supporting information, Table S4). usually marked the end of a movement. TBs were

3rd Leg sweeps (Rd) followed Rdsw and consisted of made up of ﬂicks (Fl), which were produced in rapid horizontal movements of the raised 3rd leg (Fig. 5.2a) succession. In most species (9/11 species), the number and coordinated broadband vibrations (Fig. 5.2a; see of Fl displays was stereotyped, whereas, in other also Supporting information, Table S4). The raised species, (3/11 species), the number of Fl displays

3rd leg alternated between successive Rdsw displays. varied within a small range (Table 4). Alternating presentation of 3rd legs was a property of TB Bridge:Flx where x is an integer in the range 2–5 all 3rd Leg Motifs. In the second and subsequent Rdsw displays, as the male’s 3rd leg was raised (Fig. 5.1a), Fl displays were associated with motions and sub- the previously raised leg was lowered, once again strate borne vibrations (Fig. 7). These displays typi- tightly near the body. The third type of display Bopo cally began after an Rd display when one of the 3rd consisted of stereotyped motions and associated vibra- legs was raised and the other was held tight against tions. Bopo began with the male crossing his raised the body (Fig. 7.1a). First, the male arched both his 3rd leg with his lowered 3rd leg. The male then forelegs rapidly upwards so that his legs were almost rapidly shifted his raised 3rd leg down (Fig. 5.3a), completely vertical with the tips pointing upwards which caused his entire body to shake back and forth (Fig. 7.1a). This was followed by the male arching (Fig. 5.3b). During this rapid motion, he produced a both his forelegs rapidly downwards until the foreleg loud ‘pop’ which may be have been caused by the tarsi and tips were pointing downwards (Fig. 7.1b). release of 3rd leg tension, although this mechanism This pattern was repeated for every Fl display. In the has not been determined (Fig. 5.3b). Pops were broad- ﬁnal Fl display of the TB, the raised 3rd leg was

(1) Into Tick-Rev 3rd- TB S- Wave-Reach PM

** ** (Ti Rv) (2) 0.15

0 Vibration Vibration Amplitude −0.15 (3) 0

−40 Left 1st leg Right 1st leg

Relative Pixel Relative Location −80

(4) 1 0.6 0.2 Left 3rd Leg −0.2 Right 3rd Leg Relative Pixel Relative Location −0.6 −1 0 5 10 15 20 25 30 35 40 Time (sec)

1. Ti** Rv (5) (a)

(6) 1.2 (a)

0.8 Substrate-borne vibrations RMS 0.4 0 (7) −20

−30 1st leg Vertical

Y Location −40 −50 30 (8) 1st leg 10 Horizontal

−10 X Location X −30 (9) 0.3 0.1 3rd Leg Vertical −0.1 Y Location −0.3 0.3 (10) 3rd Leg 0.1 Horizontal −0.1

X Location X −0.3 19.5 20.5 21.5 22.5 23.5 Time (sec)

Figure 4. Tick-Rev Motif. Tick-Rev Motifs consist of two display elements (Ti, Ev). For an explanation of ﬁgure organization, see Fig. 3. Display quantiﬁed from Habronattus coecatus.

Table 2. Tick-Rev Motif Table 3. 3rd Leg Motif

Species Motif order Species Motif order

Habronattus anepsius (Ti** Evlo)** Habronattus anepsius (Rdsw Rd*)* Habronattus borealis Simple Form: none Habronattus borealis Simple Form: Rd*

Complex Form: Ev** Complex Form: (Rdsw Rd*)*

Habronattus brunneus (Ti** Evlo)** (Bopo Rdsw Rd*)*

Habronattus coecatus (Ti** Evlo)** Habronattus brunneus Early movements: (Rdsw Rd*

Habronattus cuspidatus (Ti** Evlo)** Rdsw)*

Habronattus festus (Ti** Evlo)** Late movements: (Rdsw Rd* 1 Habronattus klauserii (Ti** Evlo)** Rdsw) (Rd* Bosh Rdsw)*

Habronattus mexicanus (Ti** Evhi)** Habronattus coecatus Early movements: (Rdsw Rd*)**

Habronattus pyrrithrix (Ti** Evhi)** Late movements: Rdsw Rd* 3 Habronattus schlingerii (Ti** Evhi)** (Bopo Rd )*

Habronattus virgulatus (Ti** Evhi)** Habronattus cuspidatus Early movements: (RdswRd*)*

Late movements: Rdsw Rd*

(Bopo Rdsw Rd*)* Habronattus festus Early movements: (Rd Rd*)* brought down so that it was close to the body, reset- sw Late movements: (Rdsw ting the male to the typical courtship posture Rd*)*Bopo (Fig. 7.1c, d, e). Coordinated with each foreleg motion Habronattus klauserii (RdswRd*)* was a vibratory signal. Vibratory components of Fl Habronattus mexicanus Early movements: (RdswRd*)* displays were short, intense, broadband ‘thumps’ that Late movements: Rdsw Rd*(Bosh occurred in two parts (Fig. 7; see also Supporting Rdsw Rd*)* information, Table S5). Each part was associated with Habronattus pyrrithrix Early movements: (Rdsw Rd*)* abdominal movements: one occurring on the down- Late movements: Rdsw Rd* ward deﬂection and the other on the upward deﬂec- (Bopo Rdsw Rd*)* tion. Substrate borne vibrations preceded foreleg Habronattus schlingerii Early movements: (RdswRd*)* motions in all species. Late movements: Rdsw Rd*

(Bosh Rdsw Rd*)*

Habronattus virgulatus Early movements: Rdsw Rd* FORELEG WAVE MOTIFS (FIGS 8, 9, 10, 11) (Bopo Rdsw Rd*)* Late movements: Rd Rd*(Bo Foreleg Wave Motifs (S-Wave-Reach) were made up of sw po Rd*)*(Bo Rd Rd4or5)** two distinct parts and occurred in several variations. po sw Foreleg Wave Motifs were made up of eight distinct signal elements: 3rd Leg Raises (Ra), Waving displays with low vibratory rumbles (Walo), Waving displays plane as the raised leg. Both 3rd legs were positioned with high intensity vibratory buzzes (Wahi), Waving at their highest possible point with their patellas displays with no vibrations (Wa0), Short Side Flicks touching. Vibrations produced during this behaviour (Sflo), Large Side Flicks (Sfhi), Single Contact Lunges were virtually indistinguishable from vibrations

(Cosi), and Multiple Contact Lunges (Comu) (Table 5). produced during Rdsw displays and were variable The orders of the four Foreleg Wave Motif variations (Fig. 8.1a). This posture was typical for all Foreleg were: Wave Motifs. After Ra displays, males produced a Waving display. Waving displays had three variations Foreleg Wave Motif variation 1: Ra ((Wa Sf )* lo lo or hi depending on the vibratory signals that co-occurred Wa Sf Co (Wa Sf )*)* lo hi s lo lo or hi (or did not in one instance). The motion component of Foreleg Wave Motif variation 2: Ra((Wa lo waving displays consisted of the male’s extended fore- Sf )**Wa Sf Co Co *)* hi lo hi si mu legs waved extremely fast, alternating the foreleg Foreleg Wave Motif variation 3: Ra(Wa hi waved, typically in the range of 10–35 waves/s Sf )**((Wa Sf )**(Wa Sf Co )**)** lo hi lo hi hi si (Fig. 8.2a). Coupled with this motion was either (1) a Foreleg Wave Motif variation 4: Ra((Wa 0 low frequency, narrow band ‘hum’ (Wa ; Fig. 8.2a; see Sf )**(Wa Sf Co )**) lo hi 0 hi si also Supporting information, Table S6); (2) a higher

Foreleg waves always began with a 3rd Leg Raise frequency, broad band ‘buzz’ (Wahi; Fig. 9.2a; see also (Ra). 3rd Leg Raises began after an Rd display and Supporting information, Table S6), or (3) no vibra- consisted of the male’s 3rd leg that was close to the tions (Wa0). In three species, Habronattus festus, body being raised until it was on the same horizontal Habronattus klauserii, and H. schlingerii, the

3rd-Pop (1) Intro Tick-Rev TB S-Wave-Reach PM Rd Rd Rd Rd Rd Rd Rd Rd Rd Rd Rd Rd RdRd Rd Rd Rd Rd Rd Rd sw pop sw (2) 0.2 0.1 0 −0.1 Vibration Amplitude −0.2 (3) 0

−10 Right 1st leg Left 1st leg −20 −30

Relative Pixel Relative Location −40 (4) 80 60

40 Right 3rd Leg Left 3rd Leg 20

Relative Pixel Relative Location 0 0 1 2 3 4 5 6 7 Time (sec)

1. Rdsw 2. Rd 3. Bo (5) po (a) (a) (a) (b)

1.6 2 (6) 1.6 (a) (a) (a) (b) 1.6 1.2 1.2 1.2 Substrate-borne 0.8 vibrations 0.8 0.8 RMS 0.4 0.4 0.4 0 0 0 (7) −10 −10 −10 −20 −20 −20 1st leg Vertical −30 −30 −30 Y Location −40 −40 −40 40 40 (8) 30 20 20 20 1st leg 0 0 10 Horizontal 0

−20 −20 −20 X Location X (9) −40 −40 60 60 60 3rd Leg 40 40 40 Vertical 20 20 Y Location 20 0 0 0 0 40 60 (10) 3rd Leg 20 −20 40 Horizontal 0 −40 20 −20

X Location X 0 −60 −40 0.25 0.75 1 1.25 1.5 2.2 2.4 2.6 2.8 3 3.2 3.4 4.8 4.9 5 5.1 5.2 5.3 5.4 5.5 Time (sec)

Figure 5. 3rd Leg Motif: 3rd – Pop variation. 3rd Leg Motifs consist of three of four possible display elements (Rdsw, Rd,

Bopo,Bosh). For an explanation of ﬁgure organization, see Fig. 3. Display quantiﬁed from Habronattus coecatus.

(1) Intro Tick-Rev 3rd-Shake TB S-WaveBuzz-Reach PM Rd Rd Rd Rd Rd Rd Rd Rd RdRd Rd Rd RdRd Rd RdRd Rd Rd Rd RdRd Rd Rd Rd RdRd Rd Rd sh sw sh sw sh (2) 0.8 0.4 0

Vibration Amplitude −0.4 −0.8 (3) 20 Left 1st leg 10 Right 1st leg Relative Pixel Relative Location (4) 0 40 30 Left 3rd Leg 20 Right 3rd Leg 10

Relative Pixel Relative Location 0 0123456 Time (sec)

1. Rd 2. Bosh (5)

(6) 8 Substrate-borne 6 vibrations 4

RMS 2 0 (7) 20 1st leg Vertical 10

Y Location 0 (8) 8 4 1st leg 0 Horizontal

−4 X Location X −8 −12 (9) 40

30 3rd Leg 20 Vertical 10 Y Location 0 (10) 20 10 0 3rd Leg −10 Horizontal

−20 X Location X −30 0 0.5 1 1.5 2 2.5 3 Time (sec)

Figure 6. 3rd Leg Motif: 3rd – shake variation. 3rd Leg Motifs consist of three of four possible display elements (Rdsw,

Rd, Bopo,Bosh). For an explanation of ﬁgure organization, see Fig. 3. Display quantiﬁed from Habronattus brunneus.

Table 4. Thump Burst Bridge occurred when the same foreleg that was used in Cosi display was waved in front of the female’s face, often Species Bridge touching the ground directly in front of her. Concur-

rently with this Comu motion component, males Habronattus anepsius Fl2or3 produced a series of narrow band ‘revs’ (Fig. 10.3) Habronattus borealis Simple Form: none that were lower in frequency than Cosi displays (see 2 Complex Form: Fl Supporting information, Table S6). Habronattus brunneus Fl3or4 Habronattus coecatus Fl3 3 Habronattus cuspidatus Fl REPRISE BRIDGE Habronattus festus Fl3 Reprise Bridges (RB) only occurred after Foreleg Habronattus klauserii Fl4 Wave Motifs and served to bridge these displays to Habronattus mexicanus Fl3 Tick-Rev Motifs. In our scoring of displays, RBs Habronattus pyrrithrix Fl2 served to end later display movements. RBs appeared Habronattus schlingerii Fl3 Habronattus virgulatus Fl4 to use a hodgepodge of elements from previous motifs with the addition of a Back Reset (Ba) display (Table 6). The typical order of a RB was: Reprise Bridge:Ban (Rd or Rd or Bo or Ti* frequency of Wa changed in the display (Wa and sw sh or po h hi1 Ev) Flx where x is an integer number Wahi2). In the early portion of Foreleg Wave Motifs,

Wa displays were followed by Short Side Flicks (Sflo). Reprise Bridges appeared to facilitate the switch from

Sflo were displays where the male’s forelegs were Foreleg Wave postures to ‘typical’ postures. From the moved horizontally away from his body (Fig. 8.3a) Foreleg Wave posture (forelegs horizontally orien- and then rapidly returned (Fig. 8.3b). In some species, tated just above the female), males produced a Back the patellas of the 3rd legs were brought towards the Reset (Ba) display. In Ba displays, the male’s forelegs body as the forelegs were moved away from the body were raised upwards until his forelegs were once (Fig. 9.3a). As the male’s legs were returned to their again positioned in an almost vertical position. initial position, males produced a high intensity, During each backwards movement, a coordinated broadband ‘thump’ using their abdomen (Fig. 8.3a, b). broad-band ‘rev’ was produced. After the forelegs were As this early stage progressed, the separation positioned, males produced a display that was previ- between adjacent Sf pairs became increasingly longer ously produced in other motifs [either a 3rd leg switch as the tempo of the display slowed down (Figs 8, 9). (Rdsw), a Body Shake (Bosh), a Body Pop (Bopo), or a At later stages of Wa displays (Figs 10, 11), they Tick-Rev (Ti*Ev)]. At the end of these displays, males were sometimes followed by Large Side Flicks (Sfhi). produced a Thump Burst Bridge (TB), except in H. bo-

Sfhi were displays where the male’s forelegs were realis. For some species, we did not record any RB moved horizontally away from his body until the displays. It was unclear whether these species did not femur of his forelegs were almost parallel to the ﬂoor produce this display or whether this was result of the

(Fig. 10.1a). Sfhi motion components were produced absence of multiple Foreleg Wave Motifs. concurrently with high intensity, broadband ‘thumps’ similar to Sflo displays, although they tended to be shorter in duration (Figs 10.1b, 11.2b; see also Sup- PRE-MOUNT MOTIF (FIG. 12) porting information, Table S6). Sfhi were often fol- Pre-Mount Motifs were the finale of a display compo- lowed by Contact (Co) displays. Co displays came in sition and occurred just before an attempted copula- two varieties: Single Contact Lunges (Cosi) and Mul- tion (Table 7). Because we did not use live females, tiple Contact Lunges (Comu). Cosi displays consisted of courtship recordings were terminated as soon as one or two extremely rapid foreleg flicks, where the males attempted to copulate with females. In prelimi- male arched one of his forelegs downwards towards nary observations with live females, all H. coecatus the female, making contact with the female’s legs, group males produced a different set of vibrations palps, or face. Concurrently with this flick, males during copulation (copulatory courtship). Pre-Mount produced a narrow band ‘rev’ (Figs 10.2a, 11.3a; see Motifs included a single display element Pr with the also Supporting information, Table S6). In one species general pattern: (H. schlingerii), Co motions occurred at the beginning s Pre-Mount Motif: Pr* of Wahi vibrations and were virtually indistinguishable from Wahi vibrations. In some species, this rapid Pr displays followed Foreleg Wave Motifs and

Cosi display was followed by a Comu display. Comu consisted of both motion and vibratory components. displays were much slower than Cosi displays and During Pr displays, a male arched his forelegs toward

(1) Intro Tick-Rev 3rd-Leg TB S- Wave-Reach PM

3 Rd Rd Fl (2) 0.2 0.1 0

Vibration Vibration Amplitude −0.1 −0.2 (3 40 Left 1st leg 0 Right 1st leg

Relative Pixel Relative Location −40 (4) 60

40 Right 3rd Leg Left 3rd Leg 20

Relative Pixel Relative Location 0 7 7.4 7.8 8.2 8.6 Time (sec) 1. Fl 3 (5) (a) (b) (c) (d) (e)

(6) (a) (b) (c) (d) (e) 2 Substrate-borne vibrations 1 RMS

0 (7) 40 1st leg 0 Vertical

Y Location −40 (8) 100

50 1st leg Horizontal

0 X Location X −50 (9) 60

40 3rd Leg Vertical 20 Y Location 0 (10) 0 −20 3rd Leg Horizontal −40 −60

X Location X −80 7.7 7.9 8.1 8.3 8.5 Time (sec)

Figure 7. Thump-Burst (TB) Bridge. TB displays bridge Tick-Rev Motifs with other Tick-Rev Motifs or 3rd Leg Motifs with Tick-Rev Motifs and consists of one repeated display element (Fl). For an explanation of ﬁgure organization, see Fig. 3. Display quantiﬁed from Habronattus coecatus.

Early

(1) INTRO Tick-Rev 3rd-Leg TB S-Wave-Reach PM

18 1 * 11 Rd Wa Sf ()Wa Sf Co Co ra ()lo lo lo hi si mu (2) 0.8 0.4 0 −0.4 Vibration Amplitude −0.8 (3) 20 0 Right 1st leg −20 Left 1st leg

Relative Pixel Relative Location −40 (4) 60 Right 3rd Leg 40 Left 3rd Leg 20 0

Relative Pixel Relative Location 0 5 10 15 20 25 30 35 40 45 Time (sec)

1. Rdra 2. Walo 3. Sflo (5) (a)(a) (a) (b)

Wa Sf 5 6 lo lo (6) (a) (a) (a) (b) 4 4 Substrate-borne RMS 3 vibrations 2 2 1 (7) 0 0 10 10 1st leg 0 0 Vertical Y Location −10 −10 (8) 8 10 4 1st leg 0 0 Horizontal −4

X Location X −10 −8 62 (9) 60 40 3rd Leg 61 Vertical 20 Y Location 0 60 8 (10) 8 4 4 3rd Leg 0 0 Horizontal −4 −4

X Location X −8 −8 0 0.5 1 1.5 7 7.5 8 8.5 9 Time (sec)

Figure 8. Early portion of Foreleg Wave Motif: Walo variation. Early Foreleg Wave motifs consist of three of six possible display elements (Ra, Sflo,Sfhi,Walo,Wahi,Wa0). For an explanation of ﬁgure organization, see Fig. 3. Display quantiﬁed from Habronattus coecatus.

(1) INTRO Tick-Rev 3rd-Leg TB S-Wave-Reach PM 25 * 1 24 Rd Wa Sf ((Wa Sf ) Co ) ra ()hi lo hi hi si (2) 1

Vibration Amplitude 0 −1 (3) 0 −10 Right 1st leg −20 Left 1st leg −30 Relative Pixel Relative Location −40 (4) 30 20 Right 3rd Leg 10 Left 3rd Leg 0

Relative Pixel Relative Location 01020304050 Time (sec)

1. Rdra 2. Wahi 3. Sflo

(5)

Rd Wa Sf ra hi lo (6) 10 10 8 8 6 6 RMS 4 4 Substrate-borne vibrations 2 2 (7) 0 0 4 4

0 0 1st leg Vertical −4 −4 Y Location

−8 −8 0.8 (8) 2 0.4 1st leg

0 0 Horizontal X Location −0.4X −2 −0.8 (9) 20 20 3rd Leg Vertical

Y Location 10 10

(10) 0 0 0 2 3rd Leg Horizontal −10 0 −20

X Location X −2 −30 0 123456 12 13 14 15 16 17 Time (sec)

Figure 9. Early portion of Foreleg Wave Motif: Wahi variation. Early Foreleg Wave motifs consist of three of six possible display elements (Ra, Sflo,Sfhi,Walo,Wahi,Wa0). For an explanation of ﬁgure organization, see Fig. 3. Display quantiﬁed from Habronattus schlingerii. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 522–547 538 D. O. ELIAS ET AL.

Late

(1) INTRO Tick-Rev 3rd-Leg TB S-Wave-Reach PM

18 1 * 11 Rd Wa Sf ()Wa Sf Co Co ra ()lo lo lo hi si mu (2) 0.8 0.4 0

Vibration Amplitude −0.4 −0.8 (3) 20 0 Right 1st leg −20 Left 1st leg

Relative Pixel Relative Location −40 (4) 60 Right 3rd Leg 40 Left 3rd Leg 20 0

Relative Pixel Relative Location 0 5 10 15 20 25 30 35 40 45 Time (sec) 1. Sf 2. Co * 4. Wa (5) hi si 3. Comu lo (a) (b) (a) (a) (b) (a)

(6) 6 (a) (b)(a) (a) (b) (a) Substrate-borne 4 vibrations RMS 2 0 (7) 10 0 1st leg −10 Vertical −20

Y Location −30 −40 (8) 40 20 1st leg Horizontal 0 −20

X Location X −40 (9) 68 64 3rd Leg 60 Vertical 56 Y Location 52 (10) 8 4 3rd Leg 0 Horizontal

−4 X Location X −8 28 29 30 31 32 33 Time (sec)

Figure 10. Late portion of Foreleg Wave Motif: Cosi –Comu variation. Late Foreleg Wave motifs consist of three to four of nine possible display elements (Sflo1,Sflo2 Sfhi,Walo,Wahi1,Wahi2,Wa0,Cosi,Comu). For an explanation of ﬁgure organization, see Fig. 3. Display quantiﬁed from Habronattus coecatus.

(1) INTRO Tick-Rev 3rd-Leg TB S-Wave-Reach PM 25 * 1 24 Rd Wa Sf (()Wa Sf ) Co ra ()hi lo hi hi si (2) 1

Vibration Amplitude 0 −1 (3) 0 −10 Right 1st leg −20 Left 1st leg −30 Relative Pixel Relative Location −40 (4) 30 20 Right 3rd Leg 10 Left 3rd Leg 0

Relative Pixel Relative Location 01020304050 Time (sec) 1

2. Wahi 4. Sfhi 5. Co si (5)

(6) 15

RMS Substrate-borne vibrations 5

0 (7) 0

−10 1st leg −20 Vertical

Y Location −30 −40 (8) 4 1st leg Horizontal

0 X Location X −4

(9) 3rd Leg 20 Vertical

Y Location 10

0 8 3rd Leg Horizontal 4 (10)

0 X Location X −4 −8 44 45 46 47 48 49 Time (sec)

Figure 11. Late portion of Foreleg Wave Motif: Cosi alone variation. Late Foreleg Wave Motifs consist of three to four of nine possible display elements (Sflo1,Sflo2 Sfhi,Walo,Wahi1,Wahi2,Wa0,Cosi,Comu). For an explanation of ﬁgure organization, see Fig. 3. Display quantiﬁed from Habronattus schlingerii. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 522–547 540 D. O. ELIAS ET AL.

Table 5. Foreleg Wave Motif Table 7. Pre-Mount Motif

Species Motif order Species Bridge

Habronattus anepsius Ra (Wal Sfl)*((Wal Sfh Wal Sfh Habronattus anepsius Pr* 1 CosCom (Wal Sfh)*) Habronattus borealis Simple Form: Pr* Habronattus borealis Simple Form: none Complex Form: Pr*

*Complex Form: (Wa0 Sfh** Habronattus brunneus Pr*

CosCom*)* Habronattus coecatus Pr* 1 1 Habronattus brunneus Ra (Wal Sfl) (Wal Sfh Com) Habronattus cuspidatus Pr* 1 (Wal Sfl) Habronattus festus Pr*

Habronattus coecatus Ra (Wa0 Sfh)**(Wa0 Sfh Cos Habronattus klauserii Pr*

Com*)** Habronattus mexicanus Pr*

Habronattus cuspidatus Ra(Wah Sfl)** ((Sfh Wal)* Habronattus pyrrithrix Pr* 2 (Sfh Cos Wal)**)* Habronattus schlingerii Pr*

Habronattus festus Ra (Wah1 Sfl)**(Wah2 Sfl)* Habronattus virgulatus Pr*

(Wah2 Sfh Cos)**

Habronattus klauserii †(Wah Sfl1)**((Wah Sfl2)* 2 (WalSfl2 Cos )*)** the female, twisting his foreleg tips towards and then Habronattus mexicanus Ra ((Wah Sfh)** (Wah Sfh Cos away from the female. The forelegs alternated so that Com*Wal)*)* one foreleg was twisting towards the female, whereas Habronattus pyrrithrix Ra (Wal Sfh)* (Wal Sfh Cos the other was twisting away (Fig. 12). During these Com*)* movements, males also moved their 3rd legs horizon- Habronattus schlingerii Ra ((Wah Sfl)** ((Wal Sfh)** tally away from their body. Vibratory components (Wal Sfh Cos)**)** were produced continuously in a Pre-Mount Motif, Habronattus virgulatus Ra (Wa Sf )**(Wa Sf Wa 0 h 0 h 0 and consisted of high frequency ‘buzzing’ (see Sup- Co )** s porting information, Table S8). In our scoring of components, a Pre-Mount Motif was the concluding *Co for H. borealis has no vibratory component. †H. klau- m movement (Fig. 12). serii has no Ra display; instead 3rd legs get raised gradually during the Wah display. First of Cos pair contains percussive component and tends to be lower in peak DISPLAY OF H. BOREALIS frequency. Ten of the species observed shared the same progression of movements (some species did not include RBs; see above), although details such as the numbers of Table 6. Reprise Bridge repetitions of elements and motifs, the exact paths of motions, the fine structure of vibratory signals, and Species Bridge order the elements used in each motif differed (Table 8; see also Supporting information, Tables S2–S8). Three 1or2 2 Habronattus anepsius Ba Bosh Rd* Fl additional species for which we have partial data, Habronattus borealis Simple Form: none likewise show the same overall sequence of visual Complex Form: Ba Bopo elements (Table S1). H. borealis, however, stood out Rv* for several reasons. First, H. borealis, unlike other Habronattus brunneus Ba Rd Fl3 sw members of the species group, is drab and lacks the *Habronattus coecatus n/a extensive ornamentation on the first and third legs Habronattus cuspidatus Ba2 Ev * Rd* Fl3or4 Wah that characterizes the group (Fig. 13). Because the Habronattus festus Ba2 Ev* Fl3 Habronattus klauserii BaFl2or3 complex ornaments of the group were lacking, and Habronattus mexicanus BaTi*EvFl2or3 H. borealis falls phylogenetically within the larger Habronattus pyrrithrix BaTi*EvFl2 clade with modified first and third legs (Maddison & Hedin, 2003), H. borealis displays are likely an Ba Ti* Ev Rd* Bopo Habronattus schlingerii Ba Ev Rd Fl2or3 example of evolutionary loss of display complexity. Habronattus virgulatus Ba4 Fl5 Second, unlike other H. coecatus group members where motifs are generally stereotyped, for H. borea-

*EvWah = Ev followed by vibratory component alone of Wah. lis, it is variable. Maddison & Stratton (1988a) described brieﬂy a complex display in specimens from Ontario; Richman & Cutler (1998) described a simple display in specimens from Kansas. In order to under-

(1) Intro Tick-Rev 3rd-Leg TB S- Wave-Reach PM * Wa Sf Co Co Pr lo hi si mu (2) 0.4 0.2 0

Vibration Amplitude −0.2 −0.4 (3)

0 Right 1st leg Left 1st leg −20 Relative Pixel Relative Location (4) −40 70 Right 3rd Leg 60 Left 3rd Leg

50 Relative Pixel Relative Location 01234 5 Time (sec) 1. Pr* (5) (a) (b)

(6) 8 (a) (b) 6 Substrate-borne

RMS 4 vibrations 2 0 (7) 0 1st leg Vertical Y Location −20

−40 (8) 40 20 1st leg Horizon- 0 tal

X Location X −20 (9) 70

60 3rd Leg Vertical

Y Location 50 (10) 20 3rd Leg 0 Horizontal

X Location X −20 1234 5 Time (sec)

Figure 12. Pre-Mount (Pr) Motif. Pr Motifs consist of one display element (Pr). For an explanation of ﬁgure organization, see Fig. 3. Display quantiﬁed from Habronattus coecatus.

Table 8. Element summary

Motif Elements

Tick-Rev Motif Ti (10/11 species): anepsius, brunneus, coecatus, cuspidatus, festus, klauserii, mexicanus, pyrrithrix, shlingerii, virgulatus Ev (11/11 species): anepsius, borealis, brunneus, coecatus, cuspidatus, festus, klauserii, mexicanus, pyrrithrix, schlingerii, virgulatus

3rd Leg Motif Rdsw (11/11 species): anepsius, borealis, brunneus, coecatus, cuspidatus, festus, klauserii, mexicanus, pyrrithrix, schlingerii, virgulatus Rd (11/11 species): anepsius, borealis, brunneus, coecatus, cuspidatus, festus, klauserii, mexicanus, pyrrithrix, schlingerii, virgulatus

Bopo (4/11 species): borealis, coecatus, cuspidatus, virgulatus

Bosh (5/11 species): anepsius, brunneus, festus, mexicanus, schlingerii TB Bridge Fl (11/11 species): anepsius, borealis, brunneus, coecatus, cuspidatus, festus, klauserii, mexicanus, pyrrithrix, schlingerii, virgulatus Foreleg Wave Ra (9/11 species): anepsius, brunneus, coecatus, cuspidatus, festus, mexicanus, pyrrithrix, Motif schlingerii, virgulatus

Walo (8/11 species): anepsius, brunneus, cuspidatus, festus, klauserii, mexicanus, pyrrithrix, schlingerii

Wahi(5/11 species): cuspidatus, festus, klauserii, mexicanus, schlingerii, Wa0 (2/11 species): coecatus, virgulatus

Sflo (6/11 species): anepsius, brunneus, cuspidatus, festus, klauserii, schlingerii

Sfhi (11/11 species): anepsius, borealis, brunneus, coecatus, cuspidatus, festus, klauserii, mexicanus, pyrrithrix, schlingerii, virgulatus

Cosi (10/11 species): anepsius, borealis, coecatus, cuspidatus, festus, klauserii, mexicanus, pyrrithrix, schlingerii, virgulatus

Comu (6/11 species): anepsius, borealis, brunneus, coecatus, mexicanus, pyrrithrix

stand this variation, we extensively recorded displays element (3/30 included Sflo; 2/30 included Rd; 1/30 from individuals in one population in Ontario (N = 46) included Wa0 wave). Only 29% of individuals used and on a subset of these individuals (N = 25) we complex compositions in their first display. Of the 16 recorded two courtship displays from the same indi- individuals that produced complex display composi- vidual separated by 2 weeks. No morphological dif- tions, 51% used Ou, Ev, Rd, and Pr display elements; ferences are evident between Ontario and Kansas 39% used Ou, Ev, Rd, Sfl,Com, and Pr displays; and populations. Errors in the recording procedure pre- 3% used all possible H. borealis display elements (Ou, vented us from quantifying courtship length in 3 Ev, Rd, Wa0,Sfl,Com, Pr). recordings, although data on display behaviour was To determine whether males maintain the same noted. courtship elements in Ontario populations, we Habronattus borealis displays fell into two catego- recorded the same individuals after a 2-week period ries: (1) simple display compositions which were short (N = 24). Of the males who had a complex courtship (34.6 ± 22.2 s, range 14–80, N = 30) and consisted of during the first trial, five remained complex and only very few signal elements (3.07 ± 0.27 display ele- one transitioned to a simple display composition. Of ments; range 3–4, N = 30) and (2) complex display the males who had simple courtship during the first compositions which were longer (296.8 ± 311 s, range trial, 11 remained simple and seven transitioned to 90–370 s, N = 13) and consisted of more signal ele- a complex display composition. Statistical analysis ments (5.4 ± 0.8 display elements; range 5–7 ele- using McNemar’s test for frequency of changes indi- ments, N = 16). Of the 46 individuals observed, most cates no differences between switching and nonswitch- used simple display compositions in their first courting rates (P = 0.221), suggesting that males switch ship recordings (30/46). For the majority of simple randomly between courtship types. display compositions (77%; 23/30), males performed Ou displays (Introductory Motif) and then proceeded directly to Pr displays (Pre-Mount Motif). In the MORPHOLOGICAL ORNAMENTATION (FIG. 13) remaining seven displays, males included a second We did not attempt to characterize fully the com- motif that consisted of a single courtship display plexity of morphological structures involved with

2 (B) (A) 7 1 4

6 3 5

13 14 12 (C) 15 16 17 10 18 11

9 8

Figure 13. Habronattus coecatus ornament diversity. Numbers represent distinct ornaments that are restricted to males and on body parts that are moved and visible to females during courtship. (A) H. coecatus face (B) H. coecatus 1st pair of legs. (C) H. coecatus 3rd pair of legs. The vast majority of H. coecatus group members are elaborately ornamented. Drawings by Wayne P. Maddison. courtship, although a brief description of those tally; third tibia (16) green, with (17) ridge of white found in H. coecatus (Fig. 13) shows how multifari- setae and (18) white macrosetae (Fig. 13C). ous male ornamentation is in this species group. If Although the developmental biology of spiders is not we define an ornament as a morphological structure well understood, it is likely that many independent or colour pattern that is restricted to males and on genes are involved in these traits. Except in H. bo- body parts that are moved or visible to the female realis, this type of ornamental complexity (orna- during courtship, then a male H. coecatus has 18 mented face, fringed first leg, modified third leg) is ornaments: (1) clypeus covered with bright red generally consistent across the species group, with setae; (2) lateral stripes on carapace above the eyes; the species differing in colours and detailed shapes (3) chelicerae with a large distinct white spot of the particular ornaments. (Fig. 13A); first leg (4) black beneath, with (5) lateral fringe of long setae, many with expanded DISCUSSION white tips; (6) first tibia with spatulate macrosetae; (7) first tarsus with white spot below (Fig. 13B); (8) In the present study, we show that H. coecatus group third femur with black bar centrally, (9) pale area sexual displays are some of the most elaborate in the distally, (10) prolonged into corner distally, and (11) animal kingdom. Their displays combine intricate with patch of orange setae distally; third patella ornamentation with multicomponent substrate-borne (12) pale grey, with (13) black dorsal ridge, (14) vibrations and coordinated dances. Even in the most white patch dorsobasally, and (15) two spurs dis- austere terms, one can say that their multimodal

© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 522–547 544 D. O. ELIAS ET AL. displays are complex because some species have up to Maddison & Hedin (2003) suggested that this puzzle 18 ornaments (body segments with distinct coloured, (i.e. distant hybridization concentrated in a group patterned or formed structures; Fig. 13), a plethora of with complex courtship) might be explained by a motions of various appendages (Figs 3, 4, 5, 6, 7, 8, 9, process of antagonistic coevolution driving the evolu- 10, 11, 12), and up to 20 distinct vibratory signals tion of novel exploitative male traits (and subsequent (Table 8). Displays in the H. coecatus group, however, female resistance; Holland & Rice, 1998). Complexity cannot be described in simple terms because the of H. coecatus group displays may be indicative of an entire display changes through time as males add active arms race, with females susceptible to intense new signal types and new signal combinations. In novel signals, and therefore also to displays of other addition, the overall structure and tempo of the dis- distantly related species. In one Habronattus species plays changes through time in an organized progres- group (the Habronattus pugillis group), it has been sion of element combinations (motifs), within which suggested that sexual selection is driving diversifica- individual males may vary the duration and number tion (Maddison & McMahon, 2000; Masta, 2000; of element repetitions. This temporal structuring of Masta & Maddison, 2002; Hebets & Maddison, 2005). displays is more analogous to a musical composition Interestingly, however, females of one population than to language syntax; hence, our choice of nomen- prefer males from foreign populations (Hebets & clature for display descriptions. Complex displays are Maddison, 2005) whose displays have additional a characteristic of the genus Habronattus (Griswold, vibratory elements (Elias et al., 2006a). Such xeno- 1987; Cutler, 1988; Maddison & Stratton, 1988b; philia may have, during times of population contact, Maddison & McMahon, 2000; Masta, 2000; Elias promoted hybridization. In a study on the amicus- et al., 2003, 2005, 2006c, d) and members of the species group, multiple lines of evidence demon- H. coecatus group are the maestros of the genus. strated genetic introgression between two of the Understanding the patterns that led to evolution of species: Habronattus amicus and Habronattus ustu- such highly complex displays is a challenge. latus (Hedin & Lowder, 2009). It was suggested that In the H. coecatus group, one of the most unex- introgression occurred in only one direction, with pected observations is that the complex ornamenta- H. amicus females mating with H. ustulatus males tion of the group finds an equal counterpart in (Hedin & Lowder, 2009). Habronattus ustulatus male vibratory and motion displays. This appears to be at courtship includes elements lacking in H. amicus (D. odds with prevailing ideas on multiple signal evolu- O. Elias, unpubl. observ.). In both the pugillis and tion (Moller & Pomiankowski, 1993; Pomiankowski & amicus groups, novel elements in male displays may, Iwasa, 1993, 1998; Iwasa & Pomiankowski, 1994; by exploiting naive female susceptibilities, promote Johnstone, 1996). Theoretical work on signal evolu- hybridization in a particular direction. Alternatively, tion has suggested that, if signals are costly, multiple this pattern of hybridization may be promoted by a signals are unlikely to evolve and that females should direct female preference for complex and/or novel prefer single indicators of quality (Moller & Pomi- display elements. In this scenario, females prefer ankowski, 1993; Pomiankowski & Iwasa, 1993, 1998; males with more complex signalling repertoires, Iwasa & Pomiankowski, 1994; Johnstone, 1996). potentially as a signal of overall rigour (Byers, Hebets Simple signals are predicted to be more reliable indi- & Podos, 2010). New signalling elements gained cators of mate quality and more likely targets of through introgression could then be incorporated into female choice (Schluter & Price, 1993; Iwasa & Pomi- the existing signalling repertoire over evolutionary ankowski, 1994), although this is not always the case time. Preferences for repertoire size have been in non-equilibrium conditions (van Doorn & Weissing, studied extensively in bird song and are considered to 2004). Furthermore, theoretical work on processing be a major factor driving signal evolution (Searcy, mechanisms in animals has suggested that informa- 1992; Catchpole & Slater, 1995). The likelihood of tion in signals only increases up to a point after which making mating mistakes as a result of preferences for the value of any new information precipitously drops new display traits may also lead to the rapid off (Ay, Flack & Krakauer, 2007). Under these condi- de-evolution of complex displays, as is seen in H.- tions, an upper limit on the complexity of sexual borealis and in other species groups (D. O. Elias and displays is predicted (Krakauer & Nowak, 1999; Ay W. P. Maddison, unpubl. observ.). Although we cannot et al., 2007). currently test these two hypotheses, future work will Another unexpected observation is that there is explore these scenarios across the genus. molecular evidence for genetic introgression through- Although jumping spiders have long been held as out Habronattus. Phylogenetic data points specifically one of the quintessential examples of visual displays to the H. coecatus group, including species examined in arthropods (Forster, 1982b; Jackson & Pollard, in the preset study, as being involved in hybridization 1997; Land & Nilsson, 2002), we are now beginning to with other species groups (Maddison & Hedin, 2003). understand what we have overlooked in the past.

Courtship in many jumping spider groups is more van Doorn GS, Weissing FJ. 2004. The evolution of female complex than once assumed and includes colours and preferences for multiple indicators of quality. American vibrations imperceptible to human observers without Naturalist 164: 173–186. the aid of specialized technologies (Uhl & Elias, 2011). Doucet SM, Montgomerie R. 2003. Multiple sexual orna- For systems such as the H. coecatus group, it will be ments in satin bowerbirds: ultraviolet plumage and bowers important to not only understand how females utilize signal different aspects of male quality. Behavioural Ecology information in signals, but also why the group has 14: 503–509. evolved such multifaceted displays. Understanding Edwards GB. 1981. Sound production by courting males of Phidippus mystaceus (Araneae: Salticidae): psyche. 199– the function and evolution of signals for a variety of 214. species that differ in the complexity of their commu- Elias DO, Hebets EA, Hoy RR. 2006a. Female preference nication displays could be a window into general for complex/novel signals in a spider. Behavioural Ecology principals driving species evolution, as well as how 17: 765–771. nervous systems and decision-making processes are Elias DO, Hebets EA, Hoy RR, Maddison WP, Mason AC. organized. 2006b. Regional seismic song differences in sky island populations of the jumping spider Habronattus pugillis Griswold ACKNOWLEDGEMENTS (Araneae, Salticidae). Journal of Arachnology 34: 545–556. Elias DO, Hebets EA, Hoy RR, Maddison WP, Mason AC. We would like to thank M. C. B. Andrade, S. Sivil- 2006c. Regional song differences in sky-island populations inghem, J. Goldbogen, M. M. Kasumovic, N. Lee, L. of the jumping spider Habronattus pugillis Griswold. Hedin, S. Derkarabetian, G. B. Edwards, B. Cutler, K. Journal of Arachnology 34: 566–577. Perampaladas, D. Maddison, G. Blackburn, J. Macias, Elias DO, Land BR, Mason AC, Hoy RR. 2006d. Measur- K. Needham, J. Zhang, M. Bodner, H. Wood, and E. A. ing and quantifying dynamic visual signals in jumping Hebets for field and laboratory assistance. We would spiders. Journal of Comparative Physiology A Sensory especially like to thank Marshal Hedin who was Neural and Behavioural Physiology 192: 785–797. instrumental at all stages of this project. This project Elias DO, Lee N, Hebets EA, Mason AC. 2006e. Seismic was funded by a National Science Foundation Grant signal production in a wolf spider: parallel versus serial to DOE (IOS-1021385), National Science Foundation multi-component signals. Journal of Experimental Biology 209: 1074–1084. Graduate Research Fellowship to M.B.G., Natural Elias DO, Hebets EA, Hoy RR, Mason AC. 2005. 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SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article: Table S1. Additional coecatus group observations. Table S2. Signal Properties for Intro Motif. Table S3. Signal Properties for Tick-Rev Motifs. Table S4. Signal Properties for 3rd Leg Motifs. Table S5. Signal Properties for Thump Burst Bridge (TB). Table S6. Signal Properties for Foreleg Wave Motifs (S-Wave-Reach). Table S7. Signal Properties for Reprise Bridge (RB). Table S8. Signal Properties for Pre-Mount Motif. Doc. S1. Collection locales for all Habronattus coecatus group species. Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article.