REGIONAL SEISMIC SONG DIFFERENCES IN SKY ISLAND POPULATIONS OF THE JUMPING PUGILLIS GRISWOLD (ARANEAE, SALTICIDAE) Author(s): Damian O. Elias, Eileen A. Hebets, Ronald R. Hoy, Wayne P. Maddison, and Andrew C. Mason Source: Journal of Arachnology, 34(3):545-556. 2006. Published By: American Arachnological Society DOI: 10.1636/S05-77.1 URL: http://www.bioone.org/doi/full/10.1636/S05-77.1

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. 2006 (2007). The Journal of Arachnology 34:545–556

REGIONAL SEISMIC SONG DIFFERENCES IN SKY ISLAND POPULATIONS OF THE HABRONATTUS PUGILLIS GRISWOLD (ARANEAE, SALTICIDAE)

Damian O. Elias,1,2,5 Eileen A. Hebets,3 Ronald R. Hoy,4 Wayne P. Maddison2 and Andrew C. Mason1: 1Division of Life Sciences, Integrative Behaviour and Neuroscience, University of Toronto at Scarborough, 1265 Military Trail, Scarborough, Ontario, M1C 1A4, Canada; 2Departments of Zoology and Botany, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada; 3School of Biological Sciences, University of Nebraska, Lincoln, Nebraska 68588, USA; 4Department of Neurobiology and Behavior, Cornell University, Ithaca, New York 14850, USA.

ABSTRACT. Jumping have long been used as model organisms to study visual communication. However, recent studies documenting the presence of intricate multicomponent seismic songs during court- ship displays suggest an important role of seismic communication as well. Given the relatively recent focus on seismic communication, the extent to which seismic songs vary among jumping spider species or even among populations remains poorly understood. Here, we use the extensively studied Habronattus pugillis Griswold 1987 complex to explore putative seismic song diversity among males from isolated populations. H. pugillis populations have been studied extensively because of the tremendous diversifi- cation of male visual secondary sexual ornaments observed among adjacent mountain-top populations in southeastern Arizona (‘‘sky islands’’). Here, we aim to explore putative parallel patterns of diversification in seismic courtship songs between different sky island populations. Using laser vibrometry, we examined in detail the songs of three mountaintop populations (Atascosa (AT), Santa Rita (SR), and Santa Catalina (SC)) and observed an extraordinary diversity of songs and song types among these three populations. Large differences were seen in both the temporal and spectral properties of male seismic songs. In addition, we observed differences in song complexity between populations with some populations having ‘‘simple’’ songs (1 component) and others having ‘‘complex’’ songs (3 components). We also present preliminary data from four additional populations (Galiuro (GA), Huachuca (HU), Mule (MU), and Patagonia (PA)). Results from this study suggest that the diversification of male visual signals observed among populations of H. pugillis finds a counterpart in male seismic songs Keywords: Seismic communication, signal evolution, species diversification, Salticidae

Jumping spiders have proven to be fruitful Forster 1982a,1982b; Richman 1982; Clark & models in the study of ecology, behavior, and Uetz 1990, 1992, 1993; Tarsitano & Jackson evolution, particularly as it relates to visually 1992, 1994, 1997; Edwards & Jackson 1994; guided behaviors (Land 1969a, 1969b, 1985; Jackson & Pollard 1996; Harland et al. 1999; Eakin & Brandenburger 1971; DeVoe 1975; Harland & Jackson 2000, 2001, 2002; Naka- Williams & McIntyre 1980; Blest et al. 1981; mura & Yamashita 2000; Taylor et al. 2000, Land & Nilsson 2002). Studies have demon- 2001; Clark & Morjan 2001; Jackson et al. strated the amazing visual abilities that jump- 2005; Li & Lim 2005; Nelson et al. 2005; ing spiders possess by focusing on behaviors Hoefler & Jakob 2006; Nelson & Jackson from a variety of contexts including predatory, 2006; Su & Li 2006). However, recent re- navigational, mating, and competitive inter- search has highlighted the utilization of seis- actions (Crane 1949; Jackson 1977; Hill 1979; mic (vibratory) songs during courtship dis- plays (Jackson 1977, 1982; Edwards 1981; 5 Corresponding author. E-mail: elias@utsc. Gwynne & Dadour 1985; Maddison & Strat- utoronto.ca ton 1988a, 1988b; Noordam 2002; Elias et al.

545 546 THE JOURNAL OF ARACHNOLOGY

2003) and a few studies have demonstrated tain range, males are very similar (Maddison that these seismic songs are crucial for mating & McMahon 2000). Using a combination of success (Elias et al. 2004, 2005, 2006a). De- behavioral, molecular, and phylogenetic data, spite the recent increase in studies focused on Masta & Maddison (2002) demonstrated that seismic communication in jumping spiders, sexual selection was driving the observed di- we still know very little about the taxonomic versification of male traits. Hebets & Maddi- breadth and/or importance of this mode of son (2005) then suggested that a process of communication within the family Salticidae. antagonistic co-evolution (Holland & Rice Jumping spiders in the genus Habronattus 1998) could be responsible for driving among- have been the subject of extensive studies fo- population variation in female mating prefer- cused on species diversification, phylogeog- ences and associated male traits. In a recip- raphy, communication, mate choice, signal de- rocal mate choice study, they found a sign, and sexual selection (Griswold 1987; xenophilic mating preference in which H. Cutler 1988; Maddison & Stratton 1988a, pugillis females from the Santa Rita Moun- 1988b; Masta 2000; Maddison & McMahon tains preferred males from a foreign popula- 2000; Masta & Maddison 2002; Elias et al. tion, from the Atascosa Mountains, over their 2003, 2004, 2005, 2006a, 2006b; Maddison & Hedin 2003; Hebets & Maddison 2005). Not own local males (Hebets & Maddison 2005). only is this genus diverse, with over 100 spe- Male H. pugillis from the Atascosa (AT) and cies described in North America (Griswold Santa Rita (SR) populations were also recent- 1987; Maddison & Hedin 2003), but it also ly observed to produce complex seismic songs incorporates extensive morphological and be- (Elias et al. 2005, 2006a). In a follow-up study havioral differentiation among its many spe- exploring the previously established SR fe- cies. Habronattus males include some of the male preference for AT males (Hebets & Mad- most elaborate male ornamentation and visual dison 2005), Elias et al. (2006a) demonstrated courtship behaviors known among any spider that a female bias for complex/novel seismic species (Peckham & Peckham 1889, 1890; signals was responsible for the observed xen- Griswold 1987; Maddison & Hedin 2003). In ophilic preference and suggested that a gen- addition to their elaborate ornamentation, it eral bias for complexity/novelty among fe- was recently demonstrated that some species males could have contributed to the rapid of Habronattus produce complex multicom- diversification observed in the H. pugillis ponent seismic songs (vibrations) simulta- group (Masta 2000; Masta & Maddison neous with visual signals during courtship 2002). (Maddison & Stratton 1988b; Elias et al. The goal of this particular study was to doc- 2003, 2005, 2006a). Furthermore, these seis- ument and compare seismic courtship songs mic signals were shown to be a crucial factor of H. pugillis populations. In so doing, we in mating decisions (Elias et al. 2004, 2005). demonstrate that the striking diversity of vi- One particularly well studied group of Ha- sual displays observed among populations of bronattus are those in the H. pugillis complex. H. pugillis finds a counterpart in seismic In North America, populations of H. pugillis songs among populations. We detected differ- Griswold 1987 occur in woodland habitats ences in both the temporal and spectral prop- isolated at the top of mountain ranges in erties of songs between populations. In addi- southeastern Arizona and into Mexico. These tion, we observed differences in the mountain ranges are known as ‘‘sky islands’’ because their peaks form an archipelago of complexity of songs, with some populations isolated woodlands separated by desert low- having songs with a single component and lands (Warshall 1995). Males from these var- others having multiple components. This is ious isolated populations are exceptional in the first study to our knowledge to show re- that each possesses distinct secondary sexual gional differences in spider songs. We suggest traits involving both morphological and be- that seismic songs along with visual orna- havioral differences (Maddison & McMahon ments are under strong selection in H. pugillis 2000; Elias et al. 2006b). While there is an and we discuss the evolutionary forces that impressive among-population variation in H. may have driven this diversification of seismic pugillis males, within a population or moun- songs. ELIAS ET AL.—SEISMIC SONGS IN HABRONATTUS PUGILLIS 547

METHODS and thus we have no data on male age. We Spiders.—Male and female H. pugillis were recorded seismic vibrations using a laser dop- collected from different mountain ranges in Ar- pler vibrometer (LDV) (Polytec OFV 3001 controller, OFV 511 sensor head) (Michelsen izona (Atascosas (AT) 31Њ24.63ЈN, 111Њ8.77ЈW; et al. 1982). Pieces of reflective tape (approx. Santa Ritas (SR) 31Њ40.38ЈN, 110Њ52.82ЈW; 1mm2) were attached to the underside of the Santa Catalinas (SC), 32Њ21.40ЈN, 110Њ55.37ЈW; courtship substrate 2 mm from the female to Galiuros (GA), 32Њ34.58ЈN, 110Њ16.50ЈW; Hu- serve as measurement points for the LDV. The achucas (HU) 31Њ25.94ЈN, 110Њ17.50ЈW; Pata- LDV signal was recorded on the audio track gonias (PA) 31Њ23.87ЈN, 110Њ44.44ЈW, and during standard video taping of courtship be- Mules (MU) 31Њ29.68ЈN, 109Њ59.82ЈW) over havior (Sony DVCAM DSR-20 digital VCR, three field seasons (April–June 2002, April– 48 kHz audio sampling rate). Spectrograms May 2003, April–May 2004). Males and fe- were made using Raven software (Cornell males were collected as immatures and adults. University, Lab of Ornithology). We present Male courtship songs were recorded up to a detailed measurements of spider songs of maximum of 3 mo after the were col- three populations (AT, n ϭ 15; SR, n ϭ 12; lected. As males senesce, they cease to initiate SC, n ϭ 12). Means are given Ϯ SD. courtship and instead avoid or act aggressive to- As it was not possible to record songs for wards females (Elias, pers. obs.), thus only all the populations using LDV, we present pre- males that actively courted females were used. liminary data on songs from four more pop- Animals were housed individually in plastic ulations (GA, n ϭ 10; PA, n ϭ 5; MU, n ϭ containers (AMAC Plastic Products, Petaluma, ϭ ϫ ϫ 3; HU, n 3) that we recorded using a cus- CA; 3 3 5cm) and kept segregated by sex. tom piezoelectric sensor built from a turntable Animals were kept in the lab on a 12:12 light: needle cartridge. For this recording technique, dark cycle. Spiders were fed fruit flies (Dro- the courtship arena was a sheet of graph paper sophila melanogaster) and juvenile crickets attached to a square cardboard frame (60 ϫ (Acheta domesticus) once a week. Male voucher 45 cm). Females were tethered as above and specimens are deposited at the Royal Ontario the male’s seismic signals were recorded using Museum, Toronto, Canada. a piezo-electric sensor placed directly under- Recording procedures and analysis.— neath the tethered female. Ten different fe- Detailed measurements on seismic songs were males were used in piezo-electric recordings. made using laser vibrometry (Elias et al. In comparing populations where we recorded 2003). We first anesthetized a mature female a male’s signal using both LDV and the piezo- H. pugillis with CO2 and tethered her to a wire electric sensor, we observed that although low with low melting point wax (beeswax). We frequency responses (Ͻ150 Hz) were relative- held females in place with a micromanipulator ly attenuated by the piezoelectric sensor, the ϫ on a substrate of nylon fabric (25 30 cm) male’s signals were not significantly altered stretched across a needlepoint frame to stan- and all signal components were apparent al- dardize the tension of the nylon. As courting beit at lower amplitude (Elias et al. 2003). All substrate has significant effects on signal piezo recordings were conducted in a sound- transmission (Magal et al. 2000; Cokl et al. attenuated chamber at Cornell University. 2004, 2005; Elias et al. 2004), we used the Seismic signals were amplified (Nikko nylon fabric as our courting surface since it NA790), recorded on the audio track of a vid- has negligible resonance characteristics and eo recording as above (48 kHz audio sampling passes all frequencies equally (Elias et al. rate) and high-pass filtered (Ͼ 150 Hz). We 2003, 2006c), thus enabling us to observe all present examples of typical spider songs from the potential temporal and frequency compo- the recordings available. nents of a male’s song. Mature males were As all recordings were conducted with teth- dropped individually onto this substrate 15 cm ered females, it is possible that males behave from the female and allowed to court freely. differently under these conditions than they Recordings began when males orientated to- would in the field. These differences however wards females. Fifteen different females were appear to be more in the duration of courtship used to initiate courtship from thirty-nine ma- displays and not in the individual song com- ture males. Males were collected as matures ponents. For example, in situations where fe- 548 THE JOURNAL OF ARACHNOLOGY males were not tethered, males courted for Some populations only include the crackle longer durations overall, but used the same component (see below) and these tend to have song components (Elias, pers. obs.). In addi- crackles that are longer in duration than pop- tion, since males were collected as matures, ulations with additional components. The sec- they may have previously mated in the field. ond component (B) (‘‘rasp’’) is generally long Here, also, we suggest that previous experi- in duration and broad in frequency. Rasps oc- ence is unlikely to alter the specific compo- cur in all populations immediately prior to an nents of seismic signal production but, in- attempted mount but, in some populations, stead, alters more plastic behaviors such as from long distances. The third component (C) courtship duration or latency to court. (‘‘drone’’) is short in duration and broad in frequency but occurs at lower frequencies RESULTS than crackles. Drones occur in bouts consist- Visual courtship signals in H. pugillis.— ing of multiple signals produced rapidly fol- The visual courtship behavior of H. pugillis lowing each other. varies by population, but in general courtship All H. pugillis songs are composed of sim- can be divided into two main stages: (1) the ilar song components, but there is variation in approach stage and (2) the pre-mount stage (1) the types and number of components and (Maddison & McMahon 2000). In the ap- (2) the temporal and spectral characteristics of proach stage, the male raises and spreads his the different components. Below are detailed first pair of legs and lowers and spreads his descriptions of male songs of three different palps. The male then proceeds to approach the sky island populations followed by prelimi- female either directly or in a sidling motion nary descriptions of four additional popula- while flicking (rapidly moving) his forelegs tions. and pedipalps in a stereotyped manner. When Courtship behavior of H. pugillis.—Santa the male gets within one to two body lengths Rita (SR) males: The courtship behavior of SR of the female, the pre-mount stage begins males begins with rotations of the palps (Mad- (Maddison & McMahon 2000). In the pre- dison & McMahon 2000). This palpal rotation mount stage, the male’s approach slows down, is unique to SR males and is continued and leg and pedipalp flicking becomes more throughout the courtship display. Palpal rota- rapid—especially downward flicks of the first tions are often punctuated with rapid leg pair of legs. Males also scrape the abdomen flicks. Males remain mostly stationary during repeatedly against the carapace just prior to courtship until the actual approach to the fe- mounting a female. It was suggested by Mad- male, which is generally direct rather than si- dison & McMahon (2000) that this grinding dling. The final stages of courtship involve the corresponded to the production of seismic male holding his first pair of legs above the songs. female and flicking the tips. Leg flicking oc- Seismic songs in H. pugillis.—Seismic curs less often than in other populations (i.e., songs are, in fact, produced by H. pugillis AT, SC, PA, HU). Leg flicks are coordinated males at the moment the abdomen is seen to with seismic songs (Fig. 1) which consist of rub against the carapace. Preventing the ab- a single component. SR seismic songs are of domen from moving relative to the carapace variable duration but are generally short (0.56 prevents song production (Elias et al. 2006a). Ϯ 0.393 s; n ϭ 17) and consist of high inten- Song production varies from population to sity, broad band (range: 0–2850 Hz; peak fre- population and males can produce songs in the quency: 1082 Ϯ 540 Hz; n ϭ 17) crackles approach stage and/or the pre-mount stage. (labelled ‘‘a’’ in Fig. 1). Some SR males in- Song production is usually coordinated with clude rasps at extremely short ranges just prior flicking of forelegs. The general H. pugillis to attempted copulation (Fig. 1, 48–55 s, SR song can have three components. The first column). The majority of seismic signals how- component (A) (‘‘crackle’’) is generally of ever only include the crackle component (Fig. short duration, broad frequency and relatively 1). high intensity; crackles have an impulse-like Santa Catalina (SC) males: SC courtship quality. The crackle component is generally begins with rapid foreleg flicks followed by the first song component produced and is pres- body shakes (rapid side-to-side movements) ent in all observed populations of H. pugillis. during the approach stage of courtship (Mad- ELIAS ET AL.—SEISMIC SONGS IN HABRONATTUS PUGILLIS 549

Figures 1–3.—Habronattus pugillis song from the Santa Rita, Santa Catalina and Atascosa mountain populations. 1. Oscillograms of seismic songs. 2. Detail of oscillograms (boxes in Fig. 1). 3. Spectrogram of song in Fig. 2. The notation a–c in Figs. 2 & 3 identifies the three seismic components of male songs. dison & McMahon 2000). After body shaking, Atascosa (AT) males: AT locomotory court- males approach females with vigorous foreleg ship consists of rapid sidling, in which males flicking. Seismic signals are produced during move in large arcs alternating in direction leg flicks preceding body shakes as well as with the first pair of legs held continuously during late display leg flicks. Seismic signals above the ground (Maddison & McMahon are not produced during a body shake bout but 2000). After sidling, males approach females occur immediately after body shaking ends. with vigorous foreleg flicking. Seismic signals Every foreleg flick is coordinated with a seis- are produced during leg flicking and not dur- mic signal (Fig. 2). SC male seismic songs are ing the sidling display. Every leg flick is co- long in duration (1.30 Ϯ 0.20 s; n ϭ 15) and ordinated with a seismic signal (Fig. 3). AT occur in two distinct parts (Fig. 2). The first male seismic songs are long in duration (1.85 part consists of a short (0.13 Ϯ 0.16 s; n ϭ Ϯ 0.30 s; n ϭ 15) and occur in three distinct 15), high intensity, broad band (range: 0–3937 parts (Fig. 3). The first part consists of a short Hz; peak frequency: 844 Ϯ 349 Hz; n ϭ 15) (0.11 Ϯ 0.03 s; n ϭ 15), high intensity, broad ‘‘crackle’’ (labelled ‘‘a’’ in Fig. 2). The sec- band (range: 0–2640 Hz; peak frequency: ond part consists of a prolonged long duration 1069 Ϯ 339 Hz; n ϭ 15) ‘‘crackle’’ (labelled (1.17 Ϯ 0.19 s; n ϭ 15) broadband ‘‘rasp’’ ‘‘a’’ in Fig. 3). The second part consists of a (range 1: 7–1211 Hz; peak 1 frequency: 185 prolonged (1.07 Ϯ 0.34 s; n ϭ 15) broadband Ϯ 198 Hz; range 2: 900–2500 Hz; peak 2 fre- ‘‘rasp’’ (range 1: 0–650 Hz; peak 1 frequency: quency: 1373 Ϯ 317 Hz; n ϭ 15) (labelled 203 Ϯ 218 Hz; range 2: 530–2010 Hz; peak ‘‘b’’ in Fig. 2). 2 frequency: 1170 Ϯ 210 Hz; n ϭ 15) (‘‘b’’ 550 THE JOURNAL OF ARACHNOLOGY in Fig. 3). The third part consists of a variable of the forelegs. This character is unique number of ‘‘drones’’ (3–9; n ϭ 5) of short among all the populations studied (data not duration (0.04 Ϯ 0.01 s; n ϭ 18) broad band shown). (range: 0–1850 Hz; peak frequency 371 Ϯ 457 Hz; n ϭ 18) signals (‘‘c’’ in Fig. 3). Broad DISCUSSION band drones also occur along with rasps in the H. pugillis is undergoing diversification second courtship stage (‘‘b’’ in Fig. 3) but are driven by sexual selection (Maddison & Mc- lower in intensity than rasps. Mahon 2000; Masta 2000; Masta & Maddison Other H. pugillis males: We observed the 2002; Hebets & Maddison 2005; Elias et al. seismic songs of four additional populations, 2006a). Evidence suggests that sexual selec- Galiuro (GA), Huachuca (HU), Patagonia tion acting on male secondary sexual charac- (PA), and Mule (MU) mountains (Fig. 4). De- teristics has driven extensive morphological tailed measurements were not available for and behavioral divergence between popula- these populations and we were only able to tions on the sky islands of south eastern Ari- record songs using the piezoelectric device zona (Maddison & McMahon 2000; Masta & (see above). It is possible that we were not Maddison 2002). Here we show that the di- able to observe all song components using this versity observed previously was only a partial method of sound recording therefore, future picture and is further manifested in the evo- recordings will be conducted using LDV. lution of distinct and stereotyped songs among Galiuro (GA) visual courtship consists of a different populations. ‘‘first leg wavy circle’’ where the first legs are H. pugillis songs consist of similar com- held forward and the tips moved in circles si- ponents, although some populations have multaneously (but out of phase) (Maddison & more complex songs than others. Males from McMahon 2000). Periodically the first legs the Santa Rita Mountains have simple songs, come into phase (sometimes punctuated with consisting of a single component. Males of the a rapid leg flick). Seismic songs are produced other populations have more complex songs coincident with the first legs coming into with males from the Santa Catalinas having phase (with and without leg flicks). Seismic songs consisting of two components, and songs in the GA population are made of males from the Atascosas having songs con- crackles (a) and ‘‘slow’’ crackles (s-a) (Fig. sisting of three components. In addition to 4). Slow crackles appear to consist of a series these broad scale differences between popu- of crackles. Slow crackles have an impulse- lations, temporal and spectral components are like punctuated quality like crackles and are different between each population. There also different from rasps as rasps are produced as appears to be variation in the coordination of a continuous signal. visual and seismic components of courtship. Huachuca (HU), Mule (MU), and Patagonia Signal evolution involving seismic signals is (PA) male courtship songs are similar to SC thus potentially occurring along three axes: male courtship with the notable absence of (1) frequency and temporal characteristics, (2) body shakes. HU, MU, and PA males ap- song complexity, as measured by the number proach females with flicking of the first pair of seismic components and, (3) multimodal of legs. Seismic songs are produced during leg coordination. Diversification in H. pugillis has flicks. HU, MU, and PA male seismic songs probably occurred on a small temporal and occur in two distinct parts, crackles (‘‘a,’’ Fig. spatial scale suggesting that the song differ- 4) and rasps (‘‘b,’’ Fig. 4). In the early stages ences between populations are likely due to of courtship, HU males also add a unique selection and not random effects (Maddison & component to their display. HU males ap- McMahon 2000; Masta 2000; Masta & Mad- proach females slowly with the forelegs held dison 2002). Below we discuss some of the above the ground the entire time. Periodically hypotheses that may drive the observed di- males open and close their chelicerae during versity of songs. this approach. Seismic signals are produced Spectral and temporal properties in intermittently as the male slowly approaches songs often relay information about mate the female. Seismic signals during this portion quality and/or species identity, resulting in of the display consist of crackle components substantial selection on song properties (An- and are not coordinated with any movement dersson 1994; Bradbury & Vehrencamp 1998; ELIAS ET AL.—SEISMIC SONGS IN HABRONATTUS PUGILLIS 551

Figure 4.—Seismic song diversity in the sky islands of southern Arizona. Map of southern Arizona mountain ranges with outlines representing the lower limit of oak woodland habitat (Brown & Lowe 1982), corresponding to an elevation of ϳ1300–1500 m. Dots show collecting localities for H. pugillis. Representative songs are shown for populations recorded using laser vibrometry (all caps—Atascosa, Santa Rita, Santa Catalina Mts.) and a piezo-electric sensor (Galiuro, Mule, Patagonia, and Huachuca Mts.). a–c denote the three possible seismic components of male songs. *s-a denotes a ‘‘slow crackle’’.

Kotiaho et al. 1998; Parri et al. 2002; Gerhardt tial selective pressures on signal evolution and & Huber 2002). This may be the case in Ha- on the spectral and temporal characteristics of bronattus songs as well (Elias et al. 2005). signals (Michelsen 1978; Larsen & Michelsen The characteristics of the signaling environ- 1983; Romer 1998; Magal et al. 2000; Elias ment (e.g., leaves, sand) can also add substan- et al. 2004; Cokl et al. 2005). For example, 552 THE JOURNAL OF ARACHNOLOGY

Elias et al. (2004) demonstrated that seismic formation about multiple aspects of quality. songs in H. dossenus Griswold 1987 could The observed correlation between population propagate well on only a subset of available density and signal complexity however is in substrates, resulting in differential mating suc- the exact opposite direction, as our collection cess for males across substrates. Elias et al. sites with the most spiders (SR) had the sim- (2004) went on to suggest that evolution may plest seismic songs (Elias, Hebets & Maddi- lead to substrate specialization and a tuning of son, unpubl. data). Clearly, future studies fo- spectral and temporal signal characteristics to cused specifically on testing these hypotheses the particular signaling substrates available. are necessary. Similar selective pressures may have lead to A role of antagonistic coevolution has been differences in the temporal and spectral prop- suggested in the evolution of complex, diver- erties of songs between different sky island gent courtship displays of H. pugillis (Hebets populations. & Maddison 2005; Elias et al. 2006a). Under There also appears to be variation in song antagonistic coevolution models (Holland & complexity between sky island populations. Rice 1998), females are expected to evolve Differences in song complexity among popu- resistance to exploitative male signals thus lations may be due to differences in the sig- forcing males to elaborate signals that are be- naling environment between sky islands. Ef- yond the current realm of the female’s resis- ficacy-based hypotheses of complex signal tance. Following from this, females are pre- function such as the multiple sensory environ- dicted to prefer males with novel exploitative ments hypotheses (Candolin 2003; Hebets & traits over males with local traits for which Papaj 2005) suggest that multiple signals they have evolved resistance. Under this sce- evolve when there is variation in the signaling nario, if differences in song complexity in H. environment so that under some conditions pugillis are being driven by antagonistic co- some signal components can be transmitted evolution, then we would predict the follow- effectively when other signal components are ing: SR females should prefer AT and SC not. Under an efficacy backup hypothesis (He- songs over their own male songs (SR); SC bets & Papaj 2005), one would predict the AT females should prefer AT songs over SR signaling environment to be the most variable, songs and their own male songs (SC); and AT followed by the SC and the SR signaling en- females should not show any preference. He- vironments. While this possibility remains to bets & Maddison (2005) have already dem- be explicitly tested, there are no obvious dif- onstrated that SR females prefer AT males, ferences between sky island signaling envi- and that AT females did not show any pref- ronments (Masta & Maddison 2002). erences between SR and AT males. In addi- Differences in song complexity between tion, Elias et al. (2006a) showed that SR fe- populations may also be due to selection for males preferred AT males only if they could signal content, such as the need to convey produce seismic signals. Results thus far are multiple differential messages (Moller & consistent with the hypothesis that differences Pomiankowski 1993; Johnstone 1996; for re- in song complexity are being driven by antag- view of content-based hypotheses see Hebets onistic co-evolution. & Papaj 2005). H. pugillis females mate only If we include songs for which we only have once (Hebets, unpublished observations), preliminary data, there also appears to be var- therefore informative signals may be at a pre- iation between the coordination of visual and mium. Due to differential natural selection seismic signals. Some populations show no pressure across mountaintop populations, it is multimodal coordination in certain song com- possible that males from different populations ponents (HU population), while others show might need to convey different aspects of high degrees of coordination (AT, SC, MU quality to local females, resulting in divergent populations). Coordinated signaling in multi- complex displays. Variable population densi- ple modalities can present animals with mul- ties could also influence complex signaling tiple advantages including reduced signaling evolution as increased population density costs (sender), reduced processing costs (re- could increase male competition for mates, ceiver), and increased information content potentially resulting in an increase in display (Honey & Hall 1989; Partan & Marler 1999, complexity as males are forced to provide in- 2005; Rowe 1999; Candolin 2003; Uetz & ELIAS ET AL.—SEISMIC SONGS IN HABRONATTUS PUGILLIS 553

Roberts 2002; Hebets & Papaj 2005). Differ- mens (Araneae: Salticidae). Animal Behaviour ences in the importance of coordination and/ 40:884–890. or differences in the cross-modal interactions Clark, D. L. & G. W. Uetz. 1992. Morph-indepen- between visual and seismic signal could also dent mate selection in a dimorphic jumping spi- lead to the differences observed between the der: demonstration of movement bias in female different populations. choice using video-controlled courtship behavior. Animal Behaviour 43:247–254. Although, we have only described a small Clark, D.L. & G.W. Uetz. 1993. Signal efficacy and proportion of H. pugillis songs, our results the evolution of male dimorphism in the jumping show an interesting parallel with regional spider, Maevia inclemens. Proceedings of the Na- song differences in birds (Krebs & Kroodsma tional Academy of Sciences USA 90:11954– 1980). Examining other sky islands in the US 11957. and Northern Mexico will likely reveal an Cokl, A., J. Presern, M. Virant-Doberlet, G.J. Bag- even greater diversity of songs and song well & J.G. Millar. 2004. Vibratory signals of the types. Given the extraordinary diversity of harlequin bug and their transmission through songs observed in this and other studies (Jack- plants. Physiological Entomology 29:372–380. son 1977; Edwards 1981; Gwynne & Dadour Cokl, A., M. Zorovic, A. Zunic & M. Virant-Dob- 1985; Maddison & Stratton 1988a, 1988b; erlet. 2005. Tuning of host plants with vibratory Noordam 2002; Elias et al. 2003, 2005), we songs of Nezara viridula L (Heteroptera: Penta- tomidae). Journal of Experimental Biology 208: propose that jumping spiders are a good sys- 1481–1488. tem to study the function and evolution of Crane, J. 1949. Comparative biology of salticid spi- songs. ders at Rancho Grande, Venezuela. Part IV: an ACKNOWLEDGEMENTS analysis of display. Zoologica 34:159–214. Cutler, B. 1988. Courtship Behavior in Habronattus We would like to thank M.C.B. Andrade, captiosus (Araneae, Salticidae). Great Lakes En- N. Lee, M. Kasumovic, K. Gawera, and the tomologist 21:129–131. Hoy, Mason, Andrade, and Hebets Lab DeVoe, R.D. 1975. Ultraviolet and green recepetors Groups. Funding was provided by NSERC to in principle eyes of jumping spiders. Journal of ACM (238882 241419), NIH to RRH General Physiology 66:193–207. (N1DCR01 DC00103), and an NSF IRFP Eakin, R.M. & J.L. Brandenburger. 1971. Fine (0502239) to DOE. structure of the eyes of jumping spiders. Journal of Ultrastructure Research 37:618–663. LITERATURE CITED Edwards, G.B. 1981. Sound production by courting Andersson, M. 1994. Sexual Selection. Princeton males of Phidippus mystaceus (Araneae: Salti- University Press, Princeton, New Jersey. 599 pp. cidae). Psyche 88:199–214. Blest, A.D., R.C. Hardie, P. McIntyre & D.S. Wil- Edwards, G.B. & R.R. Jackson. 1994. The role of liams. 1981. The spectral sensitivities of identi- experience in the development of predatory be- fied receptors and the function of retinal tiering haviour in Phidippus regius, a jumping spider in the principal eyes of a jumping spider. Journal (Araneae, Salticidae) from Florida. New Zealand of Comparative Physiology 145:227–239. Journal of Zoology 21:269–277. Bradbury, J.W. & S.L. Vehrencamp. 1998. Princi- Elias, D.O., E.A. Hebets & R.R. Hoy. 2006a. Fe- ples of Animal Communication. Sinauer Asso- male preference for complex/novel signals in a ciates, Sunderland, Massachusetts. 882 pp. Brown, D.E. & C.H. Lowe. 1982. Biotic Commu- spider. Behavioral Ecology 17:765–771. nities of the Southwest. U.S. Forest Service Gen- Elias, D.O., E.A. Hebets, R.R. Hoy & A.C. Mason. eral Technical Report RM-78. Rocky Mountain 2005. Seismic signals are crucial for male mating Forest and Range Experimental Station, Fort success in a visual specialist jumping spider (Ar- Collins, Colorado. aneae: Salticidae). Animal Behaviour 69:931– Candolin, U. 2003. The use of multiple cues in 938. mate choice. Biological Reviews 78:575–595. Elias, D.O., B.R. Land, A.C. Mason & R.R. Hoy. Clark, D.L. & C.L. Morjan. 2001. Attracting female 2006b. Measuring and quantifying dynamic vi- attention: the evolution of dimorphic courtship sual signals in jumping spiders. Journal of Com- displays in the jumping spider Maevia inclemens parative Physiology A: Neuroethology, Sensory, (Araneae: Salticidae). Proceedings of the Royal Neural, and Behavioral Physiology 192:785– Society of London Series B-Biological Sciences 797. 268:2461–2465. Elias, D.O., N. Lee, E.A. Hebets & A.C. Mason. Clark, D.L. & G.W. Uetz. 1990. Video image rec- 2006c. Seismic signal production in a wolf spi- ognition by the jumping spider, Maevia incle- der: parallel versus serial multi-component sig- 554 THE JOURNAL OF ARACHNOLOGY

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