High male mating effort and high variation in female quality select for male mate choice, which may be expressed as differential investment of reproductive effort based on female value. Male reproductive effort includes investment in direct contest competition with rival males for access to females, yet variation in male–male contest behavior is rarely examined in the context of male mate choice. We examine such male response to variation in female body size, reproductive state, and female-speciﬁc ornamentation in the striped plateau lizard, Sceloporus virgatus. We housed lizards in trios of 2 size-matched males and one female for 5 days, such that all 3 lizards were physi- cally isolated and the males could see the female but not each other. We then placed males simultaneously into the female’s cage and scored the interaction. Male–male aggression was not signiﬁcantly affected by female body size, reproductive state, nor ornament color, but was inﬂuenced by ornament size which reliably signals the phenotypic quality of the female and her off- spring. In the presence of larger-ornamented females, males engaged in more male–male aggres- sive display behavior more quickly, and performed fewer high-intensity contact behaviors but were equally likely to escalate to this riskier level of ﬁghting. Our data suggest that males adjust their energetic investment during intrasexual competitive interactions in response to variation in the contested female which, assuming males gain direct or indirect beneﬁts from their strategic alloca- tion of reproductive effort, ﬁts the modern understanding of male mate choice. Key words: aggression, female-speciﬁc ornaments, intrasexual competition, lizards, resource quality, sexual selection Female-biased parental investment and male-biased potential repro- effort, high variation in female mate quality, and low search costs ductive rates have long been understood to select for female mate (Dewsbury 1982; Johnstone et al. 1996; Bonduriansky 2001; choice and male–male mate competition (Trivers 1972; Clutton- Edward and Chapman 2011; South et al. 2012). Brock and Vincent 1991; Andersson 1994). However, such Male mate preferences may be expressed as a rejection of females “typical” expressions of sexual selection do not preclude the expres- below some threshold (Johnstone et al. 1996; Barry and Kokko sion of male mate choice and female–female mate competition in the 2010), but such rejection behavior is not required (Olsson 1993; same species (Kraaijeveld et al. 2007; Edward and Chapman 2011) Bonduriansky 2001; Reading and Backwell 2007; Wong and and choosiness is not necessarily negatively correlated to competi- Svensson 2009; Edward and Chapman 2011). Rather, males may tiveness within a sex (Preston et al. 2005; Bel-Venner et al. 2008; express preferences as differential investment of their reproductive Candolin and Salesto 2009). Indeed, mate choice expressed by com- effort (i.e., time and/or energy in courtship, mate guarding, sperm petitive males is now well-documented across a variety of polygy- allocation, and interactions with rival males; Bonduriansky 2001; nandrous animals and appears to be selected by high male mating Edward and Chapman 2011) in response to the perceived quality of V C The Author(s) (2018). Published by Oxford University Press. 335 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact firstname.lastname@example.org Downloaded from https://academic.oup.com/cz/article-abstract/64/3/335/4950184 by Ed 'DeepDyve' Gillespie user on 21 June 2018 336 Current Zoology, 2018, Vol. 64, No. 3 potential female mates. Male mate choice is often based on female 1999a). However, males do not have exclusive access to females; on characteristics such as receptivity (Rowland et al. 1991; LeBas and average, a given female’s territory overlaps with 3.9 different males Marshall 2000; Ruiz et al. 2008), unfamiliarity (Tokarz 1992; (Abell 1999a), females are courted by multiple males (median¼ 4 Orrell and Jenssen 2002), and phenotypic indicators of fecundity males; Smith 1985), and clutches can have mixed paternity (Abell like body size (McLain and Boromisa 1987; Olsson 1993; Reading 1997). The most likely sire is the male who maintained the closest and Backwell 2007; Wong and Svensson 2009; Ancona et al. 2010). spatial relationship with the female (Abell 1997). The amount of For instance, male chameleons are more likely to court receptive vs. courtship, repeated across multiple days throughout the pre-mating non-receptive females (Kelso and Verrell 2002) and invest more period, also has an important influence on female acceptance of a time guarding larger, more fecund females (Cuadrado 1998). Males mate (Smith 1985; Kelso and Martins 2008). Thus, to maximize their are expected to gain direct benefits from such choice by maximizing chance of paternity, males need to invest significant time and energy, the number of females inseminated and/or the number of offspring both of which are limited, in each female. Sperm also may be a limited produced (Edward and Chapman 2012). Males may also bias repro- resource as up to 10% of mated females produce clutches with one or ductive investment based on female traits that signal viability and more unfertilized eggs (Abell 1999b; Weiss et al. 2009), indicating offspring quality, such as female ornaments (Amundsen et al. 1997; possible sperm depletion or poor sperm viability. Thus, S. virgatus Whiting and Bateman 1999; Weiss 2002; Torres and Velando 2005; males have high mating effort per female and low capacity to mate Weiss et al. 2009; Swierk et al. 2013), providing opportunities for with all available females, 2 factors selecting for male mate choice indirect benefits of male mate choice. While theoretical models predict (Dewsbury 1982; Edward and Chapman 2011). that indirect benefits of male choice will be weak in strictly polygynous Here, we ask whether S. virgatus males express mate choice by species (Servedio 2007; South et al. 2012), these benefits are likely strategically modulating their aggressive interactions with rival stronger when specifics of mating system and natural history limit the males in response to female reproductive value. Although the value potential number of mates a male can have (Bonduriansky 2001). of a contested resource is well known to affect contest behavior For some species, the potential number of mates is limited and (Parker 1974; Enquist and Leimar 1987; Arnott and Elwood 2008), mating investment per female is high because territorial males must this is rarely studied in the context of male mate choice. However, sequentially and repeatedly court a small number of familiar, seden- male–male aggression has been shown to vary with female mating tary females that overlap their territory in distinct patches during an status, readiness to mate, body size, and body condition (Verrell extended pre-mating period prior to attaining copulation (Smith 1986; Dick and Elwood 1990; Bridge et al. 2000; Hoefler et al. 1985; Olsson 1993). Decisions to be made include who to visit 2009; Xu et al. 2012). If this responsiveness to female reproductive when, and how much reproductive effort to expend during a given value optimizes the allocation of male reproductive effort, it should visit (Orrell and Jenssen 2002; Ruiz et al. 2008). Because reproduc- be considered in our modern understanding of male mate choice tive effort spent visiting and courting one known female is effort (Bonduriansky 2001; Edward and Chapman 2011). When male con- that cannot be spent on another, selection may favor males that are test behaviors allow females to detect quality differences among responsive to variation in female fecundity, receptivity, and/or qual- male opponents and thereby influence female choice (Wong and ity over males that allocate their reproductive effort indiscriminately Candolin 2005; Ha ¨ma ¨la ¨ inen et al. 2012), strategic male–male across these familiar females. This scenario, in which males allocate aggressive behavior may play a similar role to strategic male court- their reproductive effort across repeated interactions with a rela- ship behavior, which is a much better studied aspect of male mate tively small number of known and readily located potential mates, choice. Certainly as we expand our conceptualization of male mate has not been fully considered by models of sequential mate choice choice to include decision-making during male–male aggression, the (Fawcett and Johnstone 2003; Ha ¨ rdling and Kokko 2005; Barry and evolutionary effects of male mate choice, male–male competition, Kokko 2010). However, the benefit of discriminating among these and female mate choice will blur (Edward and Chapman 2011). females may increase as the male’s capacity to exclusively mate with In S. virgatus, male–male contests most often occur within 2 m of all available females decreases (Edward and Chapman 2011) due to, a female (Smith 1985); thus, the aggressive displays of S. virgatus for instance, short and synchronous ovarian cycles among females in males could serve as signals of male quality to both opponents and the population, female home ranges that overlap with multiple terri- potential female mates. Costs of aggressive display behaviors main- torial males, positive relationships between investment in a given taining signal honesty include restricted aerobic metabolism and female and likelihood of paternity, and/or sperm limitation increased lactate production during lateral compression, increased (Dewsbury 1982; Olsson 1993; Abell 1997; Kelso and Martins predation risk, and decreased survival (Marler and Moore 1988; 2008; Edward and Chapman 2011). Note that such discrimination Cooper 1999; Brandt 2003). Winners of these encounters tend to be among familiar females does not preclude a male from courting an larger, are closer to the center of their territory, and have invested unfamiliar female if he happens to come across one. more effort in the courtship of the contested female relative to losers Many territorial lizards express the above natural history charac- (Smith 1985). As well, the male that predominates in courtship and teristics, including the striped plateau lizard, Sceloporus virgatus. maintains the closest spatial relationship to a given female is most Sceloporus virgatus females each produce one clutch per year during a likely to mate with her (Smith 1985; Abell 1997). However, no phys- brief and synchronous breeding season, with matings occurring dur- ical characteristics have been shown to reliably predict male mating ing a 2-week period that is preceded by a prolonged courtship period success [except for an effect of body size found only among small (Rose 1981; Weiss 2002). As capital breeders (Bonnet et al. 1998), yearling males (Abell 1997), which we exclude from our study]. females are selected to be sedentary during the period of egg develop- Female characteristics informing male mate choice decisions may ment, and do not engage in active mate searching (e.g., vitellogenic include her fecundity, readiness to mate, phenotypic quality, and females are 8 times more likely than males to be inactive and are offspring viability. In S. virgatus, the former varies significantly, rarely seen traveling; Rose 1981). In contrast, territorial males sequen- from 3 to 18 eggs/clutch, and may be assessed by female body size tially visit females whose home ranges overlap his own (Rose 1981); (Vinegar 1975a; Smith et al. 1995; Abell 1999b). The latter informa- on average, a given male’s territory overlaps with 4.4 females (Abell tion can be assessed via female-specific orange ornamentation that Downloaded from https://academic.oup.com/cz/article-abstract/64/3/335/4950184 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Weiss and Dubin Female ornaments influence male–male contest behavior 337 develops on the throat during vitellogenesis, peaks near the time of (50.8 27.9 33.0 cm) arranged as shown in Figure 1. This ovulation, and fades during the month-long gravid period when arrangement allowed visual contact between the female and each females carry fertilized eggs in the oviducts (Weiss 2002). Dynamic male of a trial group, but prevented visual contact between males. changes in ornament color allow for the assessment of readiness to Each lizard had access to a dirt substrate for burrowing, a basking mate (Weiss 2002), whereas the size of the ornament is a better indi- perch, and a heat lamp on a 14:10 light cycle. Animals were fed 2 cator of female phenotypic quality, age, and the quality of her off- small crickets every other day, and water was provided ad libitum. spring (Weiss 2006, 2016; Weiss et al. 2009, 2013; Goldberg et al. After 5 days of captivity in this arrangement, the lizards took part in 2017; Table 1). Males maintain closer spatial relationships to and a behavioral trial; afterward, we confirmed female reproductive tend to more intensely court females painted to express dark orange state as vitellogenic (with ovarian follicles) or gravid (with oviductal ornaments than females painted to express pale orange or no orange eggs) via a small incision on the ventral side of anesthetized females color (Weiss 2002). If mate choice by S. virgatus males is also and then closed the incision with surgical adhesive. The following expressed via strategic investment in competition, we predict male– day, we released lizards to their site of capture. male aggression will positively correlate to female phenotype. Responsiveness to female body size or ornament color may suggest Behavioral trials direct benefits of mate choice, optimizing mate and/or offspring num- Behavioral trials (n¼ 51) were conducted every other day from 27 May ber, whereas responsiveness to female ornament size may suggest to 20 June. All trials were conducted between 09:30 and 13:30 in a additional indirect benefits of choice, optimizing offspring quality. dedicated LAHF room (mean ambient temperature¼ 27.96 0.2 C). Materials and Methods Sceloporus virgatus individuals (102 males and 51 females) were collected by noose from 22 May to 15 June in dry streambeds and surrounding plateaus near the Southwestern Research Station (SWRS) in Cochise County, Arizona, USA. All animals were col- lected within 3.5 km of each other along various forks of the Cave Creek drainage and are considered to be one genetic population. On the day of capture, we measured each lizard’s body size (snout-to- vent length; SVL; measured to the nearest 0.5 mm), counted ectopar- asitic mites, and toe clipped lizards for permanent identification. Lizards were housed on an east-facing screened porch of SWRS’s Live Animal Holding Facility (LAHF) in trial groups comprised of 2 Figure 1. Housing arrangement of Sceloporus virgatus trial groups. Animals males and 1 female (n ¼ 51 groups). Males of a trial group were size of a given trial group (e.g., $1, #1 A, and #1B) were housed such that females matched [average difference in SVL¼ 0.66 0.1 (SE) mm] and ran- could see both males but males could not see each other. Terraria are repre- domly assigned to a female with alteration to ensure all members of sented by thin black lines, opaque dividers by thick black lines, brick perches a given trial group were collected at least 100 m apart from each by rectangles with dots, PVC pipe perches by ovals, and the location of the light source by the dashed circle. other on the same day. Lizards were housed in glass terraria Table 1. Correlates of Sceloporus virgatus female-speciﬁc ornamentation Female characteristic Ornament size Ornament color Brightness or value Wavelength or chroma a b c a b c a b c Body size P X P X X X P X X a b a b a b Body condition P X X X X X a b c a b c a b c Mite load N X X X X X N X X d d d Corticosterone N X N e e Age P X a b a b a b Clutch size X N X X X P a b a b a b Average egg mass P X X X P X f f Yolk antioxidant concentration P P f f Yolk antioxidant total content P X g g g Offspring body condition P X X g g g Offspring sprint speed P P X P, signiﬁcant positive relationship; N, signiﬁcant negative relationship; X, no relationship; italics indicate near statistical signiﬁcance (0.05< P< 0.10). The sym- bol is placed between the columns for brightness and wavelength when a general “color score” was utilized in analyses. Weiss (2006). Goldberg et al. (2017). Present study. Weiss et al. (2013). Weiss (2016). Weiss et al. (2011). Weiss et al. (2009). Downloaded from https://academic.oup.com/cz/article-abstract/64/3/335/4950184 by Ed 'DeepDyve' Gillespie user on 21 June 2018 338 Current Zoology, 2018, Vol. 64, No. 3 Approximately 10 min before the start of a trial, we moved the female’s Female ornamentation tank into the observation room, wrapped it in brown paper, provided a We quantified each female’s ornament expression on the day of her clean basking brick and a heat lamp, and placed males in separate trans- behavioral trial. To measure ornament size, we photographed each port containers. To start the trials, the 2 opponent males were simulta- female’s left color patch using an Olympus C-5050 ZOOM 5 mega- neously placed into the stimulus female’s tank as far from the female as pixel digital camera set to macro mode with a superbright zoom possible. The animals were allowed to interact freely for 20 min and the F1.8 lens. Female position relative to the camera and external light- interaction was videotaped from behind a blind. ing were standardized, and a ruler was included in each photograph Videotapes were scored by M.D. for the number of and latency for calibration. We used the “Color Range” function of Adobe to perform low-, mid-, and high-intensity behaviors by the 2 male Photoshop 4.0 with a custom-made color selection file to select opponents (see ethogram, Table 2). In general, interactions began orange pixels and used the National Institute of Health’s ImageJ with low-intensity headbob and push-up displays, some interactions (1.42q) to quantify the area of that selection in mm . escalated to mid-intensity fullshow and face-off displays, and peak To measure the ornament color, we used an Ocean Optics aggression was demonstrated by risky high-intensity behaviors USB 2000 spectrometer (integration time¼ 500 ms, average¼ 5, involving physical contact: charges, bites, and bite holds. Because boxcar¼ 5) with a PX-2 xenon light source and a Spectralon white headbobs are used in multiple contexts by lizards (Martins 1993), standard. The probe was placed directly above the female’s left including both aggression and courtship, we were unable to assess patch at a standardized distance and we captured 3 reflectance spec- whether a given male headbob was directed toward the opponent tra from each female at 0.32 nm increments. We calculated orna- male or the stimulus female; however, given that courtship-specific ment “brightness” as the mean reflectance from 577 to 700 nm displays (i.e., jiggles; Vinegar 1975b) were very rare during our tri- (inclusive of yellow-to-red wavelengths) averaged across the 3 spec- als, we opted to analyze all male headbobs in the context of male– tra of a given female. In addition, we calculated the wavelength of male aggression. In contrast, the intended receiver of charges, bites, maximum reflectance (from 577 to 700 nm) and analyzed the and bite holds was obvious; thus, we were able to separately score median value across a female’s 3 spectra. and analyze these high-intensity contact behaviors performed by males to females in attempts to gain a copulation grasp. Data analysis For each intensity category, the number of behaviors performed Statistical analyses were performed using R 3.3.1 and R Studio. during a trial was negatively correlated to the latency to perform the We used t-tests, Mann–Whitney U-tests, and Chi-squared tests, as first behavior (all P 0.002). Therefore, to generate independent necessary, to assess whether there were morphological differences response variables, we used principal component analysis (PCA) among individuals involved in trials that did (n¼ 39) and did not with varimax rotation via the psych package in R (R Core Team (n¼ 12) result in the expression of male–male aggressive behavior. 2016; Revelle 2017) and extracted the rotated component scores. We used stepwise regression to examine whether male aggressive The 6 measures of male–male aggression (total number of low-, behavior was affected by female body size (female SVL, and the SVL mid-, and high-intensity behaviors and the latency to the first low-, difference between the sexes), reproductive state (categorized as mid-, and high-intensity behavior) per trial were reduced to 2 vari- vitellogenic or gravid), and ornament expression (size, brightness, max-rotated components with eigenvalues >1(Table 3). Trials with and wavelength of maximum reflectance). Only final models are large Component 1 scores had large numbers of low and mid aggres- sion behaviors with low latencies; the scores are referred to Table 3. Loadings of varimax-rotated components of a PCA with as “male–male display behavior.” Trials with large Component measures of male–male aggression 2 scores had high levels of high aggression behaviors with low esca- lation latencies to these risky behaviors; these scores are referred to Behavior Component 1 Component 2 as “male–male contact behavior.” Low-intensity behaviors (LOW) 0.90 0.17 Similarly, the number of high-intensity behaviors directed by males Mid-intensity behaviors (MID) 0.86 0.05 to the stimulus female and the latency to the first high-intensity behav- High-intensity behaviors (HIGH) 0.20 0.79 ior were reduced to one principal component that explained 85% of Latency to LOW 0.61 20.45 the variation in the full dataset. The principal component was loaded Latency to MID 0.75 20.05 positively by the number of behaviors and negatively by the latency to Latency to HIGH 0.01 0.89 the first behavior; the scores (PC1) are referred to as “female-directed % variance 42.0 27.5 behavior.” Behavior performed by the female was rare, so although it Eigenvalue 2.87 1.30 was scored, it is not used in any statistical analysis. Table 2. Ethogram of aggressive behavior modiﬁed from Weiss and Moore (2004) Intensity category Behavior Description Low Head bob Lowering and raising of the head using the neck Low Push-up Lowering and raising of the head by ﬂexion and extension of legs Mid Fullshow hold Lateral compression of the body and dewlap extension in the absence of pushups Mid Fullshow display Lateral compression of the body and dewlap extension while performing pushups Mid Face-off Two individuals performing fullshow behavior within 2 body lengths of each other, typically in an anti-parallel orientation High Charge Rapid movement toward another individual High Bite Rapid opening and closing of mouth toward or against skin of another individual High Bite hold Clamping down with mouth on another individual, who often struggles to break free Downloaded from https://academic.oup.com/cz/article-abstract/64/3/335/4950184 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Weiss and Dubin Female ornaments influence male–male contest behavior 339 Table 4. Morphological characteristics (mean6 SE and total range) and reproductive state of individuals in trials with (n ¼ 39) and without (n ¼ 12) male–male aggressive behavior Trait With aggression Without aggression Range Average male SVL (mm) 56.960.2 56.760.4 55.0–60.5 SVL difference between paired males (mm) 0.660.1 0.760.3 0–3 Female SVL (mm) 63.160.4 63.360.6 60–68 SVL sex difference (mm) 6.260.4 6.760.9 0.5–12.0 Ornament size (mm ) 6.560.9 6.161.9 0.01–29.6 Ornament brightness (% reﬂectance) 50.362.5 54.965.1 26.6–82.9 Ornament peak wavelength (nm) 627.2611.1 641.266.9 577–700 % vitellogenic (vs. gravid) 77% (30 of 39) 58% (7 of 12) presented. We confirmed that forward and backward selection As above, data from the female with a very large ornament resulted in the same final model, and verified all variance inflation emerged as having high influence on the regression (Cook’s factors (VIFs) were under 10 to avoid issues of multicollinearity distance ¼ 2.5). Repeating the analysis after excluding this female (max VIF ¼ 3.5). The number of fullshows and female-directed strengthened our conclusion (b ¼ 0.099, b ¼ 0.501, unstd std behavior were both ln-transformed [ln(1þ x)] to meet model F ¼ 12.03, P ¼ 0.001, R ¼ 0.25). 1,36 assumptions. Component 2, which describes male–male contact behavior, was To investigate the possible signal value of ornament components significantly predicted by a final model that included ornament size, (size, brightness, and peak wavelength), we used regression models body size, and reproductive state of the female (F ¼ 3.38, 3,35 with backward stepwise selection. The original models included the P ¼ 0.029, adjusted R ¼ 0.16; Table 5A). In the presence of a large- following predictors: female body size, mite load, and reproductive ornament female, opponent males had significantly lower Component 2 scores (meaning fewer male–male contact behaviors state. Orange area was ln-transformed [ln(1þ x)] to meet model and greater latencies) relative to those in the presence of a small- assumptions. ornament female (P ¼ 0.024; Figure 2C). Stimulus females with larger body sizes tended to incite more male–male high-intensity Results contact behaviors than did smaller females (P ¼ 0.066; Figure 2D). There was no significant effect of reproductive state (P ¼ 0.135). We compared morphological measurements of individuals in trials We ran a post hoc logistic regression to determine whether that did and did not result in aggressive behavior from at least 1 ornament size affected the likelihood of escalating to male–male male (Table 4). These 2 types of trials did not differ in the average contact behaviors (in contrast to the number and latency of these body size of the 2 male opponents (t ¼ 0.52, P ¼ 0.608), the size behaviors), and no significant effect was found (P ¼ 0.240). Thus, match of the opponents (W ¼ 232, P ¼ 0.971), female body size relative to contests in the presence of small-ornament females, (t ¼ 0.34, P ¼ 0.733), the size difference between the males and the contests in the presence of large-ornament females were equally stimulus female (t ¼ 0.56, P ¼ 0.577), female ornamentation likely to escalate to risky contact behaviors, but it took longer (ornament size: t ¼ 0.19, P ¼ 0.851; brightness: t ¼ 0.87, 49 49 for this to occur and therefore fewer contact behaviors were P ¼ 0.390; peak wavelength: t ¼ 1.01, P ¼ 0.319), nor female performed during the 20 min trial. Overall, 59% of trials with reproductive state (vitellogenic or gravid; v ¼ 1.59, Monte-Carlo male–male aggressive behavior escalated to higher risk contact simulated P ¼ 0.282). Trials without male–male aggression (n¼ 12) behaviors between males. are not included in further analyses. Female-directed behavior Male–male aggression Of the 39 trials with male–male aggression, 46% included female- Component 1, which describes male–male display behavior, was sig- directed high-intensity contact behaviors that we interpreted as cop- nificantly and positively predicted by the size of the female orna- ulation attempts. PC1, which describes the number of contact ment (b ¼ 0.054, b ¼ 0.318, F ¼ 4.16, P¼ 0.049, unstd std 1,37 behaviors directed toward the female and the latency to such behav- R ¼ 0.10; Figure 2A); no other predictors remained in the final ior, was significantly predicted by a final model that included female model. One female with a very large ornament had high influence body size and the size difference between the males and the stimulus on the regression model (Cook’s distance¼ 1.9). Removing this female (F ¼ 3.52, P ¼ 0.040, adjusted R ¼ 0.12; Table 5B). female did not affect the interpretation, though the model is 2,36 Males more frequently and more quickly attempted copulation with strengthened (b ¼ 0.104, b ¼ 0.471, F ¼ 10.25, P ¼ 0.003, unstd std 1,36 females that were more similarly sized to themselves (P ¼ 0.016), R ¼ 0.22). Thus, females with large ornaments incited more male– and tended to do the same toward large females (P ¼ 0.113). This male aggressive displays more quickly than did females with small suggests that the underlying factor is actually male body size. In a ornaments. post hoc analysis, PC1 scores of larger males were significantly We also directly analyzed the total number of fullshow higher than that of smaller males (b ¼ 0.250, b ¼ 0.377, behaviors, as this is the behavior that involves lateral compression unstd std F ¼ 6.13, P ¼ 0.018, R ¼ 0.14). and is known to serve as an endurance handicap signal in other 1,37 phrynosomatid lizards (Brandt 2003). Orange area was the only variable to remain in the model and marginally positively Female ornament influenced the number of fullshows performed (b ¼ 0.047, We assessed the possible signal value of ornament size, brightness, unstd b ¼ 0.312, F ¼ 4.00, P ¼ 0.053, R ¼ 0.10; Figure 2B). and peak wavelength to assess why ornament size may be a more std 1,37 Downloaded from https://academic.oup.com/cz/article-abstract/64/3/335/4950184 by Ed 'DeepDyve' Gillespie user on 21 June 2018 340 Current Zoology, 2018, Vol. 64, No. 3 A B ● ● ● ● ●● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ●● ● ●● ● ● ● ● ● ● ● ● ● ● ● ●●●● ● ●● ● ● ● ● ●● ● 0 5 10 15 20 25 30 0 5 10 15 20 25 30 2 2 Ornament size (mm ) Ornament size (mm ) C D ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● −10 −5 0 5 10 15 20 −4 −2 0 2 4 Residuals of ornament size (mm ) Residuals of female body size (mm) Figure 2. Effect of female characteristics on male–male aggressive interactions. (A and B) There is a signiﬁcant positive inﬂuence of female ornament size on male–male display behavior (P ¼ 0.049) and a similar trend when isolating the number of fullshows (P¼ 0.053). The dashed lines show regression lines after removal of an inﬂuential data point (p ¼ 0.003, p ¼ 0.001). (C and D) Partial regression plots show the effect of female ornament size (P¼ 0.024) and body size A B (P¼ 0.066) on male–male contact behaviors when controlling for other model parameters. Table 5. Unstandardized and standardized coefﬁcients from multivariate regressions concerning (A) male–male (F ¼ 3.35, P ¼ 0.030) and 3,35 (B) male-to-female (F ¼ 3.52, P ¼ 0.040) high-intensity contact behaviors 2,36 Model predictor Unstandardized coefficient Standardized coefficient P (A) Male–male contact behaviors Ornament size 0.065 0.384 0.024 Female body size 0.134 0.306 0.066 Reproductive state: Gravid 0.550 0.135 (B) Female-directed contact behaviors Female body size 0.191 0.431 0.113 Sex difference in body size 0.257 0.672 0.016 Discussion salient signal to males than ornament color. Ornament size was pos- itively related to female body size (b ¼ 0.128, b ¼ 0.344, Aggressive behavior between male striped plateau lizards was unstd std influenced by the stimulus female’s ornament size, but was not sig- F ¼ 6.58, P ¼ 0.013, R ¼ 0.12, Figure 3A); this pattern remained 1,49 nificantly influenced by the ornament color, body size, nor repro- significant (P¼ 0.032) when we instead used relative ornament size ductive state. In the presence of large-ornamented females, (ornament size/body size). Brightness and peak wavelength of the aggressive male–male display behavior was performed more quickly ornament were only predicted by reproductive state (brightness: and more frequently. Given the overall explanatory power of the F ¼ 4.95, P ¼ 0.031, R ¼ 0.09, Figure 3B; peak wavelength: 1,49 statistical models was moderate to low, there are surely additional F ¼ 4.83, P ¼ 0.032, R ¼ 0.09, Figure 3C). Gravid females had 1,49 unmeasured factors involved in mediating these encounters such as brighter and more red ornaments than did vitellogenic females. Downloaded from https://academic.oup.com/cz/article-abstract/64/3/335/4950184 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Residuals of male−male contact behavior Male−male display behavior −1.5 −0.5 0.5 1.0 1.5 −1 012 Residuals of male−male contact behavior Number of fullshows −1.5 −0.5 0.0 0.5 1.0 1.5 0 5 10 15 20 25 30 Weiss and Dubin Female ornaments influence male–male contest behavior 341 contest behavior; the relative roles of these forces remain to be determined. Alternatively, S. virgatus males may be incited to escalate more quickly to risky contact behaviors and express more of these behav- iors in the presence of small-ornament females, as these females may be further from ovulation (Weiss 2002) and perhaps may be more likely to be unmated. Given that reproductive state was not signifi- ● ● ● ● ● ● ● cant in any model examining male–male aggression, we find this lat- ●● ● ● ● ● ● ● ● ter hypothesis to be less supported than the former. It is more likely ●● ● ● that males escalated to contact behaviors more quickly with small- ● ●● ● ● ● ●● ● ●●● ● ● ● ornamented females simply because they spent less time and energy engaged in display behaviors during these 20 min trials; ornament 60 62 64 66 68 size did not affect the likelihood of escalation, but rather the timing Female body size (mm) of it. It is noteworthy that male–male aggressive behavior was unre- sponsive to female body size and reproductive state as these are common targets of male mate choice due to their association with fecundity (Olsson 1993; Bonduriansky 2001; Reading and Backwell 2007; Ruiz et al. 2008; Edward and Chapman 2011, 2012). However, we did find a trend for more male–male contact behavior in the presence of larger females, perhaps indicating a tendency to accept a higher level of risk in the presence of more fecund females. Note that our results are specific to decision-making in the context of male–male aggression and do not inform us about the effect of female body size and reproductive state on other forms of mating investment. For instance, Abell (1997) found that S. virgatus males Vitellogenic Gravid are more likely to maintain close spatial relationships with large Reproductive state females than with small females. Overall, we conclude that males express differential investment in male–male aggressive displays (i.e., mate choice), in part, by stra- tegically investing more reproductive effort in the presence of females with larger ornaments. In our current cohort of females, ornament size was positively related to body size and was unrelated to mite load and reproductive state. In previous studies, females with larger ornaments have been found to be in better condition with fewer ectoparasitic mites and lower corticosterone levels, are older, produce larger eggs with more yolk antioxidants, and produce offspring in better body condition and with faster sprint speeds n= 37 n= 14 (Weiss 2006, 2016; Weiss et al. 2009, 2011, 2013). Differences in the results of this study with Weiss (2006) and Goldberg et al. Vitellogenic Gravid (2017) (see Table 1) may be due to differences in environmental con- Reproductive state ditions during those years of study (e.g., Chaine and Lyon 2008; Sockman 2009; Evans and Gustafsson 2017). Overall patterns sug- Figure 3. Possible signal value of ornament size, brightness, and peak wave- length. (A) Ornament size was positively related to female body size gest that males who are strategically responsive to female ornament (P¼ 0.013), whereas (B) ornament brightness (P ¼ 0.031) and (C) peak wave- size may potentially gain both direct (this and previous studies) and length (P¼ 0.032) were predicted only by reproductive state. Relative to vitel- indirect (previous studies) fitness benefits. However, males do not logenic females, gravid females had brighter and redder ornaments. seem to be prioritizing information about fecundity over informa- tion about other quality metrics during male–male contests given potential chemical cues of female mating status and individual dif- that female body size itself did not significantly predict male–male ferences among males in mate choice preferences, recent win/loss aggressive behavior. Future work will strive to disentangle the history, jaw morphology/strength, and neuroendocrinology. Males potential benefits of more vs. higher quality offspring by quantifying may benefit from performing more male–male aggressive displays if the evolutionary fitness implications of S. virgatus male mate choice. females exploit the displays to assess male quality and use this infor- Of course, it remains possible that males receive no benefit from this mation when making their own mate choice decisions (Wiley and differential investment in male contest behavior or benefit from their Poston 1996; Candolin 1999; Wong and Candolin 2005; Aquiloni mate choice via a non-sexually selected mechanism (e.g., West- et al. 2008; Chan et al. 2008; Ha ¨ma ¨la ¨ inen et al. 2012), which seems Eberhard 1983). likely for S. virgatus (e.g., Smith 1985) but needs to be tested The presence of male mate choice based on female ornaments is directly. If so, males may be selected to accept the costs of prolonged often assumed to equate to sexual selection on the female trait, aggressive display behavior in the presence of higher quality females. though this may not be the case (Edward and Chapman 2011; This hypothesis suggests that male mate choice, male–male competi- Fitzpatrick 2015; Fitzpatrick and Servedio 2017). For female orna- tion, and female mate choice may all affect the evolution of male ments to be sexually selected by male mate choice, females must Downloaded from https://academic.oup.com/cz/article-abstract/64/3/335/4950184 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Wavelength of Ornament size (mm ) max reflectance (nm) Brightness (% reflectance) 300 400 500 600 700 0 20406080 0 5 10 15 20 25 30 342 Current Zoology, 2018, Vol. 64, No. 3 benefit from males’ responses by increasing the number and/or qual- and indirect benefits from their mate preference. Although our mod- ity of mates. One commonly invoked mechanism by which females ern understanding of male mate choice encompasses differential can benefit is a form of “indirect female mate choice” (Wiley and investment in male–male competition (as well as in courtship, mate Poston 1996) where females produce signals that incite male–male guarding, sperm allocation, etc.; Bonduriansky 2001; Edward and competition and benefit by gaining higher quality mates (Farr and Chapman 2011), little work has empirically examined how male– Travis 1986; Montgomerie and Thornhill 1989; Wong and male aggressive behavior is directly affected by the quality of the Candolin 2005). It is therefore surprising that the effect of female female being contested. Male–male aggression is typically consid- ered to be a cost of male mate choice and not an expression of it ornaments on male–male aggressive behavior is rarely examined (Fawcett and Johnstone 2003; Servedio and Lande 2006; Servedio directly as we did here [but see Cox and Le Boeuf (1977); Given 2007; Mautz and Jennions 2011; Edward and Chapman 2012). (1993); Cui et al. (2010); and Xu et al. (2012) for studies of female While we do not question the costliness of contests, game theory vocalizations]. Females may also benefit from ornament expression surely predicts an effect of resource quality on fighting decisions via non-sexually selected mechanisms, including social selection (Parker 1974; Enquist and Leimar 1987; Arnott and Elwood 2008) (West-Eberhard 1983); for instance, by motivating a male to fight and this requires study in the context of male mate choice. Further, against a rival male, females may avoid persistent courtship from we encourage new theoretical models to consider the mating system other males (Abell 1997). As evidence for male mate choice based of territorial lizards and how a limited pool of familiar, sedentary, on female ornaments continues to accumulate, it will be important and predictably located females who do not engage in active mate to also discern if and how male responses benefit females and select searching and who require high mate investment may affect the evo- for female ornaments (Fitzpatrick 2015). lution of mate choice in males, as well as the strength of direct and Males’ female-directed behaviors (i.e., charges, bites, and bite holds interpreted as aggressive copulation attempts) were not indirect benefits, and the resulting selective pressure on female phe- affected by female ornament expression nor reproductive state, notype. Model predictions can be tested by taking advantage of the which was unexpected given the effect of ornamentation on wealth of diversity among lizard natural histories that impact limita- S. virgatus male–male aggression and the importance of reproduc- tions on male mate investment and variation in female mate quality, including differences in breeding season (from short and highly syn- tive state on male mate choice in many other species chronous to long and asynchronous), number of clutches per year (Bonduriansky 2001; Edward and Chapman 2011). Previous stud- (from one to many), clutch size (from fixed to highly variable), ies suggest that S. virgatus males are quite persistent when attempt- female ornament expression (from female-specific to male-like to ing copulation and are not attentive to female cues at that time absent), and more. (Abell 1997; Weiss 2002). Female-directed behaviors were more frequent when males and females were more closely size matched. Given that S. virgatus malesare smallerthanfemales,thismay Author Contributions indicate “prudent” decisions by the male (Ha ¨ rdling and Kokko 2005) to avoid attempts at subduing females much larger than they M.D. and S.L.W. conceived the study design. M.D. conducted the are, as they are unlikely to be successful and could possibly lead to experiment and scored all videos. S.W. conducted the statistical injury. Females have been observed to chase, charge, nip, and analysis and wrote the manuscript. Both M.D. and S.L.W. edited the head-butt persistent males in the field (Vinegar 1975b; Abell manuscript and approved the final version. 1997). However, because males’ female-directed behavior also tended to be more frequent toward larger females, together the Acknowledgments 2 predictors of the model (i.e., smaller size difference and larger We thank Brittany Balbag, Sandy Olenic, and Laura Wisdom for help in the female size) suggest that it is actually the body size of the males, ﬁeld, SWRS staff and volunteers for logistical support, and Peter Wimberger and not that of the female, that explains this response. A post hoc for feedback on an early draft of this manuscript. This research was supported model confirmed that larger males were more persistent in their by a Murdock Charitable Trust Life Sciences Grant (S.L.W.) and the female-directed behaviors than were smaller males, perhaps due to University of Puget Sound (S.L.W. and M.D.). Work was conducted with higher resource holding potential, higher chances of success, and approval from Coronado National Forest (Special Use Permit for Research), lower chances of injury. However, there were no successful copula- Arizona Game and Fish Department (Scientiﬁc Collecting Permit No. tions during our trials, likely indicative of the high mating invest- SP730610), and the University of Puget Sound (Institutional Animal Use and ment females require prior to accepting a mate and/or interference Care Committee Protocol). from opponent males. Both male mate choice and female-specific ornaments are well References documented in lizards (Tokarz 1992; Olsson 1993; Cuadrado 1998; Whiting and Bateman 1999; Cuadrado 2000; LeBas and Marshall Abell AJ, 1997. Estimating paternity with spatial behaviour and DNA 2000; Kelso and Verrell 2002; Orrell and Jenssen 2002; Weiss 2002; ﬁngerprinting in the striped plateau lizard Sceloporus virgatus Ruiz et al. 2008; Chan et al. 2009; Swierk et al. 2013; Stuart-Fox (Phrynosomatidae). Behav Ecol Sociobiol 41:217–226. Abell AJ, 1999a. 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