(d) Discussion
Our data support previous observations on the function of push-ups inS. occidentalis . This may be a visual signal displayed towards
conspecifics from longer distances and reduces the escalation of
conflicts between males differing in status (Sheldahl & Martins 2000).
The chromatic properties of the yellow patch significantly differ
between the sexes in this population and, specifically, its spectral
chroma correlates with the body length of the males (see Megía-Palma et
al. 2018b). However, it was not an important predictor of the behavioral
traits tested here, suggesting that intrasexual male competition does
not influence evolution of the yellow patches in this species.
Conversely, an intersexual signal of quality based on the display of
yellow patches was previously described in Sceloporus virgatus(Weiss 2006), a closely related species. This suggests that yellow
patches in S. occidentalis might also signal individual quality
(body size) to conspecifics of both sexes in this population
(Megía-Palma et al. 2018b), but not necessarily as an agonistic signal
of male aggression (Martins 1993).
The factor analysis of the behavioral traits indicated that Factor 1
correlates with push-ups, lateral compressions, and lunge behavior;
three behavioral traits displayed during male agonistic interactions inS. occidentalis . Indeed, the blue ventral patches are displayed
towards opponents during the performance of lateral compressions, at a
short distance of 1.6 cm between contestants in this study, and this
behavior frequently (76.1%) elicited aggressive responses from rivals.
Thus, factor 1 will be hereafter referred to as ‘aggressive behavior’.
The comparison of the SELF versus the RIVAL models provided us
with a comprehensive view of the relative importance of behavioral
traits, color, and infection as predictors of male aggressive behavior
during pairwise contests in S. occidentalis . The behaviors
summarized in factors 1 (i.e. aggressive behavior) and 3 (i.e.
submissive behavior; Table 1) of rival lizards were important
predictors, with similar magnitudes, of the aggressive behavior of focal
males (see Figs. 1a and 1c). Thus, our analyses suggest that behavioral
traits from rivals have an important influence on the aggressive
response of focal male lizards, supporting the escalated model of
aggression (i.e. Enquist & Leimar 1983) previously proposed for this
species (Sheldahl & Martins 2000). However, these relationships were
non-linear. Strikingly, this may follow a quadratic pattern with a
maximum intensity of escalation at intermediate aggression levels from
both contestants, deescalating if the aggression of the rival increases
(Fig. 1a). This suggests that push-ups, lateral compression, and lunge
behaviors may not necessarily imply physical altercation, but performing
these aggressive behaviors is exhausting for the lizards and has likely
physiological costs (Schall & Dearing 1987; Marler & Moore 1988).
Similarly, an intriguing result is the behavioral pattern observed for
focal lizards receiving submissive responses from their opponents; these
‘bully’ males performed the highest intensity of aggressive display with
no sign of de-escalation (Fig. 1c). Tail waving (i.e. Factor 4) was also
an important predictor of aggression in the RIVAL model, but its
relationship with the aggressive behavior from focal males suggested a
neutral effect on it (Fig. 1d). This behavior might have a deflective
function as proposed for other lizards with similar behavior (Telemeco
et al. 2011).
Not all the traits that significantly explained the aggressive behaviors
of focal males (i.e. Factor 1) had a positive feedback effect; some
behavioral traits likely related with dominance and correlated with
Factor 2, such as climbing on top of the rock, licking an opponent’s
body, or rubbing the cloaca on the substrate (i.e. marking), reduced the
level of aggression of the focal males. This suggests that males may use
other cues to assess fighting ability of rivals prior to confrontations,
avoiding the costs of fighting with males of higher status (Briffa 2014;
Abalos et al. 2016). Chemical scrutiny of the opponent’s scents might be
one discrimination mechanism used by the lizards because 40% (487/1217)
of the behaviors registered were tongue flicking, which was either
performed towards the ground, walls and air, or towards different parts
of the opponent’s body (Duvall 1982). This hypothesis is supported by
the fact that S. occidentalis can discriminate different
individuals by their odor (Duvall 1979). Furthermore, femoral secretions
of lizards convey cues of individual quality that may be used by
conspecifics to assess the fighting ability of rivals (Moreira et al.
2006; Martín et al. 2007; Martín & López 2007).
In addition, the spectral chroma of the rival’s blue patch had a
negative feedback effect on the aggressive escalation of focal males.
This suggests that the visual scrutiny of the rival’s blue patches can
also dissuade focal males from fighting, confirming that the ventral
blue patches of S. occidentalis play the dual role of ornaments
and of armaments during social interactions (e.g. Cooper & Burns 1987).
This is an interesting finding because when these males were infected by
intestinal coccidians of the genus Acroeimeria they exhibited
blue patches with lower spectral chroma (Megía-Palma et al. 2018b) and
in the present study the males that engaged in fights with lower
spectral chroma in their blue patches elicited more intense aggressive
behaviors from opponents. Thus, this relationship suggests that
intestinal coccidians may ultimately reduce the fitness of infected
males through intrasexual competition because infected lizards that
receive more aggression may also suffer higher costs of fights,
hindering their access to reproduction (Marler & Moore 1989).
Although less informative than behavioral and color traits of the rival,
parasites of focal lizards were also important predictors of their own
aggressive behavior. Lizards infected by haemococcidians displayed
significantly fewer push-ups, lateral compressions, and lunges. In this
population, larger males were shown to have a greater prevalence of
infection by this parasite (Megía-Palma et al. 2018b). However, the
observed effect of this parasite on the behavioral display of the males
was independent of lizard body size. The infection byLankesterella might reduce the males’ competitive ability and
ultimately hinder their access to reproduction (Schall & Dearing 1987;
Schall & Houle 1992). A similar effect was also suggested forPlasmodium mexicanum , a virulent haemosporidian parasite that
infects S. occidentalis in other localities (Schall & Dearing
1987). Interestingly, Lankesterella is a parasite that is
significantly more frequent in males (Megía-Palma et al. 2018b). In a
previous study in this population, we failed to find a significant
relationship between color expression in males and Lankesterellainfection (P = 0.06 with the spectral luminance of the blue
patch; Megía-Palma et al. 2018b). This does not discard the possibility
that females still perceived a difference, because if parasites of the
genus Lankesterella hinder the fighting ability of the males, we
expect that females could discriminate healthy males, likely based on
males winning fights (Schall & Dearing 1987). This might allow for the
vertical transmission of genes for parasite resistance into their male
offspring (Hamilton & Zuk 1982). These new findings suggest thatLankesterella may be a virulent parasite that plays an important
role promoting both inter- and intrasexual selection in this population
through its influence on males’ aggressive behavior.
Similarly, males with the higher tick load (> 6 ticks)
displayed less push-ups and lateral compressions, and performed fewer
lunges. However, this relationship was non-linear. Lizards tended to
perform more of these behaviors at low levels of infestation (Fig. 3b).
Testosterone may positively influence the aggressive behavior of this
lizard species, similar to other closely-related species of the family
Phrynosomatidae (Moore 1988; Weiss & Moore 2004), and tick load can
co-vary with the concentration of this androgen in S.
occidentalis (Pollock et al. 2012). Taken together, this suggests that
testosterone may link the aggressive behavior of males to low
intensities of tick infestation. However, as commented previously, the
opposite was observed at higher intensities of infestation. Ticks draw
blood from the lizards and significantly reduce their hematocrit at
moderate infestations (> 5 ticks according to Dunlap &
Mathies, 1993). As estimated in a previous study in this population, an
infestation of only 5 to 7 ticks may provoke, on average, a 10%
reduction of hematocrit in the lizards (Megía-Palma et al. 2020). This
may impair the rapid oxygen demands of the muscles involved in the
sudden movements displayed by the males during agonistic encounters
(Schall & Dearing 1987). Lizards with moderate tick infestations, which
likely impair the oxygen carrying capacity of the lizards’ blood, may
not be able to keep up the displays for an extended duration (Dunlap &
Mathies 1993). Thus, our results suggest that moderate infestations by
ticks reduce intensity of behavioral display during intrasexual
aggressive interactions in this species, supporting that aggressive
displays are exhausting for males. This, together with previous results
in this population, reaffirms that ticks exert an important selective
pressure on the lizards. Tick prevalence and mean intensity of
infestation are very high in April, reducing the body mass of some
lizards and potentially leading to their death (Megía-Palma et al.
2020), while later in May and June tick abundance is reduced but they
affect the behavior of the lizards during male agonistic interactions
(this study). This suggests that ticks may exert a selective pressure on
this population during April, when massive infestations of up to 61
nymphal ticks per lizard occur (Megía-Palma et al. 2020), and here we
revealed a similar pattern that may also contribute to the positive
selection of superior competitors or more resistant lizards during the
mating season.
Our results confirm the role of the male ventral blue patches as
armaments in S. occidentalis , given that its spectral chroma
deterred aggressive responses from rivals during pairwise contests.
Conversely, males with less chroma received higher intensity of
aggression. This suggests that intestinal coccidians affect male
agonistic interactions because the males infected by these parasites had
less blue chroma (Megía-Palma et al. 2018b). In addition, the negative
relationships between infection by haemococcidians and ticks at moderate
intensities (> 6), with the aggressive behavior of the
males indicate that these parasites reduce the lizards’ ability to
fight. This, altogether, suggests a role of parasites in male-male
interactions, and in the intrasexual selection of lizards. Parasite
resistance might be under selection in this population because the least
parasitized males are also the most competitive ones. Mate choice is
likely based on males’ behavioral display. Therefore, most aggressive
males likely achieve more frequent access to females (Schall & Dearing
1987). We propose here a mechanism mediated by parasites to explain how
parasites and male intrasexual competition contribute to the evolution
of a structural-based blue patch with dual function in S.
occidentalis .