خشونت افزایش یافته و پیروزی در مسابقات کورتیکوسترون را در اژدهای نر استرالیایی را در آبها افزایش می دهد اما باعث کاهش تستوسترون در آنها می شود

Water dragons (Intellegama [Physignathus] lesueurii) are large (to > 1 m) agamid lizards from eastern Australia. Males are fiercely combative; holding a territory requires incessant displays and aggression against other males. If a dominant male is absent, injured or fatigued, another male soon takes over his territory. Our sampling of blood from free-ranging adult males showed that baseline levels of both testosterone and corticosterone were not related to a male’s social tactic (territorial versus non-territorial), or his frequency of advertisement display, aggression, or courtship behavior. Even when we elicited intense aggression by non-territorial males (by temporarily removing territory owners), testosterone did not increase with the higher levels of aggression that ensued. Indeed, testosterone levels decreased in males that won contests. In contrast, male corticosterone levels increased with the heightened aggression during unsettled conditions, and were higher in males that won contests. High chronic male–male competition in this dense population may favor high testosterone levels in all adult males to facilitate advertisement and patrol activities required for territory maintenance (by dominant animals), and to maintain readiness for territory take-overs (in non-territorial animals). Corticosterone levels increased in response to intense aggression during socially unstable conditions, and were higher in contest winners than losers. A positive correlation between the two hormones during socially unstable conditions suggests that the high stress of contests decreased androgen production. The persistent intense competition in this population appears to exact a high physiological cost, which together with our observation that males sometimes lose their territories to challengers may indicate cycling between these two tactics to manage long-term energetic costs.

Vertebrates in which males display two or more alternative reproductive tactics provide robust model systems for the study of interactions between hormones and aggressive behavior (Baird and Hews, 2007). Steroid hormones activate male aggression associated with reproduction in many species (fish: Liley and Stacey, 1983 and Ros et al., 2004; birds: Rohwer and Rohwer, 1978 and Rohwer and Wingfield, 1981; mammals: Bouissou, 1983 and Monaghan and Glickman, 1992), including some lizards (Crews, 1975; Moore and Marler, 1987, Moore et al., 1998 and Wikelski et al., 2005). However, causal interactions between hormones and male aggression can operate in the opposite direction also. Aggression with same-sex rivals appears to elicit secretion of androgens (Arlet et al., 2011, Oliveira et al., 2009 and Smith and John-Alder, 1999), as well as corticosteroids that may reflect the social stress induced by aggression (Earley and Hsu, 2008, Gilmour et al., 2005 and Knapp and Moore, 1995). Secretion of androgens and corticosteroids might also depend on the outcome of contests with rivals, with both positive and negative associations among secretion of each hormone, social status, and winning or losing being reported (reviewed by Hsu et al., 2006). Moreover, the possibility that testosterone and corticosterone act antagonistically to one another (Moore and Jessop, 2003) may complicate matters further. If aggression prompts secretion of either hormone, levels of the other may be suppressed. The challenge hypothesis is the leading theoretical framework proposed to explain secretion of androgens in response to aggression (Wingfield et al., 1990). This hypothesis predicts that patterns of androgen secretion will be related to variation in demands on males linked to social structure and their involvement in parental activities. The challenge hypothesis was first developed for and tested in endotherms in which males are generally more aggressive during settlement of reproductive territories, but then aggression diminishes as parental activities commence (Wingfield et al., 1990). Secretion of additional androgens is expected in response to challenges from rivals when hormone levels are below physiological maximum (Wingfield et al., 1990). Because most lizards do not exhibit parental care yet it is common for males to defend territories throughout prolonged reproductive seasons during which females produce multiple clutches of eggs (Baird et al., 2001 and Fox et al., 2003), they offer interesting opportunities to test the applicability of the challenge hypothesis as a general model. If territory defense requires lizard males to maintain androgen secretion at physiologically maximal levels throughout the season, pulses of androgen secretion are not expected in response to individual challenges by rivals. Meta-analysis of male vertebrate androgen secretion in response to territorial challenges revealed only moderately strong effects (Hirschenhauser and Oliveira, 2006). Variability in the influence of aggression on androgen levels was likely influenced by differences in the context during which aggression occurred across the diversity of species sampled (Hirschenhauser and Oliveira, 2006), and a number of other ecological and behavioral variables (Goyman et al., 2007). Tests of the influence of aggression on secretion of adrenocorticoids have also generated mixed results, with both positive and negative associations being reported (reviewed by Hsu et al., 2006). Hormone responses by male lizards to contest outcome and heightened aggression are particularly variable. Male green anoles that won contests staged in the laboratory had higher androgen levels than contest-losers or control males (Greenberg and Crews, 1990). However, this response may have been influenced by the presence of females in enclosures, or the low pre-trial androgen levels of male winners. Aggression increased testosterone levels in male marine iguanas (Wikelski et al., 2005), but not in either territorial male tree lizards (Knapp and Moore, 1995) or male mountain spiny lizards (Moore, 1987). The influence of winning on both hormones depended on social status in male tree lizards, with winners having decreased testosterone, but elevated corticosterone (Knapp and Moore, 1995). These mixed results clearly indicate that data from lizard studies are insufficient to evaluate the extent to which patterns of hormone secretion in response to heightened aggression and contest outcome support theoretical predictions, and additional such studies are necessary, especially those that involve manipulations of social conditions in the field. We studied relationships among aggression, androgens, and corticosterone in the eastern water dragon, Intellagama [Physignathus] lesueurii. In our study population, males and females exhibit markedly different levels of aggression, and mature males utilize one of two alternative social tactics (territorial versus non-territorial) that are characterized by territorial males displaying at rates that were over six times that of non-territorial males which usually fled or were repelled by territory owners ( Baird et al., 2012 and Baird et al., 2013). On three occasions, however, non-territorial males challenged and defeated a territory owner and usurped their territories ( Baird et al., 2012 and Baird et al., 2013). In the present study, we used this fact to induce social changes in levels of aggression and male social tactics by temporarily removing and later reinstating individual territorial males ( Baird et al., 2012). We collected blood samples from free-ranging lizards to test whether testosterone and corticosterone differ with sex, maturity, and male social status. We also examined the extent to which hormone levels were correlated with the frequency of male behavior patterns involved in the advertisement and control of territories, and used temporary removal/reinstatement field experiments to test whether hormone levels changed in response to heightened social stress and winning or losing aggressive encounters.

Testosterone levels varied by sex and social class (H2, 108 = 58.33, P = 0.0001, Cohen’s d = 0.54), with the mean for mature males being 12.5 times that of females and 11.6 times that of lizards that we could not sex because they were immature ( Fig. 2). By contrast, baseline levels of corticosterone did not differ in these three groups of lizards (H2, 108 = 2.26, P = 0.323, Cohen’s d = 0.02). Full-size image (11 K) Fig. 2. Baseline plasma hormone levels in immature lizards of unknown sex (N = 21), mature female (N = 36), and mature male (N = 51) water dragons. Data are means ± SE. The asterisk indicates statistically higher (P = 0.0001) testosterone levels in males. Figure options Neither testosterone (t1, 29 = 0.87, P = 0.39, Cohen’s d = 0.32) nor corticosterone (t1, 29 = 0.20, P = 0.83, Cohen’s d = 0.22) levels were statistically different in territorial and non-territorial males during baseline conditions ( Fig. 3). There were also no statistically significant relationships between the three behavioral variables that we measured (displays/min, aggressive contests initiated/min, and % contests won or tied) with either hormone for all males pooled (F’s = 0.002–2.33, P’s = 0.139–0.996), or for territorial males considered separately (F’s = 0.007–2.31, P’s = 0.36–0.93). Although not statistically significant, there were positive relationships between testosterone and corticosterone when all males were pooled (F1, 29 = 2.40, P = 0.13, r = 0.28), and in territorial males considered separately (F1,13 = 3.39, P = 0.095, r = 0.46, Fig. 4). Full-size image (10 K) Fig. 3. Baseline plasma hormone levels in levels in territorial (N = 14) and non-territorial (N = 16) water dragon males. Figure options Full-size image (20 K) Fig. 4. The relationship between plasma corticosterone and testosterone (pg/mg) for (A) all male water dragons pooled, and (B) the relationship between plasma corticosterone and testosterone (pg/mg) for territorial males alone.