General and Comparative Endocrinology 199 (2014) 33–37
Contents lists available at ScienceDirect
General and Comparative Endocrinology journal homepage: www.elsevier.com/locate/ygcen
Effects of acute corticosterone treatment on partner preferences in male and female zebra finches (Taeniopygia guttata) Kimberly A. LaPlante, Enida Huremovic, Michelle L. Tomaszycki ⇑ Department of Psychology, Wayne State University, Detroit, MI, USA
a r t i c l e
i n f o
Article history: Received 7 September 2013 Revised 27 January 2014 Accepted 2 February 2014 Available online 11 February 2014 Keywords: Corticosterone Two-choice paradigm Partner preference Social preference Sex difference
a b s t r a c t Stress alters physiology and behavior across species. Most research on the effects of stress on behavior uses chronic stressors, and most are correlational. The effects of acute stressors on physiology and behavior have been mixed. Here, we use zebra finches, a highly gregarious species that forms long-term pair bonds, to test the effects of an acute corticosterone (CORT) on opposite-sex partner preferences over a same-sex individual or a group (the latter is a highly appealing option). We had two competing hypotheses. First, we predicted that acute CORT would alter preferences for the opposite sex bird in both conditions in both sexes. However, since there is a sex difference in the effects of CORT on partner preferences in voles, these effects may be more pronounced in males than in females. To test our hypotheses, we administered 2 doses of CORT (10 lg and 20 lg) or vehicle (control) using a repeated measures design. In the male vs. female test, there was a significant Sex by Treatment interaction, such that in males, 10 lg CORT increased preferences for a female over the male compared to when these same males were treated with saline at baseline. There were no effects of treatment in females. In the opposite-sex vs. group condition, there was an overall effect of Treatment, such that the 10 lg dose increased preference for the opposite-sex individual over both saline treatments, regardless of sex. These findings further our understanding of the effects of an acute stressor on sexual partner preferences. Ó 2014 Elsevier Inc. All rights reserved.
1. Introduction Stress causes a physiological response that can have diverse effects on behavior and fitness (McEwen, 2006; Sapolsky et al., 2000). The effects of chronic stressors, such as environmental challenges, have been the most frequently studied (Breuner et al., 2008; Romero et al., 1998). Under chronic stress conditions, animals may restrict reproduction in favor of other behaviors that promote immediate survival (Astheimer et al., 1995). Most of these studies have focused on birds, and many of these studies focus on seasonal breeders. For example, in female starlings, chronic stressors decrease corticosterone (CORT) and also decrease survivorship of fledglings (Cyr and Michael Romero, 2007). In zebra finches, early life stress leads not only to decreased survivorship in adulthood, but also leads to decreased survivorship of the partner (Monaghan et al., 2012). Thus, it is clear that chronic stressors affect reproductive fitness. Fewer studies have focused on the role of acute stressors in behavior and fitness. Some have argued that response to acute ⇑ Corresponding author. Address: Department of Psychology, Wayne State University, Detroit, MI 48202, United States. Fax: +1 (313) 577 7636. E-mail address: [email protected] (M.L. Tomaszycki). http://dx.doi.org/10.1016/j.ygcen.2014.02.004 0016-6480/Ó 2014 Elsevier Inc. All rights reserved.
stressor may, in contrast to chronic stressors, be beneficial (Breuner et al., 2008). Indeed, short-term increases in CORT are either associated with an increase in sexual behavior (in musk shrews) or have no effect on reproduction (in marine toads) (Orchinik et al., 1988; Schiml and Rissman, 1999). In female Japanese quail, CORT increases in response to mating with a male, but is not altered if the female simply sees and hears a male (Rutkowska et al., 2011). This increase in CORT is transient (apparent at 5 min, but not at 3 h), and does not predict fertilization (Correa et al., 2011). Thus, acute stressors may or may not impact reproductive behavior. Even fewer studies have used CORT manipulations to mimic the stress response and test the effects on behavior. This is important for inferring cause and effect relationships between glucocorticoids and behavior. Prolonged CORT administration has no effect on courtship behaviors in side-blotched lizards (Denardo and Licht, 1993). In mountain chickadees, CORT administered directly before recovery of a food cache increases food recovery (Saldanha et al., 2000). However, acute CORT had no effect on aggression in male tree sparrows (Astheimer et al., 2000), but does increase locomotion during an intruder test in rainbow trout (Øverli et al., 2002). Thus, the effects of acute CORT administration have been mixed, and deserve further investigation.
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The present study focuses on the role of CORT in partner preferences. Most studies in birds have focused on mating, and most of these studies have used seasonal breeders (Breuner et al., 2008), which form only short-term (seasonal) relationships, or animals for which mating is stressful and is not associated with a partner preference, such as the female Japanese quail (Correa et al., 2011; Rutkowska et al., 2011). Evidence from a couple of species suggests that stress affects partner preferences. For example, exposure to an acute stressor increases attraction for females in male humans (Dutton and Aron, 1974). In prairie voles, the effects of CORT on partner preferences are sexually dimorphic. Acute peripheral administration of CORT increases partner preference in males, but inhibits it in females (DeVries et al., 1995, 1996). Central administration of corticotrophin releasing hormone (CRH) furthermore has a dose-dependent effect in male prairie voles: moderate doses (0.1, 1 ng) facilitate the formation of partner preferences, but high doses (10, 100 ng) do not (DeVries et al., 2002). In Gouldian finches, females who are forced to pair with an unattractive partner have increased CORT which is accompanied by an increased pairing latency (Griffith et al., 2011). In male zebra finches, short-term fasting (4–10 h) increases CORT and decreases testosterone, and this is accompanied by a decrease in courtship and pairing behaviors (Lynn et al., 2010). Female zebra finches prefer low CORT males to high CORT males, but this difference in CORT was also associated with differences in beak and leg color, which is known to affect female preferences (Roberts et al., 2007). Furthermore, the preference of the high and low CORT males themselves was not taken into consideration. Thus, in birds that form longterm monogamous bonds, CORT or male quality are highly important in female choice, and male behavior is negatively impacted by short-term stressors. Our interest was in studying the effects of a single CORT injection (to mimic an acute stressor) on partner preferences in zebra finches, in contrast to earlier work, which has focused mainly on the effect of chronic or prolonged stressors on preferences. Furthermore, we sought to simultaneously test this in both sexes, to determine if the effects of CORT on partner preferences are sexually differentiated (as in voles) or mutually beneficial in both sexes, as predicted by research on the effects of acute stressors (Breuner et al., 2008). We used zebra finches as a model, since they form long-term monogamous pair bonds, mating appears not to be stressful, and they are highly gregarious, preferring to be near many individuals over just a few (Goodson et al., 2009; Kelly et al., 2011; Zann, 1996). Furthermore, we know that, in this species, pairing buffers the stress response, and that even the presence of familiar conspecifics can attenuate the stress response (RemageHealey et al., 2003). Does the stress response, in turn, negatively or positively impact the motivation to pair? From the research above, one could hypothesize that an acute stressor may increase the motivation to pair, although the one study on fasting in male zebra finches found the opposite effect (Lynn et al., 2010). However, in that study, it is unclear whether 4–10 h of fasting is considered an acute stressor or a more prolonged stressor. To test our hypotheses, we employed a commonly used test of partner preference: the two-choice paradigm (DeVries et al., 2002; Young and Wang, 2004), in which an animal is placed in a center compartment and is given the choice of two types of stimulus animals in the side compartments. The cage that the subject spends the most time nearest to is considered his/her preference. The two-choice paradigm has been used in birds to assess both mate and social group preferences (Adkins-Regan and Leung, 2006; Goodson and Thompson, 2010; Kelly et al., 2011). Untreated adult birds reared in a bi-parental environment show a preference for an opposite-sex bird over a same-sex bird [reviewed in (AdkinsRegan, 2002)]. Furthermore, zebra finches are a highly social
species (Zann, 1996) and when given the choice between 2 and 10 same-sex conspecifics, untreated zebra finches prefer the larger group (Goodson and Thompson, 2010; Kelly et al., 2011). The present study used two separate paradigms to determine the effects of CORT (as an acute stressor) on partner preferences; one in which birds are given the choice between a single opposite sex or single same sex bird and one in which birds are given the choice between an opposite-sex bird and a group of same-sex birds. The latter paradigm is novel and allowed us to detect preferences between two highly appealing options. Furthermore, we believed this paradigm would have a higher chance of demonstrating an effect of CORT on motivation to pair, since preference for an opposite-sex partner over a same-sex partner might be so great that CORT treatments would not increase it further. We had two competing hypotheses. First, if an acute stress response is beneficial for reproduction, then we would expect that males and females treated with CORT would spend more time in proximity to opposite-sex birds in both testing paradigms than would vehicle-treated controls, due to an increased interest in pairing. However, if the mechanisms of zebra finch partner preferences are similar to those in prairie voles, we had an alternative hypothesis, that acute CORT treatment would have a sexually dimorphic effect: increasing pairing motivation in males and decreasing pairing motivation in females. Furthermore, we tested two doses. We expected the lower dose to a stronger effect on partner preference than the higher dose, since lower doses had a greater effect than did higher doses in male prairie voles. 2. Methods 2.1. Subjects Socially reared adult male (n = 8) and female (n = 8) zebra finch subjects were maintained on a 12:12 h light/dark cycle (lights on 06:00) in a temperature and humidity controlled room under conditions ideal for mating (24 °C, 50% humidity). An additional 28 males and 28 females served as stimulus animals and were housed in the same conditions. These animals were used across 1 testing session for the 8 males or 8 females, to control for any potential differences in stimulus animal quality across treatment groups. Seed and water were provided ad libitum and their diet was supplemented with hard-boiled chicken egg and calcium-enriched grain (Simple System Breeder Crumb 5-Day Product, The Bird Care Company) twice per week. Prior to the experiment, subjects were housed in same-sex aviaries (152.4 76.2 198.1 cm) to prevent pair formation. Throughout the 4-week testing period, subjects were housed in same-sex cages (n = 8 per cage; 78.7 55.9 88.9 cm), except during testing. 2.2. Testing apparatus During testing, subjects were singly housed in an observation cage (41.9 26.7 33.0 cm). The observation cage contained one perch running along the center of the cage. The perch had 2 pieces of tape wrapped around it at 11 cm from each end to mark zones proximal to each of the stimulus cages. Stimulus cages of the same size were placed to the right and left of the observation cages and contained food, water and 2 perches (see Fig. 1). In the male vs. female condition, one stimulus cage contained a same-sex bird and the other contained an opposite-sex bird. In the opposite-sex vs. group condition, one stimulus cage contained 4 same-sex birds and the other contained 1 opposite-sex bird. Birds were exposed to both conditions for all doses. Condition order (male vs. female or opposite-sex vs. group) and stimulus sides (right vs. left) were randomized across doses for each bird.
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K.A. LaPlante et al. / General and Comparative Endocrinology 199 (2014) 33–37
1
Choice 1
Experimental Cage
*
Choice 2 0.8
0.6
Saline-Baseline Second Saline
Fig. 1. Two-choice testing apparatus in a study of the effects of acute CORT administration on partner preferences in zebra inches. Dashed lines indicate the location of perches and grey areas indicate the zones proximal to choice cages. In one condition, choice 1 was a single opposite-sex bird and choice 2 was a single same-sex bird. In the second condition, choice 1 was a single opposite-sex bird and choice 2 was a group of 4 same-sex birds. Condition order and side of stimulus presentation were counterbalanced. The proportion of time in each shaded area relative to the total time in shaded areas was computed. CORT = corticosterone.
10 µg CORT
0.4
20 µg CORT 0.2
0 Males
2.3. Injections and observations Birds were injected intra-muscularly with either vehicle (peanut oil) or CORT (low dose: 10 lg; high dose: 20 lg) in a 50 ll volume. The high dose produces has been used in the past to increase levels of circulating CORT to 1000 ng/ml in white-crowned sparrows within 15 min of treatment and has been use in other birds, including zebra finches (Breuner et al., 1998; Gam et al., 2011; Saldanha et al., 2000). We also chose a lower dose (10 lg) to test the effects of a more moderate increase of CORT on partner preferences, since earlier work in prairie voles found a dose-dependent effect on partner preferences (DeVries et al., 2002). All animals received both doses and the control. To obtain baseline data on social preference and familiarize the animals with the testing procedure, all animals received the vehicle first. Dose order (10 lg, 20 lg, and vehicle) was then randomized for the next 3 tests. Each test was separated by 7 treatment-free days. Since all animals received the vehicle dose twice, we were able to test for the possibility that CORT treatments affected subsequent tests. Immediately following each injection, animals were released into the observation cage and allowed 15 min for the treatment to become effective and to habituate to the testing cage. During this time, dividers were in place to prevent visual contact with the stimulus animals. Then, the dividers were removed and the amount of time the bird spent nearest to, and facing, each stimulus cage was recorded for 10 min. After the 10 min observation period, the test bird was moved into the observation cage for the second condition and allowed 15 min for habituation which was followed by a second 10 min observation period following the same observation protocol. 2.4. Statistical analysis The duration of time that the subject spent nearest to the cage containing a single animal of the opposite-sex was converted into a percentage of the total time spent next to either cage (same-sex or group) and arc-sin transformed to achieve normality. We then performed a Treatment (4) Sex (2) mixed factorial ANOVA on these percentages for each paradigm. Post-hoc t-tests were conducted where appropriate. 3. Results 3.1. Same-sex vs. opposite sex All groups, except males at baseline control, exhibited a preference for the opposite-sex partner over the same-sex partner. The overall Wilks’ Lamda indicated no significant effect of Treatment, F(3, 12) = 0.22, p = 0.88, g2 = 0.05, observed power = 0.08, or sex,
Females
Fig. 2. The effects of acute CORT administration on zebra finch partner preferences in a test of sexual partner preference. There was a significant Sex Treatment effect on the proportion of time spent in proximity to the opposite-sex bird vs. the samesex bird. Males treated with 10 lg CORT had a stronger preference for the female than they did when treated with saline at baseline. There were no significant effects of CORT on female partner preferences. Indicates (p < 0.05). Error bars indicate SEM. CORT = corticosterone.
F(1, 14) = 2.39, p = 0.14, g2 = 0.06, observed power = 0.30, on preference for the opposite sex over the same sex. Both sexes, overall, preferred the opposite sex, and dose did not affect this preference when both sexes were considered. However, there was a significant Treatment Sex interaction, F(3, 12) = 3.61, p = 0.046, g2 = 0.47, observed power = 0.64 (see Fig. 2). Post-hoc analyses revealed that, in males, subjects treated with 10 lg of CORT had a significantly higher preference for the female than they did at baseline, t(7) = 2.41, p = 0.047. While males treated with 20 lg of CORT also had a higher preference for the female than they did at baseline, this difference was not statistically significant, t(7) = 2.05, p = 0.08. There were no other significant differences (all p > 0.35). In contrast, in females, CORT treatments did not alter preferences for the male (all p > 0.20). 3.2. Opposite-sex vs. group In this test, both sexes were preferred the group over the opposite-sex bird in the baseline control condition. The Wilks’ Lamda revealed a significant effect of Treatment on preference for the opposite sex compared to the group, F(3, 12) = 4.06, p = 0.03, g2 = 0.50, observed power = 0.70 (see Fig. 3). Overall, subjects receiving the 10 lg of CORT had a significantly stronger preference for the opposite-sex than when they received the baseline saline dose, t(15) = 3.43, p = 0.004, and when they received the second saline dose, t(15) = 3.11, p = 0.007. No other groups differed significantly from each other (all p > 0.21). However, there was no significant effect of Sex, F(1, 14) = 0.84, p = 0.37, g2 = 0.06, observed power = 0.14, nor was there as significant Treatment Sex interaction, F(3, 12) = 1.64, p = 0.23, g2 = 0.29, observed power = 0.32. 4. Discussion We had two competing hypotheses regarding the effects of CORT treatment on sexual partner preferences. The first was that acute CORT treatment would increase opposite-sex preference in zebra finches in a two separate 2-choice paradigms, since an acute stressor may be beneficial to reproduction, and partner preferences are the first step in forming a pair bond, which eventually leads to parenting. In the choice between a same-sex and opposite-sex bird, this increase was only apparent in males, and only at the lower
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1
*
*
0.8
0.6
Saline-Baseline Second Saline 10 µg CORT
0.4
20 µg CORT
0.2
0 Males
Females
Fig. 3. The effects of acute CORT administration on zebra finch partner preferences in a test of sexual partner preference vs. group preference. There was an overall effect of Treatment, such that animals, regardless of sex, had a stronger preference for the opposite-sex individual over the group than they did with either saline treatment. Indicates (p < 0.05). Error bars indicate SEM. CORT = corticosterone.
dose (see Fig. 2), replicating findings in prairie voles (DeVries et al., 1995, 1996, 2002). However, these findings conflict with earlier work in zebra finches, which found that fasting stress decreased courtship and pairing behavior in males, indicating a decrease in the motivation to pair (Lynn et al., 2010). However, the fasting period itself (4 or 10 h) was longer than the CORT injection tested here (which lasts approximately 2.5 h in birds) (Saldanha et al., 2000), and may have had even longer lasting effects. Furthermore, the fasting study used a semi-naturalistic paradigm in which the behaviors of the focal males may have been influenced by female choice. Thus, future work should administer CORT over longer periods of time and test partner preferences in the same manner we have done and/or test birds with a single dose of CORT in a seminaturalistic environment and measure behavior of both sexes. When we presented animals with the choice of two highly appealing options (an opposite-sex partner vs. a same-sex group), both sexes preferred the group at baseline control. This suggests that the natural choice in zebra finches may be more toward gregariousness over pairing opportunities. In earlier work, zebra finches have been given the choice of 2 same-sex birds or 10 same-sex birds (Goodson et al., 2009; Kelly et al., 2011). Thus, our test was unique, but still showed that zebra finches prefer the group over a smaller group or a single opposite-sex individual. Interestingly, the administration of a low dose of CORT increased opposite-sex preferences, effectively shifting the preference toward the opposite-sex partner over the group in both sexes (see Fig. 3). This suggests that CORT may increase pairing motivation far above what is normally seen in this species. In females, the high dose of CORT seemed also increase preferences for the opposite-sex individual over the group, but the Sex Treatment test was not significant. Despite a moderate effect size, power was low in this test. The addition of more animals may have revealed an effect at this dose in females. These short-term findings lead one to question what the downstream, long-term consequences of acute CORT administration might be. For example, does this increased opposite-sex partner preference lead to increased pairing? Does it lead to increased reproductive outcomes? Previous work in other species suggests that acute stress or an increase in CORT can either increase (Schiml and Rissman, 1999) or have no effect on (Correa et al., 2011; Orchinik et al., 1988) reproductive function. In zebra finches, unattractive partners can increase pairing latency, which suggests that reproduction would be similarly delayed (Griffith et al., 2011).
However, this latter study focused on animals that may have been unattractive for a variety of reasons, and this unattractiveness increased CORT in the female paired with them. Future research should test the effects of a single injection of CORT on the latency to pair and produce the first clutch of eggs to determine if an acute stressor impacts reproductive function in this species. Nonetheless, our study provides evidence that a low dose (10 lg) of CORT increases opposite-sex preferences over samesex preferences in male zebra finches only, and does not alter preferences in females. Our study also shows that the natural (baseline) preference is for a same-sex group over an opposite-sex individual, and that the low dose of CORT actually shifts this preference in favor of the opposite-sex partner. These findings further our understanding of the cause and effect relationships between acute stressors and social preferences by extending these findings to the zebra finch, a long-term monogamous species that is also highly gregarious.
Acknowledgment We would like to thank Carrie James for assistance with animal care.
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Contents lists available at ScienceDirect
General and Comparative Endocrinology journal homepage: www.elsevier.com/locate/ygcen
Effects of acute corticosterone treatment on partner preferences in male and female zebra finches (Taeniopygia guttata) Kimberly A. LaPlante, Enida Huremovic, Michelle L. Tomaszycki ⇑ Department of Psychology, Wayne State University, Detroit, MI, USA
a r t i c l e
i n f o
Article history: Received 7 September 2013 Revised 27 January 2014 Accepted 2 February 2014 Available online 11 February 2014 Keywords: Corticosterone Two-choice paradigm Partner preference Social preference Sex difference
a b s t r a c t Stress alters physiology and behavior across species. Most research on the effects of stress on behavior uses chronic stressors, and most are correlational. The effects of acute stressors on physiology and behavior have been mixed. Here, we use zebra finches, a highly gregarious species that forms long-term pair bonds, to test the effects of an acute corticosterone (CORT) on opposite-sex partner preferences over a same-sex individual or a group (the latter is a highly appealing option). We had two competing hypotheses. First, we predicted that acute CORT would alter preferences for the opposite sex bird in both conditions in both sexes. However, since there is a sex difference in the effects of CORT on partner preferences in voles, these effects may be more pronounced in males than in females. To test our hypotheses, we administered 2 doses of CORT (10 lg and 20 lg) or vehicle (control) using a repeated measures design. In the male vs. female test, there was a significant Sex by Treatment interaction, such that in males, 10 lg CORT increased preferences for a female over the male compared to when these same males were treated with saline at baseline. There were no effects of treatment in females. In the opposite-sex vs. group condition, there was an overall effect of Treatment, such that the 10 lg dose increased preference for the opposite-sex individual over both saline treatments, regardless of sex. These findings further our understanding of the effects of an acute stressor on sexual partner preferences. Ó 2014 Elsevier Inc. All rights reserved.
1. Introduction Stress causes a physiological response that can have diverse effects on behavior and fitness (McEwen, 2006; Sapolsky et al., 2000). The effects of chronic stressors, such as environmental challenges, have been the most frequently studied (Breuner et al., 2008; Romero et al., 1998). Under chronic stress conditions, animals may restrict reproduction in favor of other behaviors that promote immediate survival (Astheimer et al., 1995). Most of these studies have focused on birds, and many of these studies focus on seasonal breeders. For example, in female starlings, chronic stressors decrease corticosterone (CORT) and also decrease survivorship of fledglings (Cyr and Michael Romero, 2007). In zebra finches, early life stress leads not only to decreased survivorship in adulthood, but also leads to decreased survivorship of the partner (Monaghan et al., 2012). Thus, it is clear that chronic stressors affect reproductive fitness. Fewer studies have focused on the role of acute stressors in behavior and fitness. Some have argued that response to acute ⇑ Corresponding author. Address: Department of Psychology, Wayne State University, Detroit, MI 48202, United States. Fax: +1 (313) 577 7636. E-mail address: [email protected] (M.L. Tomaszycki). http://dx.doi.org/10.1016/j.ygcen.2014.02.004 0016-6480/Ó 2014 Elsevier Inc. All rights reserved.
stressor may, in contrast to chronic stressors, be beneficial (Breuner et al., 2008). Indeed, short-term increases in CORT are either associated with an increase in sexual behavior (in musk shrews) or have no effect on reproduction (in marine toads) (Orchinik et al., 1988; Schiml and Rissman, 1999). In female Japanese quail, CORT increases in response to mating with a male, but is not altered if the female simply sees and hears a male (Rutkowska et al., 2011). This increase in CORT is transient (apparent at 5 min, but not at 3 h), and does not predict fertilization (Correa et al., 2011). Thus, acute stressors may or may not impact reproductive behavior. Even fewer studies have used CORT manipulations to mimic the stress response and test the effects on behavior. This is important for inferring cause and effect relationships between glucocorticoids and behavior. Prolonged CORT administration has no effect on courtship behaviors in side-blotched lizards (Denardo and Licht, 1993). In mountain chickadees, CORT administered directly before recovery of a food cache increases food recovery (Saldanha et al., 2000). However, acute CORT had no effect on aggression in male tree sparrows (Astheimer et al., 2000), but does increase locomotion during an intruder test in rainbow trout (Øverli et al., 2002). Thus, the effects of acute CORT administration have been mixed, and deserve further investigation.
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The present study focuses on the role of CORT in partner preferences. Most studies in birds have focused on mating, and most of these studies have used seasonal breeders (Breuner et al., 2008), which form only short-term (seasonal) relationships, or animals for which mating is stressful and is not associated with a partner preference, such as the female Japanese quail (Correa et al., 2011; Rutkowska et al., 2011). Evidence from a couple of species suggests that stress affects partner preferences. For example, exposure to an acute stressor increases attraction for females in male humans (Dutton and Aron, 1974). In prairie voles, the effects of CORT on partner preferences are sexually dimorphic. Acute peripheral administration of CORT increases partner preference in males, but inhibits it in females (DeVries et al., 1995, 1996). Central administration of corticotrophin releasing hormone (CRH) furthermore has a dose-dependent effect in male prairie voles: moderate doses (0.1, 1 ng) facilitate the formation of partner preferences, but high doses (10, 100 ng) do not (DeVries et al., 2002). In Gouldian finches, females who are forced to pair with an unattractive partner have increased CORT which is accompanied by an increased pairing latency (Griffith et al., 2011). In male zebra finches, short-term fasting (4–10 h) increases CORT and decreases testosterone, and this is accompanied by a decrease in courtship and pairing behaviors (Lynn et al., 2010). Female zebra finches prefer low CORT males to high CORT males, but this difference in CORT was also associated with differences in beak and leg color, which is known to affect female preferences (Roberts et al., 2007). Furthermore, the preference of the high and low CORT males themselves was not taken into consideration. Thus, in birds that form longterm monogamous bonds, CORT or male quality are highly important in female choice, and male behavior is negatively impacted by short-term stressors. Our interest was in studying the effects of a single CORT injection (to mimic an acute stressor) on partner preferences in zebra finches, in contrast to earlier work, which has focused mainly on the effect of chronic or prolonged stressors on preferences. Furthermore, we sought to simultaneously test this in both sexes, to determine if the effects of CORT on partner preferences are sexually differentiated (as in voles) or mutually beneficial in both sexes, as predicted by research on the effects of acute stressors (Breuner et al., 2008). We used zebra finches as a model, since they form long-term monogamous pair bonds, mating appears not to be stressful, and they are highly gregarious, preferring to be near many individuals over just a few (Goodson et al., 2009; Kelly et al., 2011; Zann, 1996). Furthermore, we know that, in this species, pairing buffers the stress response, and that even the presence of familiar conspecifics can attenuate the stress response (RemageHealey et al., 2003). Does the stress response, in turn, negatively or positively impact the motivation to pair? From the research above, one could hypothesize that an acute stressor may increase the motivation to pair, although the one study on fasting in male zebra finches found the opposite effect (Lynn et al., 2010). However, in that study, it is unclear whether 4–10 h of fasting is considered an acute stressor or a more prolonged stressor. To test our hypotheses, we employed a commonly used test of partner preference: the two-choice paradigm (DeVries et al., 2002; Young and Wang, 2004), in which an animal is placed in a center compartment and is given the choice of two types of stimulus animals in the side compartments. The cage that the subject spends the most time nearest to is considered his/her preference. The two-choice paradigm has been used in birds to assess both mate and social group preferences (Adkins-Regan and Leung, 2006; Goodson and Thompson, 2010; Kelly et al., 2011). Untreated adult birds reared in a bi-parental environment show a preference for an opposite-sex bird over a same-sex bird [reviewed in (AdkinsRegan, 2002)]. Furthermore, zebra finches are a highly social
species (Zann, 1996) and when given the choice between 2 and 10 same-sex conspecifics, untreated zebra finches prefer the larger group (Goodson and Thompson, 2010; Kelly et al., 2011). The present study used two separate paradigms to determine the effects of CORT (as an acute stressor) on partner preferences; one in which birds are given the choice between a single opposite sex or single same sex bird and one in which birds are given the choice between an opposite-sex bird and a group of same-sex birds. The latter paradigm is novel and allowed us to detect preferences between two highly appealing options. Furthermore, we believed this paradigm would have a higher chance of demonstrating an effect of CORT on motivation to pair, since preference for an opposite-sex partner over a same-sex partner might be so great that CORT treatments would not increase it further. We had two competing hypotheses. First, if an acute stress response is beneficial for reproduction, then we would expect that males and females treated with CORT would spend more time in proximity to opposite-sex birds in both testing paradigms than would vehicle-treated controls, due to an increased interest in pairing. However, if the mechanisms of zebra finch partner preferences are similar to those in prairie voles, we had an alternative hypothesis, that acute CORT treatment would have a sexually dimorphic effect: increasing pairing motivation in males and decreasing pairing motivation in females. Furthermore, we tested two doses. We expected the lower dose to a stronger effect on partner preference than the higher dose, since lower doses had a greater effect than did higher doses in male prairie voles. 2. Methods 2.1. Subjects Socially reared adult male (n = 8) and female (n = 8) zebra finch subjects were maintained on a 12:12 h light/dark cycle (lights on 06:00) in a temperature and humidity controlled room under conditions ideal for mating (24 °C, 50% humidity). An additional 28 males and 28 females served as stimulus animals and were housed in the same conditions. These animals were used across 1 testing session for the 8 males or 8 females, to control for any potential differences in stimulus animal quality across treatment groups. Seed and water were provided ad libitum and their diet was supplemented with hard-boiled chicken egg and calcium-enriched grain (Simple System Breeder Crumb 5-Day Product, The Bird Care Company) twice per week. Prior to the experiment, subjects were housed in same-sex aviaries (152.4 76.2 198.1 cm) to prevent pair formation. Throughout the 4-week testing period, subjects were housed in same-sex cages (n = 8 per cage; 78.7 55.9 88.9 cm), except during testing. 2.2. Testing apparatus During testing, subjects were singly housed in an observation cage (41.9 26.7 33.0 cm). The observation cage contained one perch running along the center of the cage. The perch had 2 pieces of tape wrapped around it at 11 cm from each end to mark zones proximal to each of the stimulus cages. Stimulus cages of the same size were placed to the right and left of the observation cages and contained food, water and 2 perches (see Fig. 1). In the male vs. female condition, one stimulus cage contained a same-sex bird and the other contained an opposite-sex bird. In the opposite-sex vs. group condition, one stimulus cage contained 4 same-sex birds and the other contained 1 opposite-sex bird. Birds were exposed to both conditions for all doses. Condition order (male vs. female or opposite-sex vs. group) and stimulus sides (right vs. left) were randomized across doses for each bird.
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1
Choice 1
Experimental Cage
*
Choice 2 0.8
0.6
Saline-Baseline Second Saline
Fig. 1. Two-choice testing apparatus in a study of the effects of acute CORT administration on partner preferences in zebra inches. Dashed lines indicate the location of perches and grey areas indicate the zones proximal to choice cages. In one condition, choice 1 was a single opposite-sex bird and choice 2 was a single same-sex bird. In the second condition, choice 1 was a single opposite-sex bird and choice 2 was a group of 4 same-sex birds. Condition order and side of stimulus presentation were counterbalanced. The proportion of time in each shaded area relative to the total time in shaded areas was computed. CORT = corticosterone.
10 µg CORT
0.4
20 µg CORT 0.2
0 Males
2.3. Injections and observations Birds were injected intra-muscularly with either vehicle (peanut oil) or CORT (low dose: 10 lg; high dose: 20 lg) in a 50 ll volume. The high dose produces has been used in the past to increase levels of circulating CORT to 1000 ng/ml in white-crowned sparrows within 15 min of treatment and has been use in other birds, including zebra finches (Breuner et al., 1998; Gam et al., 2011; Saldanha et al., 2000). We also chose a lower dose (10 lg) to test the effects of a more moderate increase of CORT on partner preferences, since earlier work in prairie voles found a dose-dependent effect on partner preferences (DeVries et al., 2002). All animals received both doses and the control. To obtain baseline data on social preference and familiarize the animals with the testing procedure, all animals received the vehicle first. Dose order (10 lg, 20 lg, and vehicle) was then randomized for the next 3 tests. Each test was separated by 7 treatment-free days. Since all animals received the vehicle dose twice, we were able to test for the possibility that CORT treatments affected subsequent tests. Immediately following each injection, animals were released into the observation cage and allowed 15 min for the treatment to become effective and to habituate to the testing cage. During this time, dividers were in place to prevent visual contact with the stimulus animals. Then, the dividers were removed and the amount of time the bird spent nearest to, and facing, each stimulus cage was recorded for 10 min. After the 10 min observation period, the test bird was moved into the observation cage for the second condition and allowed 15 min for habituation which was followed by a second 10 min observation period following the same observation protocol. 2.4. Statistical analysis The duration of time that the subject spent nearest to the cage containing a single animal of the opposite-sex was converted into a percentage of the total time spent next to either cage (same-sex or group) and arc-sin transformed to achieve normality. We then performed a Treatment (4) Sex (2) mixed factorial ANOVA on these percentages for each paradigm. Post-hoc t-tests were conducted where appropriate. 3. Results 3.1. Same-sex vs. opposite sex All groups, except males at baseline control, exhibited a preference for the opposite-sex partner over the same-sex partner. The overall Wilks’ Lamda indicated no significant effect of Treatment, F(3, 12) = 0.22, p = 0.88, g2 = 0.05, observed power = 0.08, or sex,
Females
Fig. 2. The effects of acute CORT administration on zebra finch partner preferences in a test of sexual partner preference. There was a significant Sex Treatment effect on the proportion of time spent in proximity to the opposite-sex bird vs. the samesex bird. Males treated with 10 lg CORT had a stronger preference for the female than they did when treated with saline at baseline. There were no significant effects of CORT on female partner preferences. Indicates (p < 0.05). Error bars indicate SEM. CORT = corticosterone.
F(1, 14) = 2.39, p = 0.14, g2 = 0.06, observed power = 0.30, on preference for the opposite sex over the same sex. Both sexes, overall, preferred the opposite sex, and dose did not affect this preference when both sexes were considered. However, there was a significant Treatment Sex interaction, F(3, 12) = 3.61, p = 0.046, g2 = 0.47, observed power = 0.64 (see Fig. 2). Post-hoc analyses revealed that, in males, subjects treated with 10 lg of CORT had a significantly higher preference for the female than they did at baseline, t(7) = 2.41, p = 0.047. While males treated with 20 lg of CORT also had a higher preference for the female than they did at baseline, this difference was not statistically significant, t(7) = 2.05, p = 0.08. There were no other significant differences (all p > 0.35). In contrast, in females, CORT treatments did not alter preferences for the male (all p > 0.20). 3.2. Opposite-sex vs. group In this test, both sexes were preferred the group over the opposite-sex bird in the baseline control condition. The Wilks’ Lamda revealed a significant effect of Treatment on preference for the opposite sex compared to the group, F(3, 12) = 4.06, p = 0.03, g2 = 0.50, observed power = 0.70 (see Fig. 3). Overall, subjects receiving the 10 lg of CORT had a significantly stronger preference for the opposite-sex than when they received the baseline saline dose, t(15) = 3.43, p = 0.004, and when they received the second saline dose, t(15) = 3.11, p = 0.007. No other groups differed significantly from each other (all p > 0.21). However, there was no significant effect of Sex, F(1, 14) = 0.84, p = 0.37, g2 = 0.06, observed power = 0.14, nor was there as significant Treatment Sex interaction, F(3, 12) = 1.64, p = 0.23, g2 = 0.29, observed power = 0.32. 4. Discussion We had two competing hypotheses regarding the effects of CORT treatment on sexual partner preferences. The first was that acute CORT treatment would increase opposite-sex preference in zebra finches in a two separate 2-choice paradigms, since an acute stressor may be beneficial to reproduction, and partner preferences are the first step in forming a pair bond, which eventually leads to parenting. In the choice between a same-sex and opposite-sex bird, this increase was only apparent in males, and only at the lower
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1
*
*
0.8
0.6
Saline-Baseline Second Saline 10 µg CORT
0.4
20 µg CORT
0.2
0 Males
Females
Fig. 3. The effects of acute CORT administration on zebra finch partner preferences in a test of sexual partner preference vs. group preference. There was an overall effect of Treatment, such that animals, regardless of sex, had a stronger preference for the opposite-sex individual over the group than they did with either saline treatment. Indicates (p < 0.05). Error bars indicate SEM. CORT = corticosterone.
dose (see Fig. 2), replicating findings in prairie voles (DeVries et al., 1995, 1996, 2002). However, these findings conflict with earlier work in zebra finches, which found that fasting stress decreased courtship and pairing behavior in males, indicating a decrease in the motivation to pair (Lynn et al., 2010). However, the fasting period itself (4 or 10 h) was longer than the CORT injection tested here (which lasts approximately 2.5 h in birds) (Saldanha et al., 2000), and may have had even longer lasting effects. Furthermore, the fasting study used a semi-naturalistic paradigm in which the behaviors of the focal males may have been influenced by female choice. Thus, future work should administer CORT over longer periods of time and test partner preferences in the same manner we have done and/or test birds with a single dose of CORT in a seminaturalistic environment and measure behavior of both sexes. When we presented animals with the choice of two highly appealing options (an opposite-sex partner vs. a same-sex group), both sexes preferred the group at baseline control. This suggests that the natural choice in zebra finches may be more toward gregariousness over pairing opportunities. In earlier work, zebra finches have been given the choice of 2 same-sex birds or 10 same-sex birds (Goodson et al., 2009; Kelly et al., 2011). Thus, our test was unique, but still showed that zebra finches prefer the group over a smaller group or a single opposite-sex individual. Interestingly, the administration of a low dose of CORT increased opposite-sex preferences, effectively shifting the preference toward the opposite-sex partner over the group in both sexes (see Fig. 3). This suggests that CORT may increase pairing motivation far above what is normally seen in this species. In females, the high dose of CORT seemed also increase preferences for the opposite-sex individual over the group, but the Sex Treatment test was not significant. Despite a moderate effect size, power was low in this test. The addition of more animals may have revealed an effect at this dose in females. These short-term findings lead one to question what the downstream, long-term consequences of acute CORT administration might be. For example, does this increased opposite-sex partner preference lead to increased pairing? Does it lead to increased reproductive outcomes? Previous work in other species suggests that acute stress or an increase in CORT can either increase (Schiml and Rissman, 1999) or have no effect on (Correa et al., 2011; Orchinik et al., 1988) reproductive function. In zebra finches, unattractive partners can increase pairing latency, which suggests that reproduction would be similarly delayed (Griffith et al., 2011).
However, this latter study focused on animals that may have been unattractive for a variety of reasons, and this unattractiveness increased CORT in the female paired with them. Future research should test the effects of a single injection of CORT on the latency to pair and produce the first clutch of eggs to determine if an acute stressor impacts reproductive function in this species. Nonetheless, our study provides evidence that a low dose (10 lg) of CORT increases opposite-sex preferences over samesex preferences in male zebra finches only, and does not alter preferences in females. Our study also shows that the natural (baseline) preference is for a same-sex group over an opposite-sex individual, and that the low dose of CORT actually shifts this preference in favor of the opposite-sex partner. These findings further our understanding of the cause and effect relationships between acute stressors and social preferences by extending these findings to the zebra finch, a long-term monogamous species that is also highly gregarious.
Acknowledgment We would like to thank Carrie James for assistance with animal care.
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