Skip to main content
NCBI home page
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2022 Jul 1.
Published in final edited form as: J Exp Zool A Ecol Integr Physiol. 2021 Jul;335(6):10.1002/jez.2499. doi: 10.1002/jez.2499

The Ontogeny of Personality: Repeatability of Social and Escape Behaviors Across Developmental Stages in Siberian Hamsters (Phodopus sungorus)

Catherine H Adaniya 1, Cara L Wellman 2,3,4, Gregory E Demas 1,2,4, Jessica A Cusick 1,2
PMCID: PMC8315155  NIHMSID: NIHMS1717054  PMID: 34184832

Abstract

Animal personality is defined as behavioral tendencies that are consistent across time and contexts within an individual, but differ across individuals. Studies investigating personality typically examine individuals across short time periods or within a single life stage. There is growing evidence that personality may be less stable across life stages, highlighting the need to consider the effects of ontogeny on the expression of consistent behavioral traits. We investigated individual consistency in social and escape behaviors across developmental stages using Siberian hamsters (Phodopus sungorus). To determine whether individuals were consistent in these behaviors as juveniles and across developmental stages, we measured male and female social and escape behaviors twice as juveniles and once as an adult. Individuals’ social scores were significantly repeatable within the juvenile stage, but not across developmental stages. In contrast, escape scores were highly repeatable across developmental stages with males’ scores being more repeatable than females’ scores. Our results support previous findings that personality traits, especially those associated with social behavior, are less stable across development, whereas behaviors associated with stress or coping may represent a more permanent feature of an individual’s phenotype. Our results also indicate potential sex differences in long-term repeatability of personality. Considering how ontogeny affects animal personality for males and females can provide insight into the evolution and mechanism that maintain animal personality.

Keywords: animal personality, aggression, investigation, escape, avoidance, behavioral consistency

Graphical Abstract

graphic file with name nihms-1717054-f0001.jpg

INTRODUCTION

Animal personality refers to behavioral tendencies that remain consistent across time and context within individuals, but differ across individuals (Réale et al., 2007; Cabrera et al., 2021). Animal personality has been documented across taxa, including mammals (e.g., Koolhaas et al., 1999; Reale et al., 2000), birds (e.g., Groothuis & Carere, 2005; Jacobs et al., 2014), amphibians (e.g., Hedrick & Kortet, 2011; Kelleher et al., 2018), and fish (e.g., Bell & Sih, 2007; Le Vin et al., 2011). Recently, research on animal personality has shifted from documenting its occurrence to understanding its ecological and evolutionary implications (Cabrera et al., 2021). New questions about the underlying mechanisms associated with personality, its adaptive benefits, and evolution (Rodel & Meyer, 2011) provide a more holistic approach (Tinbergen, 1963) to the study of animal personality. However, less attention has been given to ontogeny (Tinbergen, 1963), including sex differences, despite the importance of development in animal behavior (Guenther et al., 2014; Cabrera et al., 2021).

Personality is often examined across short time periods or within a single life stage (e.g., adulthood, Stamps & Groothuis, 2010), however there is growing evidence that personality may be less stable across life stages (Cabrera et al., 2021). Inconsistencies in behavioral traits after maturation have been observed across taxa, including in red junglefowl, (Gallus gallus Favati et al., 2016), North American red squirrels (Tamiasciurus hudsonicus Kelley et al., 2015), and great tits (Parus major Carere et al., 2005). Development is associated with morphological, physiological, and behavioral changes. For example, reaching sexual maturity (i.e., “pubertal transition” Cabrera et al., 2021) is associated with changes in physiological processes (e.g., hormones, Stamps & Groothuis, 2010), body mass, parental care and social affiliations, and new or unpredictable environments (Rodel & Meyer, 2011; Cabrera et al., 2021), which can influence the emergence or stability of personality. In eastern mosquitofish (Gambusia holbrooki) personality differences were not observed during early stages of life, but emerged later on in development (Polverino et al., 2016), and in wild guinea pigs (Cavia aperea), associations between behaviors and physiological traits disappeared after maturation (Guenther et al., 2014). Although some studies have observed behavioral consistency across ontogeny in some traits (e.g., boldness in female cichlids, Neolamprologus pulcher, Schürch & Heg, 2010; docility in yellow-bellied marmots Marmota flaviventris, Petelle et al., 2013), few studies have investigated personality across ontogeny and of those studies, even fewer have identified consistent trends in behavioral traits across development (Cabrera et al., 2021).

Whether certain personality traits are repeatable across ontogeny could depend on the mechanisms and environmental conditions that mediate those behaviors or could reflect different selective pressures on phenotypic variance (Bell et al., 2009). Behaviors like aggression or sociality, which may be influenced by morphological or physiological mechanisms influenced by ontogenetic changes, may be more repeatable within a life stage (i.e., adulthood) and not across life stages (Bell et al., 2009). For example, in red squirrels, individual aggressiveness was not consistent across ontogeny (Kelley et al., 2015). In zebra finches (Taeniopygia guttata), only female aggressiveness was repeatable (Wuerz & Kruger, 2015) while fearlessness was strongly repeatable across all life stages (Wuerz & Kruger, 2015). Differences in repeatability may even be species-specific. In some species boldness and activity tended to be consistent within, but not across life stages (Cabrera et al., 2021; Herde & Eccard, 2013), whereas in other species, activity level (Kanda et al., 2012; Schuster et al., 2017) and boldness (Schuster et al., 2017), were more consistent across development. Additional studies investigating the ontogeny of personality are necessary to identify if certain behavioral traits are more susceptible to developmental changes and to understand the evolution and maintenance of personality (Cabrera et al., 2021; Reale et al., 2000).

We investigated individual consistency in social and escape behaviors across ontogeny using Siberian hamsters (Phodopus sungorus), which is an ideal, non-model system in which to test individual consistency in behavioral traits across time. Social and escape behaviors have been well documented in our lab population in both juveniles (Cusick et al. in review) and adults (Cusick et al. in prep; Munley et al., 2021; Sylvia et al., 2017; Scotti et al., 2008), and are comparable to behaviors in wild populations (Ross, 1998). Social (e.g., aggressiveness, investigation) and escape behaviors are commonly measured traits in animal personality (e.g., Cabrera et al., 2021). To determine whether these behaviors were consistent across development, we measured individuals’ social and escape behaviors twice as juveniles and then once after they reached adulthood (approximately 40 days later). Our main objectives were to (1) identify individual characteristics associated with differences in social and escape behavior and (2) determine whether individuals were consistent in their social and escape behavior within the juvenile stage (i.e., prior to the pubertal transition) and across developmental stages (i.e., from juvenile to adulthood).

METHODS

Animal Housing

Individuals were housed in same-sex pairs in polypropylene cages (28×17×12cm) in a 16:8 light:dark photoperiod (light on at 1:00am EST), with an ambient temperature of 22 ± 2°C and a relative humidity of 55 ± 5%. To identify each individual within a cage, a small patch of fur was shaved on either the right or left side of the hamster. Hamsters had ad libitum access to laboratory rodent chow (Envigo Teklad Global Diets 18% Rodent Diet) and water. All procedures adhered to the National Institutes of Health Guide for the Care and Use of Laboratory Animals and were approved by the Bloomington Institution Animal Care and Use Committee (BIACUC) at Indiana University.

Behavioral Trials

Social behavior of both males and females was assessed using a 15-minute resident-intruder trial. For each individual (n = 8 females, n=11 males), we conducted two “juvenile trials” when the focal individuals were 51–56 days old; juvenile trials were separated by one to three days. The third trial occurred after the pubertal transition had begun when individuals were 98–101 days old (pubertal transition begins at approximately 60 days old; n=7 females, n=8 males).

Trials occurred within the first three hours of the dark-light period under low, red-light illumination and were video recorded. Staged interactions consisted of the “intruder,” which was the focal animal in this study and the “resident” individual (non-focal individual). For each trial, the focal animal was placed into the resident’s cage for 15 minutes, then returned to its home cage. Resident-intruder pairs were matched by sex, weight (± 3 grams), age, and had different parental lines. The residents’ cages were not changed for at least three days prior to the trials and individuals were weighed the day before the trial.

Video Scoring and Behavioral Analyses

Behaviors from video recordings were scored using BORIS v 7.9.6 (Friard & Gamba, 2016) by one unbiased observer (C.H.A.). Duration of behaviors performed by the focal individual during the first five minutes of the trial were scored, following standard procedure in our lab. Behaviors scored included aggression, investigation, run, jump, and received aggression (defined in Table S1).

For each trial, we calculated the focal individual’s “social score” and “escape score.” An individual’s social score was defined as the total amount of time the focal individual interacted with the resident (e.g., attacked or investigated). An individual’s escape score was defined as the total amount of time the focal individual spent evading the resident (e.g., ran away or jumping at cage wall).

Statistical Analyses

All statistical analyses were conducted in R v. 4.0.2 (R Core Team, 2020). We report mean±standard error of the mean unless stated otherwise.

Juvenile social scores (Shapiro-Wilk W=0.79, p<0.05) and escape scores (Shapiro-Wilk W=0.88, p=0.02) during trial one were not normally distributed. We performed a square-root transformation (social score Shapiro-Wilk W=0.95, p=0.43, escape score Shapiro-Wilk W=0.94, p =0.23) and conducted separate generalized linear models (GLM, Gaussian, identity link) to test for an effect of sex, juvenile weight, and these terms’ interaction on social and escape scores during juvenile trial one.

We conducted separate GLMs (Gaussian, identity link) to determine whether an individual’s sex, weight, these two terms’ interaction, or their received aggression score from juvenile trial 1 affected juvenile social scores and escape scores during the second juvenile trial. Juvenile trial two escape scores were not normally distributed (Shapiro-Wilk W=0.73, p<0.01) and were log transformed (Shapiro-Wilk W=0.95, p=0.46) prior to analyses.

We assessed whether the interaction of sex and weight affected adult social and escape scores during the adult trials using a GLM (Gaussian, identity link). Adult escape scores were not normally distributed (Shapiro-Wilk W=0.88, p=0.05) and we performed a square-root transformation (W=0.96,p=0.63) prior to analyses.

We assessed repeatability (“R”) of social and escape scores using the lmm method in the “rpt” function for normal distributions in rptR package (Stoffel et al., 2017; Nakagawa & Schielzeth, 2010). Repeatability values range from 0–1 with values ranging from 0.5–0.7 indicating moderate repeatability and values greater than 0.7 indicating high repeatability (Harper, 1994; Koo & Li, 2016). When data did not follow normal distributions, as described previously, we transformed the data before analysis (Nakagawa & Schielzeth, 2010). To assess the significance of repeatability estimates we calculated 95% confidence intervals using 1000 parametric bootstrapping iterations (Nakagawa & Cuthill, 2007). We also calculated the “VarW/VarA ratio,” which represents the ratio of within and among variances, using the ICCest function in the ICC package (Wolak et al., 2012). Lower ratios are associated with higher repeatability (Réale et al., 2007). We assessed the repeatability of individuals’ social scores and escape scores across the two juvenile trials and the repeatability of individuals’ social and escape scores across juvenile trial one and the adult trial. To determine whether one sex displayed greater repeatability, we repeated these analyses separately for each sex.

RESULTS

Social and Escape Score

Juveniles’ average social scores during trial one (males = 24.26 ± 7.72s, females = 16.31 ± 4.27s) and trial two (males = 20.50 ± 5.89s, females = 23.67 ± 4.65s) were unrelated to sex, weight, or their interaction (Table 1a,b). As adults, we observed a non-significant interactive effect of sex and weight (Table 1c); as males’ weight increased their social scores (21.23 ± 5.24s) tended to decrease whereas females’ social scores (11.65 ± 1.78s) increased with increasing weight.

Table 1.

Effects of sex and weight on social and escape scores across juvenile and adult trials.

Trial Behavioral Score Terms Estimate ± S.E. t value p value
(a) Juvenile Trial 1 Social Score Sex Male vs. Female 12.26±13.50 0.91 0.38
Weight 0.49±0.35 1.42 0.18
Sex*Weight −0.41±0.43 −0.94 0.36
Escape Score Sex Male vs. Female 9.19±13.50 0.68 0.51
Weight 0.15±0.35 0.42 0.68
Sex*Weight −0.26±0.43 −0.60 0.56
(b) Juvenile Trial 2 Social Score Sex Male vs. Female 96.38±116.48 0.83 0.42
Weight 3.75±2.89 1.29 0.22
Received Aggression Trial 1 −0.37±1.29 −0.29 0.78
Sex*Weight −3.45±3.69 −0.94 0.37
Escape Score Sex Male vs. Female 9.40±5.26 1.79 0.10
Weight 0.13±0.13 1.01 0.33
Received Aggression Trial 1 0.01±0.06 0.24 0.82
Sex*Weight −0.29±0.17 −1.73 0.11
(c) Adult Trial Social Score Sex Male vs. Female 119.66±57.17 2.09 0.06
Weight 0.40±1.06 0.37 0.72
Sex*Weight −2.94±1.57 −1.87 0.08
Escape Score Sex Male vs. Female −3.12±16.10 −0.19 0.85
Weight 0.16±0.30 0.53 0.61
Sex*Weight 0.04±0.44 0.09 0.93
Open in a new tab

Results of GLMs (Gaussian, identity link) investigating the effects of sex, weight, their interaction, and received aggression trial 1 (for Juvenile trail 2 only) on male and female social and escape scores. The same 19 individuals were assessed during Juvenile Trial 1 and Juvenile Trial 2. Of the 19 individuals assessed as juveniles, 15 individuals were assessed a third time as an adult. Terms in italics indicate non-significant terms (0.05<p<0.1) trending towards significance.

We found no effect of sex, weight, or their interaction on juveniles’ escape scores during trial 1 (males = 50.69 ± 10.09s, females = 34.93 ± 6.98, Table 1a), trial two (males = 49.37 ± 15.85s, females = 29.97 ± 5.04s, Table 1b), or during the adult trial (males = 46.03 ± 16.46s, females = 47.72 ± 5.30s, Table 1c).

Repeatability of Social and Escape Scores

Individuals’ social scores were significantly repeatable across the two juvenile trials (R=0.55, SE=0.17, 95%CI=0.14,0.80,p<0.01, VarW/VarA=0.82, Figure 1a). Juvenile males’ social scores were highly repeatable across juvenile trials (R=0.64, SE=0.20, 95%CI=0.11,0.88, p=0.01, N=11) and juvenile females’ social scores were moderately repeatable across trials (R=0.40, SE=0.27, 95%CI=0,0.81, p=0.16, N=8). Escape scores were not highly repeatable across the two juvenile trials (R=0.35, SE=0.19, 95%CI=0,0.69,p=0.07, VarW/VarA=1.8; Figure 1b). Juvenile females tended to exhibit slightly higher levels of repeatability in their escape scores (R=0.54, SE=0.24, 95%CI=0,0.86, p=0.07, N=8) compared to juvenile males (R=0.34, SE=0.23, 95%CI=0,0.75, p=0.15, N=11).

Figure 1.

Figure 1.

Open in a new tab

Individual repeatability of (a) social scores and (b) escape scores across juvenile trials (n=19), and (c) social scores and (d) escape scores across developmental stages (n=15).Trial type is listed on the x-axis: “J1” indicates juvenile trial one, “J2” indicates juvenile trial two, and “Adult” indicates adult trial. Individuals’ social scores were significantly repeatable across the two juvenile trials and individuals’ escape scores were significantly repeatable across developmental stages. Dots represents individual scores and solid lines connect the scores of a single individual across trials.

Social scores of both females (R=0.29, SE=0.26, 95%CI=0,0.80,p=0.28, N=7) and males (R=0.21, SE=0.24, 95%CI=0,0.76, p=0.35, N=8) were not repeatable across developmental stages (R=0.23, SE=0.20, 95%CI=0,0.62, p=0.23, VarW/VarA =3.4; Figure 1c). In contrast, escape scores were highly repeatable across development (R=0.62, SE=0.17, 95%CI=0.18,0.85, p<0.01, VarW/VarA =0.42; Figure 1d), which was driven by the greater repeatability in males (R=0.70, SE=0.21, 95%CI=0.03,0.93, p=0.02, N=8 individuals) compared to females (R=0.25, SE=0.25, 95%CI=0,0.78, p=0.32, N=7 individuals).

Discussion

There is growing evidence that personality may be less stable across life stages, highlighting the need to consider how ontogeny affects animal personality (Cabrera et al., 2021). We measured individual hamsters’ social and escape behaviors as juveniles and as adults. Individuals’ social scores were repeatable within the juvenile stage, but not across developmental stages. Individuals’ escape scores were repeatable across developmental stages, despite not being repeatable as juveniles

Social Scores

Reaching sexual maturity, especially in direct-developing species, is associated with a variety of physiological, social, and environmental changes that may influence the stability of certain behavioral traits, while not affecting others (Cabrera et al., 2021). In the current study, individuals’ social scores, which were comprised of aggressive and investigatory behavior, were not consistent across development in both males and females. Few studies have documented consistency in such behaviors across developmental stages. A recent review by Cabrera et al. (2021) revealed that none of the studies they evaluated detected consistency in sociality, found aggression to be consistent across development in only two out of the 10 studies investigating this phenomenon, and found consistency in exploration across life stages in only one of 14 studies. In our study, juveniles’ social scores consisted of investigation (mean±SD=19.56±18.52s) more than aggression (mean±SD=1.35±3.18s), while adults’ social scores consisted of an increase in aggression (mean±SD=7.23±11.36s) and a decrease in investigation (mean±SD=9.03±5.94s). This suggests that Siberian hamsters become more aggressive and less investigatory with age, similar to other species. For example, investigation can decrease with age (e.g., Miller et al., 2015) as exploration may be more beneficial to juveniles than adults (Sih & Del Giudice, 2012). Further, in the study species, aggression appears to be under gonadal regulation during long-day photoperiods (Munley et al., 2018), which is the condition under which this study occurred. As individual mature, changes in gonad morphology and function as well as gonadal steroid secretion may influence individual’s aggressive behavior and explain why social scores were not consistent across developmental stages. Both aggressive and investigatory behaviors may be susceptible to hormonal, social, and environmental changes associated with maturation (e.g., Kelley et al., 2015; Miller et al., 2015), therefore social behavior, as seen in this study, may be subject to behavioral reconstruction across development.

Escape Scores

Escape scores were highly repeatable across maturation. Escape scores were comprised of run and jump behaviors, which are associated with avoiding and escaping from an unfamiliar conspecific. In other studies, behavioral traits similar to escape behavior are repeatable across developmental stages. In Eurasian harvest mice (Micromys minutus) individual activity (i.e., similar to escape behavior measured in the current study) was consistent across maturation (Schuster et al., 2017). In a different population of Siberian hamsters, open field activity, a measure similar to jump behavior assessed in the current study, was highly correlated across juvenile and adult trials (Kanda et al., 2012).

Escape score repeatability across maturation was primarily driven by the high repeatability scores of males. Although sex differences in repeatability are not always reported, higher repeatability for certain behavioral traits in males has been reported (e.g., response to threat: Amy et al., 2017; aggression: Schürch & Heg, 2010). Behavioral traits associated with fearlessness, anxiety, stress, and coping mechanisms are often highly repeatable. Individuals’ coping styles and escape attempts were consistent across time in the Senegalese sole (Solea senegalensis, Ibarra-Zatarain et al., 2020) and in wild guinea pigs (Cavia aperea), fearlessness was consistent across two distinct ontogenetic stages (Guenther et al., 2014). Individual variation in stress response, specifically baseline and stress-induced glucocorticoid levels, also tend to be repeatable across life stages (e.g., Rensel & Schoech, 2011; Guenther et al., 2014; Small & Schoech, 2015; Baugh et al., 2017). Sex differences in these physiological mechanisms, which can be the result of sex differences in prenatal programming (Seckl & Meaney, 2004), could be one aspect influencing individual variation and consistency in behavior. For example, in dark-eyed juncos (Junco hyemalis) circulating testosterone related to aggressiveness in males only, but neural sensitivity to testosterone (e.g., abundance of androgen receptor) related to individual variation in aggressive behavior in females and males (Rosvall et al., 2012). Sex-differences in various aspects of the stress response (e.g., corticotropin-releasing hormone, Bangasser & Wiersielis, 2018) could also lead to long-lasting individual differences in behaviors. Consistent individual differences in stress response could represent a permanent feature of an individual’s phenotype (Cockrem, 2013; Duckworth, 2015) and may explain why behaviors associated with this physiological system, like escape behavior measured in the current study, remain consistent across long periods of time (Baugh et al., 2017).

Conclusion

Assessing personality within a single life stage may result in a partial view of an individual’s behavioral range. Our study found individuals’ social scores were repeatable within the juvenile stage while individuals’ escape scores were repeatable across developmental stages. Further, we observed strong sex differences in the repeatability of certain behavioral traits, but not others. We also observed that which traits were repeatable across ontogeny differed between the sexes. Our results are consistent with previous findings that sex differences in repeatability of behavioral traits are observed for some traits, but not others, and whether sex-differences are observed can depend on the species (Cabrera et al., 2021). Considering how ontogeny affects animal personality for males and females can provide insight into the evolution and mechanisms that maintain animal personality (Cabrera et al., 2021).

Supplementary Material

s1

Acknowledgements

This work was supported by National Institutes of Health (NIH) training grant (T32HD049336, awarded to JAC), by National Science Foundation (NSF) grant (IOS-1656414, awarded to GED and CLW), and the Indiana University Cox Research Scholarship (awarded to CHA). We thank all members of the Demas Lab, including Kat Munley, Beth Morrison, Jessica Deyoe, Luke Gohmann, and all the undergraduate volunteers that assisted with the study. Thank you to the Indiana University Veterinary and LAR staff, including Alicia Meranda, Calan Quate, and Dr. Randalyn Shepherd for animal care.

Footnotes

Conflict of Interest: The authors declare no conflict of interest.

Supplementary Material: Supplementary files are provided online

Data Availability: The data from this study are available upon request

References

  1. Amy M, Ung D, Béguin N, Leboucher G, & Fusani L (2017). Personality traits and behavioural profiles in the domestic canary are affected by sex and photoperiod. Ethology, 123(12), 885–893. doi: 10.1111/eth.12662 [DOI] [Google Scholar]
  2. Bangasser DA, & Wiersielis KR (2018). Sex differences in stress responses: a critical role for corticotropin-releasing factor. Hormones (Athens), 17(1), 5–13. doi: 10.1007/s42000-018-0002-z [DOI] [PubMed] [Google Scholar]
  3. Baugh AT, Senft RA, Firke M, Lauder A, Schroeder J, Meddle SL, …Hau M (2017). Risk-averse personalities have a systemically potentiated neuroendocrine stress axis: A multilevel experiment in Parus major. Horm Behav, 93, 99–108. doi: 10.1016/j.yhbeh.2017.05.011 [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bell AM, Hankison SJ, & Laskowski KL (2009). The repeatability of behaviour: a meta-analysis. Anim Behav, 77(4), 771–783. doi: 10.1016/j.anbehav.2008.12.022 [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bell AM, & Sih A (2007). Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett, 10(9), 828–834. doi: 10.1111/j.1461-0248.2007.01081.x [DOI] [PubMed] [Google Scholar]
  6. Cabrera D, Nilsson JR, & Griffen BD (2021). The development of animal personality across ontogeny: a cross-species review. Animal Behaviour, 173, 137–144. doi: 10.1016/j.anbehav.2021.01.003 [DOI] [Google Scholar]
  7. Carere C, Drent PJ, Privitera L, Koolhaas JM, & Groothuis TGG (2005). Personalities in great tits, Parus major: stability and consistency. Animal Behaviour, 70(4), 795–805. doi: 10.1016/j.anbehav.2005.01.003 [DOI] [Google Scholar]
  8. Cockrem JF (2013). Corticosterone responses and personality in birds: Individual variation and the ability to cope with environmental changes due to climate change. General and comparative endocrinology, 190, 156–163. doi: 10.1016/j.ygcen.2013.02.021 [DOI] [PubMed] [Google Scholar]
  9. Duckworth RA (2015). Neuroendocrine mechanisms underlying behavioral stability: implications for the evolutionary origin of personality. Ann N Y Acad Sci, 1360, 54–74. doi: 10.1111/nyas.12797 [DOI] [PubMed] [Google Scholar]
  10. Favati A, Zidar J, Thorpe H, Jensen P, & Løvlie H (2016). The ontogeny of personality traits in the red junglefowl, Gallus gallus. Behavioral Ecology, 27(2), 484–493. doi: 10.1093/beheco/arv177 [DOI] [Google Scholar]
  11. Friard O, & Gamba M (2016). BORIS: a free, versatile open-sourced event-logging software for video/audio coding and live observations. Methods in Ecology and Evolution, 7, 1325–1330. [Google Scholar]
  12. Groothuis TGG, & Carere C (2005). Avian personalities: characterization and epigenesis. Neuroscience & Biobehavioral Reviews, 29(1), 137–150. doi: 10.1016/j.neubiorev.2004.06.010 [DOI] [PubMed] [Google Scholar]
  13. Guenther A, Finkemeier MA, & Trillmich F (2014). The ontogeny of personality in the wild guinea pig. Animal Behaviour, 90, 131–139. doi: 10.1016/j.anbehav.2014.01.032 [DOI] [Google Scholar]
  14. Harper DGC (1994). Some comments on the repeatability of measurements. Ringing & Migration, 15(2), 84–90. doi: 10.1080/03078698.1994.9674078 [DOI] [Google Scholar]
  15. Hedrick AV, & Kortet R (2011). Sex differences in the repeatability of boldness over metamorphosis. Behavioral Ecology and Sociobiology, 66(3), 407–412. doi: 10.1007/s00265-011-1286-z [DOI] [Google Scholar]
  16. Herde A, & Eccard JA (2013). Consistency in boldness, activity and explorationat different stages of life. BMC Ecology, 13(49), 1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ibarra-Zatarain Z, Rey S, Boglino A, Fatsini E, & Duncan N (2020). Senegalese sole (Solea senegalensis) coping styles are consistent over time: behavioural and physiological responses during ontogenesis. Physiol Behav, 217, 112803. doi: 10.1016/j.physbeh.2020.112803 [DOI] [PubMed] [Google Scholar]
  18. Jacobs CGC, van Overveld T, Careau V, Matthysen E, Adriaensen F, & Slabbekoorn H (2014). Personality-dependent response to field playback in great tits: slow explorers can be strong responders. Animal Behaviour, 90, 65–71. doi: 10.1016/j.anbehav.2014.01.016 [DOI] [Google Scholar]
  19. Kanda LL, Louon L, & Straley K (2012). Stability in Activity and Boldness Across Time and Context in Captive Siberian Dwarf Hamsters. Ethology, 118(6), 518–533. doi: 10.1111/j.1439-0310.2012.02038.x [DOI] [Google Scholar]
  20. Kelleher SR, Silla AJ, & Byrne PG (2018). Animal personality and behavioral syndromes in amphibians: a review of the evidence, experimental approaches, and implications for conservation. Behavioral Ecology and Sociobiology, 72(5). doi: 10.1007/s00265-018-2493-7 [DOI] [Google Scholar]
  21. Kelley AD, Humphries MM, McAdam AG, & Boutin S (2015). Changes in wild red squirrel personality across ontogeny: activity and aggression regress towards the mean. Behaviour, 152(10), 1291–1306. doi: 10.1163/1568539x-00003279 [DOI] [Google Scholar]
  22. Koo TK, & Li MY (2016). A Guideline of Selecting and Reporting Intraclass Correlation Coefficients for Reliability Research. J Chiropr Med, 15(2), 155–163. doi: 10.1016/j.jcm.2016.02.012 [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Koolhaas JM, Korte SM, de Boer SF, Van Der Vegt BJ, Van Reene CG, Hopster H, …Blokhuis HJ (1999). Coping stypes in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev, 23, 925–935. [DOI] [PubMed] [Google Scholar]
  24. Le Vin AL, Mable BK, Taborsky M, Heg D, & Arnold KE (2011). Individual variation in helping in a cooperative breeder: relatedness versus behavioural type. Animal Behaviour, 82(3), 467–477. doi: 10.1016/j.anbehav.2011.05.021 [DOI] [Google Scholar]
  25. Miller R, Bugnyar T, Polzl K, & Schwab C (2015). Differences in exploration behaviour in common ravens and carrion crows during development and across social context. Behav Ecol Sociobiol, 69(7), 1209–1220. doi: 10.1007/s00265-015-1935-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Munley KM, Rendon NM, & Demas GE (2018). Neural Androgen Synthesis and Aggression: Insights From a Seasonally Breeding Rodent. Front Endocrinol (Lausanne), 9, 136. doi: 10.3389/fendo.2018.00136 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Munley KM, Trinidad JC, Deyoe JE, Adaniya CH, Nowakowski AM, Ren CC, …Demas GE (2021). Melatonin-dependent changes in neurosteroids are associated with increased aggression in a seasonally breeding rodent. J Neuroendocrinol, 33(3), e12940. doi: 10.1111/jne.12940 [DOI] [PubMed] [Google Scholar]
  28. Nakagawa S, & Cuthill IC (2007). Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev Camb Philos Soc, 82(4), 591–605. doi: 10.1111/j.1469-185X.2007.00027.x [DOI] [PubMed] [Google Scholar]
  29. Nakagawa S, & Schielzeth H (2010). Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev Camb Philos Soc, 85(4), 935–956. doi: 10.1111/j.1469-185X.2010.00141.x [DOI] [PubMed] [Google Scholar]
  30. Petelle MB, McCoy DE, Alejandro V, Martin JGA, & Blumstein DT (2013). Development of boldness and docility in yellow-bellied marmots. Animal Behaviour, 86(6), 1147–1154. doi: 10.1016/j.anbehav.2013.09.016 [DOI] [Google Scholar]
  31. Polverino G, Cigliano C, Nakayama S, & Mehner T (2016). Emergence and development of personality over the ontogeny of fish in absence of environmental stress factors. Behavioral Ecology and Sociobiology, 70(12), 2027–2037. doi: 10.1007/s00265-016-2206-z [DOI] [Google Scholar]
  32. R Core Team. (2020). R: A language and environment for statistical computeing. R Foundation for Statistical Computing [Google Scholar]
  33. Reale D, Gallent BY, Leblanc M, & Festa-Bianchet M (2000). Consistency of temperment in bighorn ewes and correlates with behaviour and life history. Animal Behaviour, 60, 589–597. [DOI] [PubMed] [Google Scholar]
  34. Réale D, Reader SM, Sol D, McDougall PT, & Dingemanse NJ (2007). Integrating animal temperament within ecology and evolution. Biological Reviews, 82(2), 291–318. doi: 10.1111/j.1469-185X.2007.00010.x [DOI] [PubMed] [Google Scholar]
  35. Rensel MA, & Schoech SJ (2011). Repeatability of baseline and stress-induced corticosterone levels across early life stages in the Florida scrub-jay (Aphelocoma coerulescens). Horm Behav, 59(4), 497–502. doi: 10.1016/j.yhbeh.2011.01.010 [DOI] [PubMed] [Google Scholar]
  36. Rodel HG, & Meyer S (2011). Early development influences ontogeny of personality types in young laboratory rats. Dev Psychobiol, 53(6), 601–613. doi: 10.1002/dev.20522 [DOI] [PubMed] [Google Scholar]
  37. Ross PD (1998). Phodopus sungorus. Mammalian Species, 595, 1–9. doi: 10.2307/0.595.1/2600758 [DOI] [Google Scholar]
  38. Rosvall KA, Bergeon Burns CM, Barske J, Goodson JL, Schlinger BA, Sengelaub DR, & Ketterson ED (2012). Neural sensitivity to sex steroids predicts individual differences in aggression: implications for behavioural evolution. Proc Biol Sci, 279(1742), 3547–3555. doi: 10.1098/rspb.2012.0442 [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Schürch R, & Heg D (2010). Life history and behavioral type in the highly social cichlid Neolamprologus pulcher. Behavioral Ecology, 21(3), 588–598. doi: 10.1093/beheco/arq024 [DOI] [Google Scholar]
  40. Schuster AC, Carl T, & Foerster K (2017). Repeatability and consistency of individual behaviour in juvenile and adult Eurasian harvest mice. Naturwissenschaften, 104(3–4), 10. doi: 10.1007/s00114-017-1430-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Scotti MA, Belen J, Jackson JE, & Demas GE (2008). The role of androgens in the mediation of seasonal territorial aggression in male Siberian hamsters (Phodopus sungorus). Physiol Behav, 95(5), 633–640. doi: 10.1016/j.physbeh.2008.09.009 [DOI] [PubMed] [Google Scholar]
  42. Seckl JR, & Meaney MJ (2004). Glucocorticoid programming. Ann N Y Acad Sci, 1032, 63–84. doi: 10.1196/annals.1314.006 [DOI] [PubMed] [Google Scholar]
  43. Sih A, & Del Giudice M (2012). Linking behavioural syndromes and cognition: a behavioural ecology perspective. Philos Trans R Soc Lond B Biol Sci, 367(1603), 2762–2772. doi: 10.1098/rstb.2012.0216 [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Small TW, & Schoech SJ (2015). Sex differences in the long-term repeatability of the acute stress response in long-lived, free-living Florida scrub-jays (Aphelocoma coerulescens). Journal of Comparative Physiology B, 185(1), 119–133. doi: 10.1007/s00360-014-0866-4 [DOI] [PubMed] [Google Scholar]
  45. Stamps J, & Groothuis TG (2010). The development of animal personality: relevance, concepts and perspectives. Biol Rev Camb Philos Soc, 85(2), 301–325. doi: 10.1111/j.1469-185X.2009.00103.x [DOI] [PubMed] [Google Scholar]
  46. Stoffel MA, Nakagawa S, Schielzeth H, & Goslee S (2017). rptR: repeatability estimation and variance decomposition by generalized linear mixed‐effects models. Methods in Ecology and Evolution, 8(11), 1639–1644. doi: 10.1111/2041-210x.12797 [DOI] [Google Scholar]
  47. Sylvia KE, Jewell CP, Rendon NM, St John EA, & Demas GE (2017). Sex-specific modulation of the gut microbiome and behavior in Siberian hamsters. Brain Behav Immun, 60, 51–62. doi: 10.1016/j.bbi.2016.10.023 [DOI] [PubMed] [Google Scholar]
  48. Tinbergen N (1963). On aims and methods of ethology. Zeitschrift für Tierpsychologie, 20, 410–433. [Google Scholar]
  49. Wolak ME, Fairbairn DJ, & Paulsen YR (2012). Guidelines for estimating repeatability. Methods in Ecology and Evolution, 3(1), 129–137. doi: 10.1111/j.2041-210X.2011.00125.x [DOI] [Google Scholar]
  50. Wuerz Y, & Kruger O (2015). Personality over ontogeny in zebra finches: long-term repeatable traits but unstable behaviouralsyndromes. Frontiers in Zoology, 12, 1–12. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

s1
NIHMS1717054-supplement-s1.docx (13.9KB, docx)

RESOURCES