An exploratory study of behavioral traits and the establishment of social relationships in female laboratory rats

1.

Hinde RA. Interactions, relationships and social structure. Man. 1976; 11(1):1–17.

2.

Massen J, Sterck E, de Vos H. Close social associations in animals and humans: functions and mechanisms of friendship. Behaviour. 2010; 147(11):1379–412.

3.

Seyfarth RM, Cheney DL. The Evolutionary Origins of friendship. Annu Rev Psychol. 2011; 63(1):153–

77. https://doi.org/10.1146/annurev-psych-120710-100337 PMID: 21740224

4.

Silk JB. The adaptive value of sociality in mammalian groups. Philos Trans R Soc Lond B Biol Sci.

2007; 362(1480):539–59. https://doi.org/10.1098/rstb.2006.1994 PMID: 17363359

5.

Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, et al. Strong and consistent

social bonds enhance the longevity of female baboons. Curr Biol. 2010; 20(15):1359–61. https://doi.

org/10.1016/j.cub.2010.05.067 PMID: 20598541

6.

Cameron EZ, Setsaas TH, Linklater WL. Social bonds between unrelated females increase reproductive success in feral horses. Proc Natl Acad Sci. 2009; 106(33):13850–3. https://doi.org/10.1073/pnas.

0900639106 PMID: 19667179

7.

Weidt A, Hofmann SE, Ko¨nig B. Not only mate choice matters: fitness consequences of social partner

choice in female house mice. Anim Behav. 2008; 75(3):801–8.

PLOS ONE | https://doi.org/10.1371/journal.pone.0295280 December 4, 2023

18 / 21

PLOS ONE

Behavioral traits and the establishment of social relationships in rats

8.

Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, et al. The benefits of social

capital: close social bonds among female baboons enhance offspring survival. Proc Biol Sci. 2009; 276

(1670):3099–104. https://doi.org/10.1098/rspb.2009.0681 PMID: 19515668

9.

Hirsch BT, Stanton MA, Maldonado JE. Kinship shapes affiliative social networks but not aggression in

ring-tailed coatis. PLOS ONE. 2012; 7(5):e37301. https://doi.org/10.1371/journal.pone.0037301 PMID:

22624010

10.

Schino G. Grooming, competition and social rank among female primates: a meta-analysis. Anim

Behav. 2001; 62(2):265–71.

11.

Silk J. Using the ’F’-word in primatology. Behaviour. 2002; 139(2):421–46.

12.

Guilhem C, Bideau E, Gerard JF, Maublanc ML. Agonistic and proximity patterns in enclosed mouflon

(Ovis gmelini) ewes in relation to age, reproductive status and kinship. Behav Process. 2000; 50

(2):101–12. https://doi.org/10.1016/s0376-6357(00)00094-2 PMID: 10969187

13.

de Waal FBM, Luttrell LM. The Similarity Principle underlying social bonding among female rhesus

monkeys. Folia Primatol. 1986; 46(4):215–34. https://doi.org/10.1159/000156255 PMID: 3557225

14.

Dingemanse NJ, Re´ale D. Natural selection and animal personality. Behaviour. 2005; 142(9–10):1159–

84.

15.

Uher J. Comparative personality research: methodological approaches. Eur J Pers. 2008; 22: 427–

455.

16.

Freeman HD, Gosling SD. Personality in nonhuman primates: a review and evaluation of past research.

Am J Primatol. 2010; 72: 653–671. https://doi.org/10.1002/ajp.20833 PMID: 20568079

17.

Re´ale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. Integrating animal temperament within

ecology and evolution. Biol Rev. 2007; 82(2):291–318. https://doi.org/10.1111/j.1469-185X.2007.

00010.x PMID: 17437562

18.

Gartland LA, Firth JA, Laskowski KL, Jeanson R, Ioannou CC. Sociability as a personality trait in animals: methods, causes and consequences. Biol Rev Camb Philos Soc. 2022; 97(2):802–16. https://doi.

org/10.1111/brv.12823 PMID: 34894041

19.

Best EC, Blomberg SP, Goldizen AW. Shy female kangaroos seek safety in numbers and have fewer

preferred friendships. Behav Ecol. 2015; 26(2):639–46.

20.

Michelena P, Jeanson R, Deneubourg J-L, Sibbald AM. Personality and collective decision-making in

foraging herbivores. Proc R Soc B: Biol Sci. 2009; 277(1684):1093–9. https://doi.org/10.1098/rspb.

2009.1926 PMID: 19955156

21.

Snijders L, Naguib M, van Oers K. Dominance rank and boldness predict social attraction in great tits.

Behav Ecol. 2017; 28(2):398–406.

22.

Skinner M, Miller N. Aggregation and social interaction in garter snakes (Thamnophis sirtalis sirtalis).

Behav Ecol Sociobiol. 2020; 74(5):51.

23.

Varma V, Vasoya H, Jain A, Binoy VV. ‘The Bold are the Sociable’: Personality traits and laterality in an

indigenous megafish, the Deccan Mahseer (Tor khudree). Ichthyol Res. 2020; 67(4):483–92.

24.

Irving E, Brown C. Examining the link between personality and laterality in a feral guppy Poecilia reticulata population. J Fish Biol. 2013; 83(2):311–25.

25.

Bevan PA, Gosetto I, Jenkins ER, Barnes I, Ioannou CC. Regulation between personality traits: individual social tendencies modulate whether boldness and leadership are correlated. Proc R Soc B: Biol Sci.

2018; 285(1880):20180829. https://doi.org/10.1098/rspb.2018.0829 PMID: 29899075

26.

Aplin LM, Farine DR, Morand-Ferron J, Cole EF, Cockburn A, Sheldon BC. Individual personalities predict social behaviour in wild networks of great tits (Parus major). Ecol Lett. 2013; 16(11):1365–72.

27.

Petelle MB, Martin JGA, Blumstein DT. Heritability and genetic correlations of personality traits in a wild

population of yellow-bellied marmots (Marmota flaviventris). J Evol Biol. 2015; 28(10):1840–8.

28.

Michelangeli M, Chapple DG, Wong BBM. Are behavioural syndromes sex specific? Personality in a

widespread lizard species. Behav Ecol Sociobiol. 2016; 70(11):1911–9.

29.

Ro¨del HG, Zapka M, Talke S, Kornatz T, Bruchner B, Hedler C. Survival costs of fast exploration during

juvenile life in a small mammal. Behav Ecol Sociobiol. 2015; 69(2):205–17.

30.

Thys B, Eens M, Aerts S, Delory A, Iserbyt A, Pinxten R. Exploration and sociability in a highly gregarious bird are repeatable across seasons and in the long term but are unrelated. Anim Behav. 2017;

123:339–48.

31.

Jolles JW, Boogert NJ, Sridhar VH, Couzin ID, Manica A. Consistent individual differences drive collective behavior and group functioning of schooling fish. Curr Biol. 2017; 27(18):2862–8.e7. https://doi.org/

10.1016/j.cub.2017.08.004 PMID: 28889975

32.

Massen JJM, Koski SE. Chimps of a feather sit together: chimpanzee friendships are based on homophily in personality. Evol Hum Behav. 2014; 35(1):1–8.

PLOS ONE | https://doi.org/10.1371/journal.pone.0295280 December 4, 2023

19 / 21

PLOS ONE

Behavioral traits and the establishment of social relationships in rats

33.

Morton FB, Weiss A, Buchanan-Smith HM, Lee PC. Capuchin monkeys with similar personalities have

higher-quality relationships independent of age, sex, kinship and rank. Anim Behav. 2015; 105:163–71.

34.

Verspeek J, Staes N, Leeuwen EJCv, Eens M, Stevens JMG. Bonobo personality predicts friendship.

Sci Rep. 2019; 9(1):19245. https://doi.org/10.1038/s41598-019-55884-3 PMID: 31848407

35.

Lindsey JR, Baker HJ. Chapter 1—Historical Foundations. In: Suckow MA, Weisbroth SH, Franklin CL,

editors. The Laboratory Rat ( Second Edition). Burlington: Academic Press; 2006. p. 1–52.

36.

Davis DE. The Characteristics of rat populations. Q Rev Biol. 1953; 28(4):373–401. https://doi.org/10.

1086/399860 PMID: 13121239

37.

Calhoun JB. The ecology and sociology of the Norway rat. Maryland: Department of Health, Education

and Welfare; 1963.

38.

Ma´rquez C, Rennie Scott M, Costa Diana F, Moita Marta A. Prosocial choice in rats depends on foodseeking behavior displayed by recipients. Curr Biol. 2015; 25(13):1736–45. https://doi.org/10.1016/j.

cub.2015.05.018 PMID: 26051895

39.

B-A Bartal I, Decety J, Mason P. Empathy and pro-social behavior in rats. Science. 2011; 334

(6061):1427–30. https://doi.org/10.1126/science.1210789 PMID: 22158823

40.

Schweinfurth MK, Taborsky M. Reciprocal trading of different commodities in Norway rats. Curr Biol.

2018; 28(4):594–9.e3. https://doi.org/10.1016/j.cub.2017.12.058 PMID: 29398215

41.

Meyza KZ, Bartal IB-A, Monfils MH, Panksepp JB, Knapska E. The roots of empathy: Through the lens

of rodent models. Neurosci Biobehav Rev. 2017; 76:216–34. https://doi.org/10.1016/j.neubiorev.2016.

10.028 PMID: 27825924

42.

Gheusi G, Goodall G, Dantzer R. Individually distinctive odours represent individual conspecifics in rats.

Anim Behav. 1997; 53(5):935–44.

43.

Hepper PG. The amniotic fluid: an important priming role in kin recognition. Anim Behav. 1987; 35

(5):1343–6.

44.

Proops L, Troisi CA, Kleinhappel TK, Romero T. Non-random associations in group housed rats (Rattus

norvegicus). Sci Rep. 2021; 11(1):15349.

45.

Schweinfurth MK, Neuenschwander J, Engqvist L, Schneeberger K, Rentsch AK, Gygax M, et al. Do

female Norway rats form social bonds? Behav Ecol Sociobiol. 2017; 71(6).

46.

Rudolfova´ V, Petra´sek T, Antosˇova´ E, Frynta D, Landova´ E, Valesˇ K, et al. Inter-individual differences

in laboratory rats as revealed by three behavioural tasks. Sci Rep. 2022; 12(1):9361. https://doi.org/10.

1038/s41598-022-13288-w PMID: 35672428

47.

Sachser N. Of Domestic and wild Guinea pigs: Studies in sociophysiology, domestication, and social

evolution. Naturwissenschaften. 1998; 85(7):307–17. https://doi.org/10.1007/s001140050507 PMID:

9722963

48.

Ku¨nzl C, Sachser N. The behavioral endocrinology of domestication: A comparison between the

domestic Guinea pig (Cavia apereaf.porcellus) and its wild ancestor, the cavy (Cavia aperea). Horm

Behav. 1999; 35(1):28–37.

49.

Albert FW, Shchepina O, Winter C, Ro¨mpler H, Teupser D, Palme R, et al. Phenotypic differences in

behavior, physiology and neurochemistry between rats selected for tameness and for defensive aggression towards humans. Horm Behav. 2008; 53(3):413–21. https://doi.org/10.1016/j.yhbeh.2007.11.010

PMID: 18177873

50.

Nagayama H, Matsumoto Y, Tanave A, Nihei M, Goto T, Koide T. Measuring active and passive tameness separately in mice. J Vis Exp. 2018(138):58048. https://doi.org/10.3791/58048 PMID: 30148490

51.

Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R. Animal personality: what are behavioural ecologists measuring? Biol Rev. 2013; 88: 465–475. https://doi.org/10.1111/brv.12007 PMID:

23253069

52.

Mathis A, Mamidanna P, Cury KM, Abe T, Murthy VN, Mathis MW, et al. DeepLabCut: markerless pose

estimation of user-defined body parts with deep learning. Nat Neurosci. 2018; 21(9):1281–9. https://doi.

org/10.1038/s41593-018-0209-y PMID: 30127430

53.

Ziporyn T, McClintock MK. Passing as an indicator of social dominance among female wild and domestic Norway rats. Behaviour. 1991; 118(1–2):26–41.

54.

R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical

Computing, Vienna, Austria. 2022 URL https://www.R-project.org/.

55.

Weiss A, Adams MJ, Widdig A, Gerald MS. Rhesus macaques (Macaca mulatta) as living fossils of

hominoid personality and subjective well-being. J Comp Psychol. 2011; 125(1):72–83.

56.

Rankin G, Stokes M. Reliability of assessment tools in rehabilitation: an illustration of appropriate statistical analyses. Clin Rehabil. 1998; 12(3):187–99. https://doi.org/10.1191/026921598672178340 PMID:

9688034

PLOS ONE | https://doi.org/10.1371/journal.pone.0295280 December 4, 2023

20 / 21

PLOS ONE

Behavioral traits and the establishment of social relationships in rats

57.

Castro JE, Diessler S, Varea E, Ma´rquez C, Larsen MH, Cordero MI, et al. Personality traits in rats predict vulnerability and resilience to developing stress-induced depression-like behaviors, HPA axis

hyper-reactivity and brain changes in pERK1/2 activity. Psychoneuroendocrinology. 2012; 37(8):1209–

23. https://doi.org/10.1016/j.psyneuen.2011.12.014 PMID: 22240307

58.

Ramos A, Berton O, Mormède P, Chaouloff F. A multiple-test study of anxiety-related behaviours in six

inbred rat strains. Behav Brain Res. 1997; 85(1):57–69. https://doi.org/10.1016/s0166-4328(96)001647 PMID: 9095342

59.

Moroi S, Nishimura K, Imai N, Kunishige K, Sato S, Goto T. Rapid behavioral assay using handling test

provides breed and sex differences in tameness of chickens. Brain Behav. 2019; 9(10):e01394. https://

doi.org/10.1002/brb3.1394 PMID: 31456336

60.

Korpela K, Sundell J, Ylo¨nen H. Does personality in small rodents vary depending on population density? Oecologia. 2011; 165(1):67–77. https://doi.org/10.1007/s00442-010-1810-2 PMID: 20976607

ˇ lipogor V, Graf C, Massen JJM, Bugnyar T. Personality and social environment predict cognitive perS

formance in common marmosets (Callithrix jacchus). Sci Rep. 2022; 12(1):6702.

61.

62.

McMahon EK, Farhan S, Cavigelli SA. How do we characterize temperament? Broad testing of temperament across time and contexts in low-variable conditions. Anim Behav. 2023; 195:29–42.

63.

Clutton-Brock TH, Lukas D. The evolution of social philopatry and dispersal in female mammals. Mol

Ecol. 2012; 21(3):472–92. https://doi.org/10.1111/j.1365-294X.2011.05232.x PMID: 21883582

64.

Gardner-Santana LC, Norris DE, Fornadel CM, Hinson ER, Klein SL, Glass GE. Commensal ecology,

urban landscapes, and their influence on the genetic characteristics of city-dwelling Norway rats (Rattus

norvegicus). Mol Ecol. 2009; 18(13):2766–78.

65.

Schweinfurth MK. The social life of Norway rats (Rattus norvegicus). Elife. 2020; 9.

66.

Kiyokawa Y, Honda A, Takeuchi Y, Mori Y. A familiar conspecific is more effective than an unfamiliar

conspecific for social buffering of conditioned fear responses in male rats. Behav Brain Res. 2014;

267:189–93. https://doi.org/10.1016/j.bbr.2014.03.043 PMID: 24698797

67.

Rogers-Carter MM, Varela JA, Gribbons KB, Pierce AF, McGoey MT, Ritchey M, et al. Insular cortex

mediates approach and avoidance responses to social affective stimuli. Nat Neurosci. 2018; 21(3):404–

14. https://doi.org/10.1038/s41593-018-0071-y PMID: 29379116

68.

Dorfman A, Weiss O, Hagbi Z, Levi A, Eilam D. Social spatial cognition. Neurosci Biobehav Rev. 2021;

121:277–90. https://doi.org/10.1016/j.neubiorev.2020.12.023 PMID: 33373664

69.

Weiss O, Levi A, Segev E, Simbirsky M, Eilam D. Spatio-temporal organization during group formation

in rats. Anim Cogn. 2018; 21(4):513–29. https://doi.org/10.1007/s10071-018-1185-z PMID: 29721699

70.

Wilkins AS, Wrangham RW, Fitch WT. The "domestication syndrome" in mammals: a unified explanation based on neural crest cell behavior and genetics. Genetics. 2014; 197(3):795–808.

71.

Pellis SM, Pellis VC, Himmler BT, Modlinska K, Stryjek R, Kolb B, et al. Domestication and the role of

social play on the development of socio-cognitive skills in rats. Int J Comp Psychol.2019; 32: 41031.

PLOS ONE | https://doi.org/10.1371/journal.pone.0295280 December 4, 2023

21 / 21

...