Linking personality traits and reproductive success in common marmoset (Callithrix jacchus)
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
NC/K500434/1
National Centre for the Replacement, Refinement and Reduction of Animals in Research - United Kingdom
P51 OD011106
NIH HHS - United States
PubMed
35922528
PubMed Central
PMC9349211
DOI
10.1038/s41598-022-16339-4
PII: 10.1038/s41598-022-16339-4
Knihovny.cz E-zdroje
- MeSH
- Callithrix * MeSH
- osobnost MeSH
- poruchy osobnosti MeSH
- rozmnožování * MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Animal personality can affect individual fitness and population growth. Personality traits of either parent or parents' combination may facilitate reproduction and offspring survival across species. However, previous studies focused mainly on the role of only one sex, and the link between personality and fitness has not been confirmed in primates. We examined this link in both sexes of captive common marmosets (Callithrix jacchus), a cooperatively breeding primate with extensive paternal care. We studied the effects of five personality traits of the parents (Agreeableness, Assertiveness, Conscientiousness, Inquisitiveness, and Patience), including their absolute and directional differences within pairs, on key components of reproductive performance. We expected pairs with more similar personality scores to have higher reproductive success as found in other species with long-term pairs and biparental care, but found no evidence for this hypothesis. Instead, we detected strong effects of female traits on inter-birth intervals, which were shorter in more agreeable females, and fecundity rates, which were higher in more inquisitive females. Male traits appeared to have only a limited effect on reproductive success of the pair. Our study demonstrates that various aspects of animal personality underpin reproductive performance in captive common marmosets and provides novel insights into the possible ultimate causes of personality in cooperatively breeding species.
Czech Academy of Sciences Biology Centre Institute of Entomology České Budějovice Czech Republic
Department of Zoology Faculty of Science University of South Bohemia České Budějovice Czech Republic
Psychology Faculty of Natural Sciences University of Stirling Stirling Scotland UK
Scottish Primate Research Group Stirling Scotland UK
Wisconsin National Primate Research Center University of Wisconsin Madison USA
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Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. Integrating animal temperament within ecology and evolution. Biol. Rev. 2007;82:291–318. doi: 10.1111/j.1469-185X.2007.00010.x. PubMed DOI
Smith BR, Blumstein DT. Fitness consequences of personality: A meta-analysis. Behav. Ecol. 2008;19:448–455. doi: 10.1093/beheco/arm144. DOI
Gasparini C, Speechley EM, Polverino G. The bold and the sperm: Positive association between boldness and sperm number in the guppy. R. Soc. Open Sci. 2019;6:190474. doi: 10.1098/rsos.190474. PubMed DOI PMC
Jokela M, Alvergne A, Pollet TV, Lummaa V. Reproductive behavior and personality traits of the five factor model. Eur. J. Pers. 2011;25:487–500. doi: 10.1002/per.822. DOI
Schuett W, Dall SRX, Royle NJ. Pairs of zebra finches with similar ‘personalities’ make better parents. Anim. Behav. 2011;81:609–618. doi: 10.1016/j.anbehav.2010.12.006. DOI
Vetter SG, et al. Shy is sometimes better: Personality and juvenile body mass affect adult reproductive success in wild boars, Sus scrofa. Anim. Behav. 2016;115:193–205. doi: 10.1016/j.anbehav.2016.03.026. DOI
Weiss A. Personality traits: A view from the animal kingdom. J. Pers. 2018;86:12–22. doi: 10.1111/jopy.12310. PubMed DOI
Bergmüller R, Taborsky M. Animal personality due to social niche specialisation. Trends Ecol. Evol. 2010;25:504–511. doi: 10.1016/j.tree.2010.06.012. PubMed DOI
Montiglio PO, Wey TW, Chang AT, Fogarty S, Sih A. Correlational selection on personality and social plasticity: Morphology and social context determine behavioural effects on mating success. J. Anim. Ecol. 2017;86:213–226. doi: 10.1111/1365-2656.12610. PubMed DOI
Wolf M, McNamara JM. On the evolution of personalities via frequency-dependent selection. Am. Nat. 2012;179:679–692. doi: 10.1086/665656. PubMed DOI
Munson AA, Jones C, Schraft H, Sih A. You’re just my type: Mate choice and behavioral types. Trends Ecol. Evol. 2020;35:823–833. doi: 10.1016/j.tree.2020.04.010. PubMed DOI
Muller H, Chittka L. Animal personalities: The advantage of diversity. Curr. Biol. 2008;18:961–963. doi: 10.1016/j.cub.2008.09.001. PubMed DOI
Biro PA, Stamps JA. Are animal personality traits linked to life-history productivity? Trends Ecol. Evol. 2008;23:361–368. doi: 10.1016/j.tree.2008.04.003. PubMed DOI
Dingemanse NJ, Both C, Drent PJ, Tinbergen JM. Fitness consequences of avian personalities in a fluctuating environment. Proc. R. Soc. B. 2004;271:847–852. doi: 10.1098/rspb.2004.2680. PubMed DOI PMC
Boon AK, Réale D, Boutin S. The interaction between personality, offspring fitness and food abundance in North American red squirrels. Ecol. Lett. 2007;10:1094–1104. doi: 10.1111/j.1461-0248.2007.01106.x. PubMed DOI
Nicolaus M, Tinbergen JM, Ubels R, Both C, Dingemanse NJ. Density fluctuations represent a key process maintaining personality variation in a wild passerine bird. Ecol. Lett. 2016;19:478–486. doi: 10.1111/ele.12584. PubMed DOI
Altschul DM, et al. Personality links with lifespan in chimpanzees. eLife. 2018;7:e33781. doi: 10.7554/eLife.33781. PubMed DOI PMC
Réale D, Martin J, Coltman DW, Poissant J, Festa-Bianchet M. Male personality, life-history strategies and reproductive success in a promiscuous mammal. J. Evol. Biol. 2009;22:1599–1607. doi: 10.1111/j.1420-9101.2009.01781.x. PubMed DOI
Brent LJN, et al. Personality traits in rhesus macaques (Macaca mulatta) are heritable but do not predict reproductive output. Int. J. Primatol. 2014;35:188–209. doi: 10.1007/s10764-013-9724-6. PubMed DOI PMC
Rangassamy M, Dalmas M, Féron C, Gouat P, Rödel HG. Similarity of personalities speeds up reproduction in pairs of a monogamous rodent. Anim. Behav. 2015;103:7–15. doi: 10.1016/j.anbehav.2015.02.007. DOI
Schuett W, Tregenza T, Dall SRX. Sexual selection and animal personality. Biol. Rev. 2010;85:217–246. doi: 10.1111/j.1469-185X.2009.00101.x. PubMed DOI
Carlstead K, Fraser J, Bennett C, Kleiman DG. Black rhinoceros (Diceros bicornis) in US zoos: II. Behavior, breeding success, and mortality in relation to housing facilities. Zoo Biol. 1999;18:35–52. doi: 10.1002/(SICI)1098-2361(1999)18:1<35::AID-ZOO5>3.0.CO;2-L. DOI
Martin-Wintle MS, et al. Do opposites attract? Effects of personality matching in breeding pairs of captive giant pandas on reproductive success. Biol. Conserv. 2017;207:27–37. doi: 10.1016/j.biocon.2017.01.010. DOI
Fox RA, Millam JR. Personality traits of pair members predict pair compatibility and reproductive success in a socially monogamous parrot breeding in captivity. Zoo Biol. 2014;33:166–172. doi: 10.1002/zoo.21121. PubMed DOI
Choi S, Grocutt E, Erlandsson R, Angerbjörn A. Parent personality is linked to juvenile mortality and stress behavior in the arctic fox (Vulpes lagopus) Behav. Ecol. Sociobiol. 2019;73:162. doi: 10.1007/s00265-019-2772-y. DOI
Kappeler PM, van Schaik CP. Evolution of primate social systems. Int. J. Primatol. 2002;23:707–740. doi: 10.1023/A:1015520830318. DOI
Tardif SD, et al. Reproduction in captive common marmosets (Callithrix jacchus) Comp. Med. 2003;53:364–368. PubMed
Marini R, Wachtman L, Tardif S, Mansfield K, Fox J. The Common Marmoset in Captivity and Biomedical Research. Academic Press; 2019.
Arruda MDF, Yamamoto ME, Pessoa DMA, Araujo A. Taxonomy and Natural History. In: Marini R, Wachtman L, Tardif S, Mansfield K, Fox J, editors. The Common Marmoset in Captivity and Biomedical Research. Academic Press; 2019. pp. 3–15.
Buchanan-Smith HM. Marmosets and tamarins. In: Hubrecht R, Kirkwood J, editors. The UFAW Handbook on the Care and Management of Laboratory and Other Research Animals. Wiley-Blackwell; 2010.
Smucny DA, et al. Reproductive output, maternal age, and survivorship in captive common marmoset females (Callithrix jacchus) Am. J. Primatol. 2004;64:107–121. doi: 10.1002/ajp.20065. PubMed DOI
Ash H, Buchanan-Smith HM. Long-term data on reproductive output and longevity in captive female common marmosets (Callithrix jacchus) Am. J. Primatol. 2014;76:1062–1073. doi: 10.1002/ajp.22293. PubMed DOI
Frye BM, et al. After short interbirth intervals, captive callitrichine monkeys have higher infant mortality. iScience. 2022;25:103724. doi: 10.1016/j.isci.2021.103724. PubMed DOI PMC
McCoy DE, et al. A comparative study of litter size and sex composition in a large dataset of callitrichine monkeys. Am. J. Primatol. 2019;81:e23038. doi: 10.1002/ajp.23038. PubMed DOI PMC
Jaquish CE, Tardif SD, Cheverud JM. Interactions between infant growth and survival: Evidence for selection on age-specific body weight in captive common marmosets (Callithrix jacchus) Am. J. Primatol. 1997;42:269–280. doi: 10.1002/(SICI)1098-2345(1997)42:4<269::AID-AJP2>3.0.CO;2-V. PubMed DOI
Tardif SD, Jaquish CE. Number of ovulations in the marmoset monkey (Callithrix jacchus): Relation to body weight, age and repeatability. Am. J. Primatol. 1997;42:323–329. doi: 10.1002/(SICI)1098-2345(1997)42:4<323::AID-AJP7>3.0.CO;2-Z. PubMed DOI
Poole TB, Evans RG. Reproduction, infant survival and productivity of a colony of common marmosets (Callithrix jacchus jacchus) Lab. Anim. 1982;16:88–97. doi: 10.1258/002367782780908760. PubMed DOI
Tardif SD, Richter CB, Carson RL. Effects of sibling-rearing experience on future reproductive success in two species of callitrichidae. Am. J. Primatol. 1984;6:377–380. doi: 10.1002/ajp.1350060408. PubMed DOI
Rothe H, Koenig A, Darms K. Infant survival and number of helpers in captive groups of common marmosets (Callithrix jacchus) Am. J. Primatol. 1993;30:131–137. doi: 10.1002/ajp.1350300205. PubMed DOI
Koski SE, Buchanan-Smith HM, Burkart JM, Bugnyar T, Weiss A. Common marmoset (Callithrix jacchus) personality. J. Comp. Psychol. 2017;131:326–336. doi: 10.1037/com0000089. PubMed DOI
Šlipogor V, Burkart JM, Martin JS, Bugnyar T, Koski SE. Personality method validation in common marmosets (Callithrix jacchus): Getting the best of both worlds. J. Comp. Psychol. 2020;134:52–70. doi: 10.1037/com0000188. PubMed DOI
Weiss A, Yokoyama C, Hayashi T, Inoue-Murayama M. Personality, subjective well-being, and the serotonin 1a receptor gene in common marmosets (Callithrix jacchus) PLoS ONE. 2021;16:e0238663. doi: 10.1371/journal.pone.0238663. PubMed DOI PMC
Freeman H, Gosling SD, Schapiro SJ. Comparison of methods for assessing personality in nonhuman primates. In: Weiss A, King JE, Murray L, editors. Personality and Temperament in Nonhuman Primates. Springer; 2011. pp. 17–40.
Finkenwirth C, Burkart JM. Why help? Relationship quality, not strategic grooming predicts infant-care in group-living marmosets. Physiol. Behav. 2018;193:108–116. doi: 10.1016/j.physbeh.2018.02.050. PubMed DOI
Haines JA, et al. Sex- and context-specific associations between personality and a measure of fitness but no link with life history traits. Anim. Behav. 2020;167:23–39. doi: 10.1016/j.anbehav.2020.06.013. DOI
Carlstead K, Mellen J, Kleiman DG. Black rhinoceros (Diceros bicornis) in US zoos: I. Individual behavior profiles and their relationship to breeding success. Zoo Biol. 1999;18:17–34. doi: 10.1002/(SICI)1098-2361(1999)18:1<17::AID-ZOO4>3.0.CO;2-K. DOI
Berg V, Lummaa V, Lahdenperä M, Rotkirch A, Jokela M. Personality and long-term reproductive success measured by the number of grandchildren. Evol. Hum. Behav. 2014;35:533–539. doi: 10.1016/j.evolhumbehav.2014.07.006. DOI
Silva HPA, Sousa MBC. The pair-bond formation and its role in the stimulation of reproductive function in female common marmosets (Callithrix jacchus) Int. J. Primatol. 1997;18:387–400. doi: 10.1023/A:1026386417039. DOI
Cavanaugh J, Mustoe AC, Taylor JH, French JA. Oxytocin facilitates fidelity in well-established marmoset pairs by reducing sociosexual behavior toward opposite-sex strangers. Psychoneuroendocrinology. 2014;49:1–10. doi: 10.1016/j.psyneuen.2014.06.020. PubMed DOI PMC
Andersen IL, Nævdal E, Bøe KE. Maternal investment, sibling competition, and offspring survival with increasing litter size and parity in pigs (Sus scrofa) Behav. Ecol. Sociobiol. 2011;65:1159–1167. doi: 10.1007/s00265-010-1128-4. PubMed DOI PMC
Johnstone-Yellin TL, Shipley LA, Myers WL, Robinson HS. To twin or not to twin? Trade-offs in litter size and fawn survival in mule deer. J. Mammal. 2009;90:453–460. doi: 10.1644/08-MAMM-A-030.1. DOI
Ariyomo TO, Watt PJ. The effect of variation in boldness and aggressiveness on the reproductive success of zebrafish. Anim. Behav. 2012;83:41–46. doi: 10.1016/j.anbehav.2011.10.004. DOI
Patterson LD, Schulte-Hostedde AI. Behavioural correlates of parasitism and reproductive success in male eastern chipmunks, Tamias striatus. Anim. Behav. 2011;81:1129–1137. doi: 10.1016/j.anbehav.2011.02.016. DOI
Mutzel A, Dingemanse NJ, Araya-Ajoy YG, Kempenaers B. Parental provisioning behaviour plays a key role in linking personality with reproductive success. Proc. R. Soc. B. 2013;280:20131019. doi: 10.1098/rspb.2013.1019. PubMed DOI PMC
Costa TSO, et al. Individual behavioral differences and health of golden-headed lion tamarins (Leontopithecus chrysomelas) Am. J. Primatol. 2020;82:e23118. doi: 10.1002/ajp.23118. PubMed DOI
Harrison PM, et al. Personality-dependent spatial ecology occurs independently from dispersal in wild burbot (Lota lota) Behav. Ecol. 2015;26:483–492. doi: 10.1093/beheco/aru216. DOI
Tardif SD, Power M, Oftedal OT, Power RA, Layne DG. Lactation, maternal behavior and infant growth in common marmoset monkeys (Callithrix jacchus): Effects of maternal size and litter size. Behav. Ecol. Sociobiol. 2001;51:17–25. doi: 10.1007/s002650100400. DOI
Mills DA, Windle CP, Baker HF, Ridley RM. Analysis of infant carrying in large, well-established family groups of captive marmosets (Callithrix jacchus) Primates. 2004;45:259–265. doi: 10.1007/s10329-004-0095-7. PubMed DOI
Leutenegger W. Maternal-fetal weight relationships in primates. Folia Primatol. 1973;20:280–293. doi: 10.1159/000155580. PubMed DOI
Schultz-Darken N, Ace L, Ash H. Behavior and behavioral management. In: Marini R, Wachtman L, Tardif S, Mansfield K, Fox J, editors. The Common Marmoset in Captivity and Biomedical Research. Academic Press; 2019. pp. 109–117.
Bardi M, Petto AJ. Parental failure in captive common marmosets (Callithrix jacchus): A comparison with tamarins. Folia Primatol. 2002;73:46–48. doi: 10.1159/000060418. PubMed DOI
Barbosa MN, da Silva Mota MT. Alloparental responsiveness to newborns by nonreproductive, adult male, common marmosets (Callithrix jacchus) Am. J. Primatol. 2013;75:145–152. doi: 10.1002/ajp.22092. PubMed DOI
Rutherford JN, et al. Womb to womb: Maternal litter size and birth weight but not adult characteristics predict early neonatal death of offspring in the common marmoset monkey. PLoS ONE. 2021;16:e0252093. doi: 10.1371/journal.pone.0252093. PubMed DOI PMC
Finkenwirth C, Martins E, Deschner T, Burkart JM. Oxytocin is associated with infant-care behavior and motivation in cooperatively breeding marmoset monkeys. Horm. Behav. 2016;80:10–18. doi: 10.1016/j.yhbeh.2016.01.008. PubMed DOI
Edwards HA, Dugdale HL, Richardson DS, Komdeur J, Burke T. Extra-pair parentage and personality in a cooperatively breeding bird. Behav. Ecol. Sociobiol. 2018;72:37. doi: 10.1007/s00265-018-2448-z. PubMed DOI PMC
Schürch R, Heg D. Variation in helper type affects group stability and reproductive decisions in a cooperative breeder. Ethology. 2010;116:257–269. doi: 10.1111/j.1439-0310.2009.01738.x. DOI
Class B, Dingemanse NJ. A variance partitioning perspective of assortative mating: Proximate mechanisms and evolutionary implications. J. Evol. Biol. 2022;35:483–490. doi: 10.1111/jeb.13998. PubMed DOI
Scherer U, Godin JGJ, Schuett W. Do female rainbow kribs choose males on the basis of their apparent aggression and boldness? A non-correlational mate choice study. Behav. Ecol. Sociobiol. 2020;74:34. doi: 10.1007/s00265-019-2794-5. DOI
Schuett W, Godin J-GJ, Dall SRX. Do female zebra finches, Taeniopygia guttata, choose their mates based on their ‘personality’? Ethology. 2011;117:908–917. doi: 10.1111/j.1439-0310.2011.01945.x. DOI
Ophir AG, Crino OL, Wilkerson QC, Wolff JO, Phelps SM. Female-directed aggression predicts paternal behavior, but female prairie voles prefer affiliative males to paternal males. Brain. Behav. Evol. 2008;71:32–40. doi: 10.1159/000108609. PubMed DOI
Lazaro-Perea C. Intergroup interactions in wild common marmosets, Callithrix jacchus: Territorial defence and assessment of neighbours. Anim. Behav. 2001;62:11–21. doi: 10.1006/anbe.2000.1726. DOI
Koski SE, Burkart JM. Common marmosets show social plasticity and group-level similarity in personality. Sci. Rep. 2015;5:8878. doi: 10.1038/srep08878. PubMed DOI PMC
Norman M, Rowden LJ, Cowlishaw G. Potential applications of personality assessments to the management of non-human primates: A review of 10 years of study. PeerJ. 2021;9:e12044. doi: 10.7717/peerj.12044. PubMed DOI PMC
Gorsuch RL. Factor Analysis. 2. Lawrence Erlbaum Associates; 1983.
R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (2020).
Bates D, Mächler M, Bolker BM, Walker SC. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. Mixed Effects Models and Extensions in Ecology with R. Springer; 2009.
Christensen, R. H. B. Ordinal—Regression Models for Ordinal Data. R package version 2019.4-25. (2019).
Burnham KP, Anderson DR. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer-Verlag; 2002.
Bartoń, K. Mu-MIn: Multi-model inference. R package version 2019 1.43.6. (2019).
Grueber CE, Nakagawa S, Laws RJ, Jamieson IG. Multimodel inference in ecology and evolution: Challenges and solutions. J. Evol. Biol. 2011;24:699–711. doi: 10.1111/j.1420-9101.2010.02210.x. PubMed DOI
Richards SA. Dealing with overdispersed count data in applied ecology. J. Appl. Ecol. 2008;45:218–227. doi: 10.1111/j.1365-2664.2007.01377.x. DOI
Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R package version 0.2.7 (2020).
Lüdecke, D. sjPlot: Data Visualization for Statistics in Social Science. R package version 2.8.2 (2020)
du Sert NP, et al. Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 2.0. PLoS Biol. 2020;18:e3000411. doi: 10.1371/journal.pbio.3000411. PubMed DOI PMC
Does the primate face cue personality?