Skip to main content
SpringerLink
Log in

Mating system as a possible driver of behavioral diversity in Peromyscus

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Identifying mechanisms underlying behavioral variation is important for understanding ecological and evolutionary processes. Comparative studies can help test hypotheses about the adaptive value of behaviors. Pace of life history and mating systems are broad factors hypothesized to drive species differences in behaviors. We tested these hypotheses using several Peromyscus species from lab stocks that varied in predicted life history and level of monogamy. We predicted that species with faster life histories would be more bold, active, and neophilic, and that these traits would also be positively correlated at the individual level. We further predicted that there would be greater sex differences in behaviors in non-monogamous, more sexually dimorphic species and that sociability would be more highly correlated with other behavioral traits in monogamous than in non-monogamous species. Counter to predictions, we found that larger stocks (with slower paces of life history) tended to be bolder, and that stock size was not associated with differences in activity, neophilia, or sociability. There was greater sexual differentiation in non-monogamous species in sociability, but not in other behaviors. Monogamous species were generally more sociable, and this was especially pronounced in male mice. Monogamous species showed a positive association between boldness and activity, while non-monogamous species showed a positive association between boldness and neophilia. A negative association between neophilia and sociability was stronger in species predicted to be monogamous. Thus, the pace-of-life-history syndrome hypothesis was not supported in this study, but mating system differences could help drive behavioral diversity.

Significance statement

Social system and pace of life history are two factors hypothesized to drive evolution of behavioral diversity, both between and within populations. We examined whether behavioral variation in several species of Peromyscus mice was associated with either of these factors. Larger species, with slower life histories, were potentially bolder. Monogamous species were generally more social (attracted to other individuals), especially when comparing males, and males and females differed more in this trait in non-monogamous species. The correlations among boldness, response to novelty, and sociability were also different between mating systems. These results do not support predictions from pace-of-life history hypotheses, but they suggest that the evolution of different mating systems is associated with systematic behavioral differences across these related species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abouheif E, Fairbairn DJ (1997) A comparative analysis of allometry for sexual size dimorphism: assessing Rensch’s rule. Am Nat 149:540–562

    Article  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. ArXiv E-Print arXiv:1406.5823

  • Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783

    Article  PubMed  PubMed Central  Google Scholar 

  • Bendesky A, Kwon Y-M, Lassance J-M, Lewarch CL, Yao S, Peterson BK, He MX, Dulac C, Hoekstra HE (2017) The genetic basis of parental care evolution in monogamous mice. Nature 544:434–439

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B Methodol 57:289–300

    Google Scholar 

  • Bergmüller R, Taborsky M (2010) Animal personality due to social niche specialisation. Trends Ecol Evol 25:504–511

    Article  PubMed  Google Scholar 

  • Bester-Meredith JK, Young LJ, Marler CA (1999) Species differences in paternal behavior and aggression in Peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm Behav 36:25–38

    Article  PubMed  CAS  Google Scholar 

  • Birdsall DA, Nash D (1973) Occurrence of successful multiple insemination of females in natural populations of deer mice (Peromyscus maniculatus). Evolution 27:106–110

    Article  PubMed  Google Scholar 

  • Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368

    Article  PubMed  Google Scholar 

  • Blanckenhorn WU (2005) Behavioral causes and consequences of sexual size dimorphism. Ethology 111:977–1016

    Article  Google Scholar 

  • Blomberg SP, Garland T Jr, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745

    Article  PubMed  Google Scholar 

  • Bolnick DI, Amarasekare P, Araújo MS, Bürger R, Levine JM, Novak M, Rudolf VHW, Schreiber SJ, Urban MC, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192

    Article  PubMed  PubMed Central  Google Scholar 

  • Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28

    Article  PubMed  Google Scholar 

  • Careau V, Bininda-Emonds ORP, Thomas DW, Réale D, Humphries MM (2009) Exploration strategies map along fast–slow metabolic and life-history continua in muroid rodents. Funct Ecol 23:150–156

    Article  Google Scholar 

  • Careau V, Réale D, Humphries MM, Thomas DW (2010) The pace of life under artificial selection: personality, energy expenditure, and longevity are correlated in domestic dogs. Am Nat 175:753–758

    Article  PubMed  Google Scholar 

  • Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117:641–653

    Article  Google Scholar 

  • Careau V, Thomas D, Pelletier F, Turki L, Landry F, Garant D, Réale D (2011) Genetic correlation between resting metabolic rate and exploratory behaviour in deer mice (Peromyscus maniculatus). J Evol Biol 24:2153–2163

    Article  PubMed  CAS  Google Scholar 

  • Crawley JN, Belknap JK, Collins A et al (1997) Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology 132:107–124

    Article  PubMed  CAS  Google Scholar 

  • Crispim-Junior CF, Pederiva CN, Bose RC, Garcia VA, Lino-de-Oliveira C, Marino-Neto J (2012) ETHOWATCHER: validation of a tool for behavioral and video-tracking analysis in laboratory animals. Comput Biol Med 42:257–264

    Article  PubMed  Google Scholar 

  • Debecker S, Sanmartín-Villar I, de Guinea-Luengo M, Cordero-Rivera A, Stoks R (2016) Integrating the pace-of-life syndrome across species, sexes and individuals: covariation of life history and personality under pesticide exposure. J Anim Ecol 85:726–738

    Article  PubMed  Google Scholar 

  • Dewey MJ, Dawson WD (2001) Deer mice: the Drosophila of North American mammalogy. Genesis 29:105–109

    Article  PubMed  CAS  Google Scholar 

  • Dewsbury DA (1981) An exercise in the prediction of monogamy in the field from laboratory data on 42 species of muroid rodents. Biologist 63:138–162

    Google Scholar 

  • Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54

    Article  PubMed  Google Scholar 

  • Dunn PO, Whittingham LA, Pitcher TE (2001) Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution 55:161–175

    Article  PubMed  CAS  Google Scholar 

  • Eisenberg JF (1963) The intraspecific social behavior of some Cricetine rodents of the genus Peromyscus. Am Midl Nat 69:240–246

    Article  Google Scholar 

  • Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    Article  PubMed  CAS  Google Scholar 

  • Fidler AE, van Oers K, Drent PJ, Kuhn S, Mueller JC, Kempenaers B (2007) Drd4 gene polymorphisms are associated with personality variation in a passerine bird. Proc R Soc Lond B 274:1685–1691

    Article  CAS  Google Scholar 

  • Foltz DW (1981) Genetic evidence for long-term monogamy in a small rodent, Peromyscus polionotus. Am Nat 117:665–675

    Article  Google Scholar 

  • Garamszegi LZ, Markó G, Herczeg G (2012) A meta-analysis of correlated behaviours with implications for behavioural syndromes: mean effect size, publication bias, phylogenetic effects and the role of mediator variables. Evol Ecol 26:1213–1235

    Article  Google Scholar 

  • Garamszegi LZ, Markó G, Herczeg G (2013) A meta-analysis of correlated behaviors with implications for behavioral syndromes: relationships between particular behavioral traits. Behav Ecol 24:1068–1080

    Article  Google Scholar 

  • Garamszegi LZ, Markó G, Szász E, Zsebők S, Azcárate M, Herczeg G, Török J (2015) Among-year variation in the repeatability, within- and between-individual, and phenotypic correlations of behaviors in a natural population. Behav Ecol Sociobiol 69:2005–2017

    Article  PubMed  PubMed Central  Google Scholar 

  • Glasper ER, DeVries AC (2005) Social structure influences effects of pair-housing on wound healing. Brain Behav Immun 19:61–68

    Article  PubMed  Google Scholar 

  • Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Holtmann B, Lagisz M, Nakagawa S (2017) Metabolic rates, and not hormone levels, are a likely mediator of between-individual differences in behaviour: a meta-analysis. Funct Ecol 31:685–696

    Article  Google Scholar 

  • Jašarević E, Williams SA, Roberts RM, Geary DC, Rosenfeld CS (2012) Spatial navigation strategies in Peromyscus: a comparative study. Anim Behav 84:1141–1149

    Article  PubMed  PubMed Central  Google Scholar 

  • Johansson F (2000) The slow—fast life style characteristics in a suite of six species of odonate larvae. Freshw Biol 43:149–159

    Article  Google Scholar 

  • Joyner CP, Myrick LC, Crossland JP, Dawson WD (1998) Deer mice as laboratory animals. ILAR J 39:322–330

    Article  PubMed  Google Scholar 

  • King JA (1968) Biology of Peromyscus (Rodentia). American Society of Mammalogists, Stillwater

    Book  Google Scholar 

  • Kirkland GL Jr, Layne JN (1989) Advances in the study of Peromyscus (Rodentia). Texas Tech University Press, Lubbock

    Google Scholar 

  • Kleiman DG (1977) Monogamy in mammals. Q Rev Biol 52:39–69

    Article  PubMed  CAS  Google Scholar 

  • Koolhaas JM, Korte SM, de Boer SF, van der Vegt BJ, van Reenen CG, Hopster H, de Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935

    Article  PubMed  CAS  Google Scholar 

  • Kuznetsova A, Bruun Brockhoff P, Haubo Bojesen Christensen R (2015) lmerTest: tests in linear mixed effects models. R package version 2.0–29, http://CRAN.R-project.org/package=lmerTest

  • Lukas D, Clutton-Brock TH (2013) The evolution of social monogamy in mammals. Science 341:526–530

    Article  PubMed  CAS  Google Scholar 

  • Martin LB, Hasselquist D, Wikelski M (2006) Investment in immune defense is linked to pace of life in house sparrows. Oecologia 147:565–575

    Article  PubMed  Google Scholar 

  • Martin LBII, Weil ZM, Nelson RJ (2007) Immune defense and reproductive pace of life in Peromyscus mice. Ecology 88:2516–2528

    Article  PubMed  Google Scholar 

  • Mock DW, Fujioka M (1990) Monogamy and long-term pair bonding in vertebrates. Trends Ecol Evol 5:39–43

    Article  PubMed  CAS  Google Scholar 

  • Modi WS (1984) Reproductive tactics among deer mice of the genus Peromyscus. Can J Zool 62:2576–2581

    Article  Google Scholar 

  • Montiglio P-O, Ferrari C, Réale D (2013) Social niche specialization under constraints: personality, social interactions and environmental heterogeneity. Philos Trans R Soc B 368:20120343

    Article  Google Scholar 

  • Munafò MR, Yalcin B, Willis-Owen SA, Flint J (2008) Association of the dopamine D4 receptor (DRD4) gene and approach-related personality traits: meta-analysis and new data. Biol Psychiatry 63:197–206

    Article  PubMed  CAS  Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    Article  PubMed  CAS  Google Scholar 

  • Pruitt JN, Oufiero CE, Avilés L, Riechert SE (2012) Iterative evolution of increased behavioral variation characterizes the transition to sociality in spiders and proves advantageous. Am Nat 180:496–510

    Article  PubMed  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org/

    Google Scholar 

  • Réale D, Dingemanse NJ (2010) Personality and individuals social specialisation. In: Székely T, Moore AJ, Komdeur J (eds) Social behaviour: genes, ecology and evolution. Cambridge University Press, Cambridge, pp 417–441

    Chapter  Google Scholar 

  • Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio P-O (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos Trans R Soc B 365:4051–4063

    Article  Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    Article  PubMed  Google Scholar 

  • Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Article  Google Scholar 

  • Ribble DO (1991) The monogamous mating system of Peromyscus californicus as revealed by DNA fingerprinting. Behav Ecol Sociobiol 29:161–166

    Article  Google Scholar 

  • Ribble DO (2003) The evolution of social and reproductive monogamy in Peromyscus, evidence from Peromyscus californicus (the California mouse). In: Riechard U, Boesh C (eds) Monogamy: mating strategies and partnerships in birds, humans, and other mammals. Cambridge University Press, Cambridge, pp 81–92

    Chapter  Google Scholar 

  • Ribble DO, Salvioni M (1990) Social organization and nest co-occupancy in Peromyscus californicus, a monogamous rodent. Behav Ecol Sociobiol 26:9–15

    Article  Google Scholar 

  • Ricklefs RE, Wikelski M (2002) The physiology/life history nexus. Trends Ecol Evol 17:462–468

    Article  Google Scholar 

  • Sachser N, Kaiser S, Hennessy MB (2013) Behavioural profiles are shaped by social experience: when, how and why. Philos Trans R Soc B 368:20120344

    Article  CAS  Google Scholar 

  • Schuett W, Tregenza T, Dall SRX (2010) Sexual selection and animal personality. Biol Rev 85:217–246

    Article  PubMed  Google Scholar 

  • Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277

    Article  PubMed  Google Scholar 

  • Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289

    Article  PubMed  Google Scholar 

  • Shorter KR, Anderson V, Cakora P, Owen A, Lo K, Crossland J, South ACH, Felder MR, Vrana PB (2014a) Pleiotropic effects of a methyl donor diet in a novel animal model. PLoS One 9:e104942

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shorter KR, Owen A, Anderson V et al (2014b) Natural genetic variation underlying differences in Peromyscus repetitive and social/aggressive behaviors. Behav Genet 44:126–135

    Article  PubMed  PubMed Central  Google Scholar 

  • Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, Princeton

    Google Scholar 

  • Smith BR, Blumstein DT (2008) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455

    Article  Google Scholar 

  • Stamps J, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325

    Article  PubMed  Google Scholar 

  • Stamps JA (2007) Growth-mortality tradeoffs and “personality traits” in animals. Ecol Lett 10:355–363

    Article  PubMed  Google Scholar 

  • Tieleman BI, Williams JB, Ricklefs RE, Klasing KC (2005) Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proc R Soc Lond B 272:1715–1720

    Article  Google Scholar 

  • Trainor BC, Finy MS, Nelson RJ (2008) Paternal aggression in a biparental mouse: parallels with maternal aggression. Horm Behav 53:200–207

    Article  PubMed  Google Scholar 

  • Trainor BC, Marler CA (2001) Testosterone, paternal behavior, and aggression in the monogamous California mouse (Peromyscus californicus). Horm Behav 40:32–42

    Article  PubMed  CAS  Google Scholar 

  • Vessey SH, Vessey KB (2007) Linking behavior, life history and food supply with the population dynamics of white-footed mice (Peromyscus leucopus). Integr Zool 2:123–130

    Article  PubMed  Google Scholar 

  • von Merten S, Zwolak R, Rychlik L (2017) Social personality: a more social shrew species exhibits stronger differences in personality types. Anim Behav 127:125–134

    Article  Google Scholar 

  • Vrana PB, Shorter KR, Szalai G et al (2014) Peromyscus (deer mice) as developmental models. WIRES Dev Biol 3:211–230

    Article  Google Scholar 

  • Weber JN, Hoekstra HE (2009) The evolution of burrowing behaviour in deer mice (genus Peromyscus). Anim Behav 77:603–609

    Article  Google Scholar 

  • Weber JN, Peterson BK, Hoekstra HE (2013) Discrete genetic modules are responsible for complex burrow evolution in Peromyscus mice. Nature 493:402–405

    Article  PubMed  CAS  Google Scholar 

  • Whitehead H (2008) Analyzing animal societies. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Wikelski M, Spinney L, Schelsky W, Scheuerlein A, Gwinner E (2003) Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes. Proc R Soc Lond B 270:2383–2388

    Article  Google Scholar 

  • Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461

    Article  PubMed  Google Scholar 

  • Wolff JO (1989) Social behavior. In: Kirkland GL Jr, Layne JN (eds) Advances in the study of Peromyscus (Rodentia). Texas Tech University Press, Lubbock, pp 271–291

    Google Scholar 

  • Wolff JO, Sherman PW (eds) (2007) Rodent societies. The University of Chicago Press, Chicago

  • Xia X, Millar JS (1991) Genetic evidence of promiscuity in Peromyscus leucopus. Behav Ecol Sociobiol 28:171–178

    Article  Google Scholar 

Download references

Acknowledgments

We thank Janet Crossland, Michael Felder, Kimberly Shorter, and Rebecca Kelley for help at the PGSC, and A. J. Saunders for help scoring videos. We thank Pierre-Olivier Montiglio for feedback on statistical analysis. We are also grateful to two anonymous reviewers who provided constructive input on earlier versions of this manuscript.

Funding

This work was funded by NSF IOS-1149056 to KEM.

Author information

Author notes

  1. Tina W. Wey

    Present address: Université de Sherbrooke, Sherbrooke, QC, Canada

Authors and Affiliations

  1. Department of Biology, New Mexico State University, Las Cruces, NM, USA

    Tina W. Wey & Karen E. Mabry

  2. Peromyscus Genetic Stock Center, Department of Biological Sciences, University of South Carolina, Columbia, SC, USA

    Paul B. Vrana

  3. Zymo Research Corp, Irvine, CA, USA

    Paul B. Vrana

Authors
  1. Tina W. Wey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul B. Vrana
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karen E. Mabry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tina W. Wey.

Ethics declarations

Ethical note

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All procedures were approved by the University of South Carolina Institutional Animal Care and Use Committee (protocol #1809-100340-061011).

Conflict of interest

The authors declare that they have no conflict of interest.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Additional information

Communicated by C. Soulsbury

Electronic Supplementary Material

Fig. S1

Graphical representations of phenotypic correlations among behaviors for (a) monogamous stocks and (b) non-monogamous stocks. Positive correlations are in blue, and negative correlations are in red. Stronger correlations are indicated by darker color (PDF 6 kb)

(PDF 6 kb)

Video S1

Example of latency to emerge and activity in open field test (MP4 1075 kb)

Video S2

Example of novel and social stimulus test (MP4 1331 kb)

Appendix 1 Wild-type stock information and supplemental methods

Appendix 1 Wild-type stock information and supplemental methods

(Table 5)

Table 5 Source populations of Peromyscus wild-type stocks
Full size table

Methods A1 Additional information on use of body mass as a proxy for pace of life history.

Modi (1984) compared growth and reproductive measures across 18 Peromyscus species and subspecies, including all species represented in this study (see “Methods”), to test expectations from life history theory. He found a strong positive correlation between adult mass and a standard index of overall development time—age at eye opening (r = 0.838, p < 0.001), a strong negative correlation between adult mass and litter mass relative to adult mass (r = −0.820, p < 0.001), and a moderate negative correlation between adult mass and relative birth mass (r = − 0.620, p < 0.05). Overall this indicated that, across Peromyscus species, body mass is moderately to strongly correlated with several developmental traits, in a direction consistent with larger species having slower life histories.

The complete list of traits studied in Modi (1984) is: adult mass, relative birth mass, litter size, relative mass of the conceptus (litter size × birth mass / adult mass), age at eye opening, gestation period while lactating, age at weaning, growth rate (weaning mass − birth mass / age at weaning), and age at first estrous.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wey, T.W., Vrana, P.B. & Mabry, K.E. Mating system as a possible driver of behavioral diversity in Peromyscus . Behav Ecol Sociobiol 71, 163 (2017). https://doi.org/10.1007/s00265-017-2392-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-017-2392-3

Keywords

Search

Navigation