Skip to main content
SpringerLink
Log in

Sex pheromone levels are associated with paternity rate in brown rats

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

Abstract

In muroid rodents, urine-borne volatile compounds and major urinary proteins (MUPs) constitute the key male pheromones that shape the sexual attractiveness of males. Here, we aimed to examine whether male pheromone levels were related to sexual attractiveness and reproductive success in the North China subspecies of the brown rat (Rattus norvegicus humiliatus). According to the abundance of 2-heptanone (2H), the predominant male pheromone in male urine, male rats were first categorized into a high-2H group and a low-2H group. The levels of the whole volatile profile and non-volatile MUPs were found to be higher in the high-2H group than in the low-2H group. Moreover, the abundances of urinary volatile pheromones or pheromone candidates were positively correlated with the abundance of total MUPs. Two-way choice tests revealed that male urine from the high-2H group was more attractive to females than that from the low-2H group. Microsatellite loci analysis of paternal lineage revealed that the females had single-paternity offspring and that the high-2H group sired more offspring and had higher rates of paternity than did the low-2H group. These results suggest that urine-borne volatile pheromones alone or together with MUP pheromones can predict sexual attractiveness and reproductive success in male rats.

Significance statement

Sexual attractiveness can be quantified using volatile and MUP pheromones and their candidates in deposited urine. 2-Heptanone (a major pheromone) and other urine-borne volatile pheromones or their candidates and total MUPs showed the same difference patterns in males and predicted male sexual attractiveness. The abundances of volatile pheromones or their candidates and total MUPs were associated with reproductive success and paternity rate in males.

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
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability statements

All data generated or analyzed during this study are included in this published article.

References

  • Amo L, Aviles JM, Parejo D, Pena A, Rodriguez J, Tomas G (2012) Sex recognition by odour and variation in the uropygial gland secretion in starlings. J Anim Ecol 81:605–613

    Article  Google Scholar 

  • Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302

    Article  Google Scholar 

  • Armstrong SD, Robertson DH, Cheetham SA, Hurst JL, Beynon RJ (2005) Structural and functional differences in isoforms of mouse major urinary proteins: a male-specific protein that preferentially binds a male pheromone. Biochem J 391:343–350

    Article  CAS  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Berdoy M, Drickamer LC (2007) Comparative social organization and life history of Rattus and Mus. In: Wolff J, Sherman P (eds) Rodent societies: an ecological and evolutionary perspective. University of Chicago Press, Chicago, pp 380–393

    Google Scholar 

  • Brooks R (2000) Negative genetic correlation between male sexual attractiveness and survival. Nature 406:67–70

    Article  CAS  Google Scholar 

  • Calzada-Garcia JA, Gonzalez MNP, BenitoAndres FJ, Garcia LJM, Cabezas JA, SanchezBernal C (1996) Evaluation of patterns of urinary proteins by SDS-PAGE in rats of different ages. Mech Ageing Dev 87:1–13

    Article  CAS  Google Scholar 

  • Costa F, Richardson JL, Dion K, Mariani C, Pertile AC, Burak MK, Childs JE, Ko AI, Caccone A (2016) Multiple paternity in the Norway rat, Rattus norvegicus, from urban slums in Salvador, Brazil. J Hered 107:181–186

    Article  Google Scholar 

  • Dewsbury DA (1990) Fathers and sons—genetic-factors and social-dominance in deer mice, peromyscus-maniculatus. Anim Behav 39:284–289

    Article  Google Scholar 

  • Drickamer LC, Gowaty PA, Holmes CM (2000) Free female mate choice in house mice affects reproductive success and offspring viability and performance. Anim Behav 59:371–378

    Article  CAS  Google Scholar 

  • Fang Q, Zhang YH, Shi YL, Zhang JH, Zhang JX (2016) Individuality and transgenerational inheritance of social dominance and sex pheromones in isogenic male mice. J Exp Zool B 326:225–236

    Article  CAS  Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Article  Google Scholar 

  • Gómez-Baena G, Armstrong SD, Phelan MM, Hurst JL, Beynon RJ (2014) The major urinary protein system in the rat. Biochem Soc Trans 42:886–892

    Article  Google Scholar 

  • Guo H, Fang Q, Huo Y, Zhang Y, Zhang J (2015) Social dominance-related major urinary proteins and the regulatory mechanism in mice. Integr Zool 10:543–554

    Article  Google Scholar 

  • Guo HL (2016) Interspecific chemical signals and behavioral interactions between Rattus tanezumi and R. norvegicus. Master Dissertation, University of Chinese Academy of Sciences, Chinese Academy of Sciences

  • Guo X, Guo H, Zhao L, Zhang YH, Zhang JX (2018) Two predominant MUPs, OBP3 and MUP13, are male pheromones in rats. Front Zool 15:6

    Article  Google Scholar 

  • Hinson ER, Hannah MF, Norris DE, Glass GE, Klein SL (2006) Social status does not predict responses to Seoul virus infection or reproductive success among male Norway rats. Brain Behav Immun 20:182–190

    Article  Google Scholar 

  • Hosken DJ, Taylor ML, Hoyle K, Higgins S, Wedell N (2008) Attractive males have greater success in sperm competition. Curr Biol 18:R553–R554

    Article  CAS  Google Scholar 

  • Hunt J, Breuker CJ, Sadowski JA, Moore AJ (2009) Male-male competition, female mate choice and their interaction: determining total sexual selection. J Evol Biol 22:13–26

    Article  Google Scholar 

  • Ilayaraja R, Rajkumar R, Rajesh D, Muralidharan AR, Padmanabhan P, Archunan G (2014) Evaluating the binding efficiency of pheromone binding protein with its natural ligand using molecular docking and fluorescence analysis. Sci Rep 4:5201

    Article  CAS  Google Scholar 

  • Ingleby FC, Hunt J, Hosken DJ (2013) Heritability of male attractiveness persists despite evidence for unreliable sexual signals in Drosophila simulans. J Evol Biol 26:311–324

    Article  CAS  Google Scholar 

  • Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82:265–289

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  Google Scholar 

  • Kortet R, Hedrick A (2005) The scent of dominance: female field crickets use odour to predict the outcome of male competition. Behav Ecol Sociobiol 59:77–83

    Article  Google Scholar 

  • Kumar V, Vasudevan A, Soh LJT, Le Min C, Vyas A, Zewail-Foote M, Guarraci FA (2014) Sexual attractiveness in male rats is associated with greater concentration of major urinary proteins. Biol Reprod 91:150

    PubMed  Google Scholar 

  • Lanuza E, Martin-Sanchez A, Marco-Manclus P, Cadiz-Moretti B, Fortes-Marco L, Hernandez-Martinez A, McLean L, Beynon RJ, Hurst JL, Martinez-Garcia F (2014) Sex pheromones are not always attractive: changes induced by learning and illness in mice. Anim Behav 97:265–272

    Article  Google Scholar 

  • Lee W, Khan A, Curley JP (2017) Major urinary protein levels are associated with social status and context in mouse social hierarchies. Proc R Soc B 284:20171570

    Article  Google Scholar 

  • Lopes PC, König B (2016) Choosing a healthy mate: sexually attractive traits as reliable indicators of current disease status in house mice. Anim Behav 111:119–126

    Article  Google Scholar 

  • Lovell JL, Diehl A, Joyce E, Cohn J, Lopez J, Guarraci FA (2007) “Some guys have all the luck”: mate preference influences paced-mating behavior in female rats. Physiol Behav 90:537–544

    Article  CAS  Google Scholar 

  • Marcondes F, Bianchi F, Tanno A (2002) Determination of the estrous cycle phases of rats: some helpful considerations. Braz J Biol 62:609–614

    Article  CAS  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  CAS  Google Scholar 

  • Møller AP (2017) Experimental manipulation of size and shape of tail spots and sexual selection in barn swallows. Curr Zool 63:569–572

    PubMed  Google Scholar 

  • Musser GG, Carleton MD (2005) Superfamily Muroidea. In: Wilson DE, Reeder DM (eds) Mammal species of the world a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore, pp 894–1531

    Google Scholar 

  • Nelson AC, Cauceglia JW, Merkley SD, Youngson NA, Oler AJ, Nelson RJ, Cairns BR, Whitelaw E, Potts WK (2013) Reintroducing domesticated wild mice to sociality induces adaptive transgenerational effects on MUP expression. P Natl Acad Sci USA 110:19848–19853

    Article  CAS  Google Scholar 

  • Nelson AC, Cunningham CB, Ruff JS, Potts WK (2015) Protein pheromone expression levels predict and respond to the formation of social dominance networks. J Evol Biol 28:1213–1224

    Article  CAS  Google Scholar 

  • Novotny M, Harvey S, Jemiolo B (1990) Chemistry of male dominance in the house mouse, Mus domesticus. Experientia 46:109–113

    Article  CAS  Google Scholar 

  • Papes F, Logan DW, Stowers L (2010) The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 141:692–703

    Article  CAS  Google Scholar 

  • Penn D, Potts W (1998a) MHC-disassortative mating preferences reversed by cross-fostering. Proc R Soc Lond B 265:1299–1306

    Article  CAS  Google Scholar 

  • Penn D, Potts WK (1998b) Chemical signals and parasite-mediated sexual selection. Trends Ecol Evol 13:391–396

    Article  CAS  Google Scholar 

  • Qvarnstrom A, Forsgren E (1998) Should females prefer dominant males? Trends Ecol Evol 13:498–501

    Article  CAS  Google Scholar 

  • Rantala MJ, Jokinen I, Kortet R, Vainikka A, Suhonen J (2002) Do pheromones reveal male immunocompetence? Proc R Soc Lond B 269:1681–1685

    Article  Google Scholar 

  • Roberts SA, Simpson DM, Armstrong SD, Davidson AJ, Robertson DH, McLean L, Beynon RJ, Hurst JL (2010) Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male's odour. BMC Biol 8:75

    Article  Google Scholar 

  • Roberts SC, Gosling LM (2003) Genetic similarity and quality interact in mate choice decisions by female mice. Nat Genet 35:103–106

    Article  CAS  Google Scholar 

  • Scheuber H, Jacot A, Brinkhof MWG (2003) Condition dependence of a multicomponent sexual signal in the field cricket Gryllus campestris. Anim Behav 65:721–727

    Article  Google Scholar 

  • Shimmin GA, Sofronidis G, Bowden DK, Temple-Smith PD (1995) DNA fingerprinting to determine paternity in laboratory rat sperm competition experiments. Electrophoresis 16:1627–1632

    Article  CAS  Google Scholar 

  • Simmons LW, Thomas ML, Simmons FW, Zuk M (2013) Female preferences for acoustic and olfactory signals during courtship: male crickets send multiple messages. Behav Ecol 24:1099–1107

    Article  Google Scholar 

  • Szulkin M, Stopher KV, Pemberton JM, Reid JM (2013) Inbreeding avoidance, tolerance, or preference in animals? Trends Ecol Evol 28:205–211

    Article  Google Scholar 

  • Takacs S, Gries R, Zhai HM, Gries G (2016) The sex attractant pheromone of male brown rats: identification and field experiment. Angew Chem Int Ed 55:6062–6066

    Article  CAS  Google Scholar 

  • Taylor ML, Wedell N, Hosken DJ (2007) The heritability of attractiveness. Curr Biol 17:R959–R960

    Article  CAS  Google Scholar 

  • Teng HJ, Zhang YH, Shi CM, Mao FB, Cai WS, Lu L, Zhao FQ, Sun ZS, Zhang JX (2017) Population genomics reveals speciation and introgression between brown Norway rats and their sibling species. Mol Biol Evol 34:2214–2228

    Article  CAS  Google Scholar 

  • Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027

    Article  CAS  Google Scholar 

  • Wang YX (2003) A complete checklists of mammal species and subspecies in China. China Forestry Publishing House, Beijing

    Google Scholar 

  • Wedell N, Tregenza T (1999) Successful fathers sire successful sons. Evolution 53:620–625

    Article  CAS  Google Scholar 

  • Whittaker DJ, Soini HA, Atwell JW, Hollars C, Novotny MV, Ketterson ED (2010) Songbird chemosignals: volatile compounds in preen gland secretions vary among individuals, sexes, and populations. Behav Ecol 21:608–614

    Article  Google Scholar 

  • Winland C, Bolton JL, Ford B, Jampana S, Tinker J, Frohardt RJ, Guarraci FA, Zewail-Foote M (2012) “Nice guys finish last”: influence of mate choice on reproductive success in Long Evans rats. Physiol Behav 105:868–876

    Article  CAS  Google Scholar 

  • Wu DL (1982) Subspecies of the brown rat (Rattus norvegicus Berkenhout) in China. Acta Theriol Sin 2:107–112

    Google Scholar 

  • Wyatt T (2014) Pheromones and animal behavior: chemical signals and signatures. Cambridge University Press, Cambridge

    Google Scholar 

  • Zewail-Foote M, Diehl A, Benson A, Lee KH, Guarraci FA (2009) Reproductive success and mate choice in Long-Evans rats. Physiol Behav 96:98–103

    Article  CAS  Google Scholar 

  • Zhang JX, Sun L, Zhang YH (2010) Foxn1 gene knockout suppresses sexual attractiveness and pheromonal components of male urine in inbred mice. Chem Senses 35:47–56

    Article  CAS  Google Scholar 

  • Zhang JX, Sun LX, Zhang JH, Feng ZY (2008) Sex- and gonad-affecting scent compounds and 3 male pheromones in the rat. Chem Senses 33:611–621

    Article  CAS  Google Scholar 

  • Zhang YH, Du YF, Zhang JX (2013) Uropygial gland volatiles facilitate species recognition between two sympatric sibling bird species. Behav Ecol 24:1271–1278

    Article  CAS  Google Scholar 

  • Zhang YH, Liang HC, Guo HL, Zhang JX (2016) Exaggerated male pheromones in rats may increase predation cost. Curr Zool 62:431–437

    Article  Google Scholar 

  • Zhang YH, Zhang JX (2011) Urine-derived key volatiles may signal genetic relatedness in male rats. Chem Senses 36:125–135

    Article  CAS  Google Scholar 

  • Zhang YH, Zhang JX (2014) A male pheromone-mediated trade-off between female preferences for genetic compatibility and sexual attractiveness in rats. Front Zool 11:73

    Article  Google Scholar 

Download references

Acknowledgments

We thank the editors and the two anonymous reviewers for their constructive comments and suggestions, which helped to improve this manuscript.

Funding

This work was supported by grants from the Strategic Priority Research Program of the Chinese Academy of Sciences (grant number XDB11010400 to JXZ), and the National Natural Science Foundation of China (grant number 31672306 to YHZ and 31572277 to JXZ).

Author information

Author notes

  1. Yao-Hua Zhang and Lei Zhao contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Integrated Management of Pest Insects and Rodents in Agriculture, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road 1-5, Chaoyang District, Beijing, 100101, China

    Yao-Hua Zhang, Lei Zhao, Xiao Guo, Jin-Hua Zhang & Jian-Xu Zhang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Lei Zhao & Xiao Guo

Authors
  1. Yao-Hua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiao Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jin-Hua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jian-Xu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JXZ and YHZ conceived and designed the experiments. YHZ and JHZ performed the behavioral experiments and GC-MS analysis. LZ analyzed the paternity. LZ and XG performed the SDS-PAGE analysis. YHZ, LZ and JXZ wrote the paper. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Jian-Xu Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

The procedures for animal care and use were performed in strict accordance with the guidelines of the Animal Use Committee of the Institute of Zoology, Chinese Academy of Sciences (IOZ 2015) and were approved by the Animal Use Committee of the Institute of Zoology, Chinese Academy of Sciences. Information regarding the animals’ origin and housing conditions are described above. Handling and experimental monitoring were conducted in a manner aimed at reducing stress and maximizing animal welfare.

Additional information

Communicated by A. I. Schulte-Hostedde

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, YH., Zhao, L., Guo, X. et al. Sex pheromone levels are associated with paternity rate in brown rats. Behav Ecol Sociobiol 73, 15 (2019). https://doi.org/10.1007/s00265-018-2627-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-018-2627-y

Keywords

Search

Navigation