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Sex pheromone levels are associated with paternity rate in brown rats

  • Yao-Hua Zhang
  • Lei Zhao
  • Xiao Guo
  • Jin-Hua Zhang
  • Jian-Xu ZhangEmail author
Original Article

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.

Keywords

Pheromone MUP Sexual attractiveness Paternity 

Notes

Acknowledgments

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

Author contribution

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.

Funding information

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).

Compliance with ethical standards

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.

References

  1. 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 81:605–613PubMedCrossRefGoogle Scholar
  2. Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302PubMedCrossRefGoogle Scholar
  3. 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 391:343–350PubMedPubMedCentralCrossRefGoogle Scholar
  4. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188CrossRefGoogle Scholar
  5. 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 380–393Google Scholar
  6. Brooks R (2000) Negative genetic correlation between male sexual attractiveness and survival. Nature 406:67–70PubMedCrossRefGoogle Scholar
  7. 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 87:1–13PubMedCrossRefGoogle Scholar
  8. 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 107:181–186PubMedPubMedCentralCrossRefGoogle Scholar
  9. Dewsbury DA (1990) Fathers and sons—genetic-factors and social-dominance in deer mice, peromyscus-maniculatus. Anim Behav 39:284–289CrossRefGoogle Scholar
  10. Drickamer LC, Gowaty PA, Holmes CM (2000) Free female mate choice in house mice affects reproductive success and offspring viability and performance. Anim Behav 59:371–378PubMedCrossRefGoogle Scholar
  11. 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 326:225–236CrossRefGoogle Scholar
  12. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  13. Gómez-Baena G, Armstrong SD, Phelan MM, Hurst JL, Beynon RJ (2014) The major urinary protein system in the rat. Biochem Soc Trans 42:886–892PubMedCrossRefGoogle Scholar
  14. 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 10:543–554PubMedCrossRefGoogle Scholar
  15. 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 SciencesGoogle Scholar
  16. Guo X, Guo H, Zhao L, Zhang YH, Zhang JX (2018) Two predominant MUPs, OBP3 and MUP13, are male pheromones in rats. Front Zool 15:6PubMedPubMedCentralCrossRefGoogle Scholar
  17. 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 20:182–190PubMedCrossRefGoogle Scholar
  18. Hosken DJ, Taylor ML, Hoyle K, Higgins S, Wedell N (2008) Attractive males have greater success in sperm competition. Curr Biol 18:R553–R554PubMedCrossRefGoogle Scholar
  19. 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 22:13–26PubMedCrossRefGoogle Scholar
  20. 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 4:5201PubMedPubMedCentralCrossRefGoogle Scholar
  21. Ingleby FC, Hunt J, Hosken DJ (2013) Heritability of male attractiveness persists despite evidence for unreliable sexual signals in Drosophila simulans. J Evol Biol 26:311–324PubMedCrossRefGoogle Scholar
  22. Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82:265–289PubMedCrossRefGoogle Scholar
  23. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106PubMedCrossRefGoogle Scholar
  24. Kortet R, Hedrick A (2005) The scent of dominance: female field crickets use odour to predict the outcome of male competition. Behav Ecol Sociobiol 59:77–83CrossRefGoogle Scholar
  25. 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 91:150PubMedGoogle Scholar
  26. 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 97:265–272CrossRefGoogle Scholar
  27. 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 284:20171570PubMedCrossRefGoogle Scholar
  28. Lopes PC, König B (2016) Choosing a healthy mate: sexually attractive traits as reliable indicators of current disease status in house mice. Anim Behav 111:119–126CrossRefGoogle Scholar
  29. 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 90:537–544PubMedCrossRefGoogle Scholar
  30. Marcondes F, Bianchi F, Tanno A (2002) Determination of the estrous cycle phases of rats: some helpful considerations. Braz J Biol 62:609–614PubMedCrossRefGoogle Scholar
  31. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedCrossRefGoogle Scholar
  32. Møller AP (2017) Experimental manipulation of size and shape of tail spots and sexual selection in barn swallows. Curr Zool 63:569–572PubMedGoogle Scholar
  33. 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 894–1531Google Scholar
  34. 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 110:19848–19853CrossRefGoogle Scholar
  35. 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 28:1213–1224PubMedPubMedCentralCrossRefGoogle Scholar
  36. Novotny M, Harvey S, Jemiolo B (1990) Chemistry of male dominance in the house mouse, Mus domesticus. Experientia 46:109–113PubMedCrossRefGoogle Scholar
  37. Papes F, Logan DW, Stowers L (2010) The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 141:692–703PubMedPubMedCentralCrossRefGoogle Scholar
  38. Penn D, Potts W (1998a) MHC-disassortative mating preferences reversed by cross-fostering. Proc R Soc Lond B 265:1299–1306CrossRefGoogle Scholar
  39. Penn D, Potts WK (1998b) Chemical signals and parasite-mediated sexual selection. Trends Ecol Evol 13:391–396PubMedCrossRefGoogle Scholar
  40. Qvarnstrom A, Forsgren E (1998) Should females prefer dominant males? Trends Ecol Evol 13:498–501PubMedCrossRefGoogle Scholar
  41. Rantala MJ, Jokinen I, Kortet R, Vainikka A, Suhonen J (2002) Do pheromones reveal male immunocompetence? Proc R Soc Lond B 269:1681–1685CrossRefGoogle Scholar
  42. 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 8:75PubMedPubMedCentralCrossRefGoogle Scholar
  43. Roberts SC, Gosling LM (2003) Genetic similarity and quality interact in mate choice decisions by female mice. Nat Genet 35:103–106PubMedCrossRefGoogle Scholar
  44. Scheuber H, Jacot A, Brinkhof MWG (2003) Condition dependence of a multicomponent sexual signal in the field cricket Gryllus campestris. Anim Behav 65:721–727CrossRefGoogle Scholar
  45. Shimmin GA, Sofronidis G, Bowden DK, Temple-Smith PD (1995) DNA fingerprinting to determine paternity in laboratory rat sperm competition experiments. Electrophoresis 16:1627–1632PubMedCrossRefGoogle Scholar
  46. 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 24:1099–1107CrossRefGoogle Scholar
  47. Szulkin M, Stopher KV, Pemberton JM, Reid JM (2013) Inbreeding avoidance, tolerance, or preference in animals? Trends Ecol Evol 28:205–211PubMedCrossRefGoogle Scholar
  48. 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 55:6062–6066CrossRefGoogle Scholar
  49. Taylor ML, Wedell N, Hosken DJ (2007) The heritability of attractiveness. Curr Biol 17:R959–R960PubMedCrossRefGoogle Scholar
  50. 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 34:2214–2228PubMedPubMedCentralCrossRefGoogle Scholar
  51. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027PubMedCrossRefGoogle Scholar
  52. Wang YX (2003) A complete checklists of mammal species and subspecies in China. China Forestry Publishing House, BeijingGoogle Scholar
  53. Wedell N, Tregenza T (1999) Successful fathers sire successful sons. Evolution 53:620–625PubMedCrossRefGoogle Scholar
  54. 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 21:608–614PubMedPubMedCentralCrossRefGoogle Scholar
  55. 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 105:868–876PubMedCrossRefGoogle Scholar
  56. Wu DL (1982) Subspecies of the brown rat (Rattus norvegicus Berkenhout) in China. Acta Theriol Sin 2:107–112Google Scholar
  57. Wyatt T (2014) Pheromones and animal behavior: chemical signals and signatures. Cambridge University Press, CambridgeGoogle Scholar
  58. Zewail-Foote M, Diehl A, Benson A, Lee KH, Guarraci FA (2009) Reproductive success and mate choice in Long-Evans rats. Physiol Behav 96:98–103PubMedCrossRefGoogle Scholar
  59. Zhang JX, Sun L, Zhang YH (2010) Foxn1 gene knockout suppresses sexual attractiveness and pheromonal components of male urine in inbred mice. Chem Senses 35:47–56PubMedCrossRefGoogle Scholar
  60. Zhang JX, Sun LX, Zhang JH, Feng ZY (2008) Sex- and gonad-affecting scent compounds and 3 male pheromones in the rat. Chem Senses 33:611–621PubMedPubMedCentralCrossRefGoogle Scholar
  61. Zhang YH, Du YF, Zhang JX (2013) Uropygial gland volatiles facilitate species recognition between two sympatric sibling bird species. Behav Ecol 24:1271–1278CrossRefGoogle Scholar
  62. Zhang YH, Liang HC, Guo HL, Zhang JX (2016) Exaggerated male pheromones in rats may increase predation cost. Curr Zool 62:431–437PubMedPubMedCentralCrossRefGoogle Scholar
  63. Zhang YH, Zhang JX (2011) Urine-derived key volatiles may signal genetic relatedness in male rats. Chem Senses 36:125–135PubMedCrossRefGoogle Scholar
  64. Zhang YH, Zhang JX (2014) A male pheromone-mediated trade-off between female preferences for genetic compatibility and sexual attractiveness in rats. Front Zool 11:73CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yao-Hua Zhang
    • 1
  • Lei Zhao
    • 1
    • 2
  • Xiao Guo
    • 1
    • 2
  • Jin-Hua Zhang
    • 1
  • Jian-Xu Zhang
    • 1
    Email author
  1. 1.State Key Laboratory of Integrated Management of Pest Insects and Rodents in Agriculture, Institute of ZoologyChinese Academy of SciencesBeijingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina

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