Skip to main content
SpringerLink
Log in

Varying levels of female promiscuity in four Apodemus mice species

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

Abstract

Sexual selection in most vertebrates is based on the evolution of fitness optimization strategies such as multiple-male mating (MMM). Several ecological correlates of MMM have been identified in bird and fish populations; however, only few studies have documented the effects of environmental change on promiscuity in mammals. In this study, the 127 pregnant females from four central European and ecologically diverse species of field mice (genus Apodemus) were studied to assess the role of ecological factors that may have shaped the evolution of particular mating systems. MMM was found in all analyzed species: in Apodemus uralensis and Apodemus flavicollis, up to two males could be identified as the fathers of a particular litter, while three males sired 9.1% of analyzed litters of Apodemus sylvaticus and 20.6% of Apodemus agrarius. Furthermore, there were obvious differences between species in relative testes size and the proportion of multiple sired litters during those seasons when the opportunity for multiple mating was high. The species with the smallest testes and the least promiscuous was A. uralensis (only 43.5% of multiple sired litters), while the species with the biggest testes and the most promiscuous was A. agrarius (69.2%). MMM was significantly associated with higher litter size in A. flavicollis, and the probability of MMM strongly increased with season in A. agrarius and with abundance in A. uralensis. These results indicate that ecological factors are associated with MMM rates in Apodemus field mice and more research is needed to fully understand the evolution of mating strategies at different levels of biological resolution.

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

Similar content being viewed by others

References

  • Albrecht T, Kreisinger J, Piálek J (2006) The strength of direct selection against female promiscuity is associated with rates of extrapair fertilizations in socially monogamous songbirds. Am Nat 167:739–744

    Article  PubMed  Google Scholar 

  • Anderson MJ, Nyholt J, Dixson AF (2005) Sperm competition and the evolution of sperm midpiece in mammals. J Zool 267:135–142

    Article  Google Scholar 

  • Arnquist G, Kirkpatrick M (2005) The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behavior in females. Am Nat 165:S26–S37

    Article  Google Scholar 

  • Avise JC, Jones AG, Walker D, DeWoody JA (2002) Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annu Rev Genet 36:19–45

    Article  PubMed  CAS  Google Scholar 

  • Baker RJ, Makova KD, Chesser RK (1999) Microsatellites indicate a high frequency of multiple paternity in Apodemus (Rodentia). Mol Ecol 8:107–111

    Article  PubMed  CAS  Google Scholar 

  • Bartmann S, Gerlach G (2001) Multiple paternity and similar variance in reproductive success of male and female wood mice (Apodemus sylvaticus). Ethology 107:889–899

    Article  Google Scholar 

  • Bennett P, Owens IPF (2002) Evolutionary ecology of birds. Life histories, mating systems, and extinction. Oxford University Press, Oxford

    Google Scholar 

  • Booth W, Montgomery WI, Prodöhl PA (2007) Polyandry by wood mice in natural populations. J Zool 273:176–182

    Article  Google Scholar 

  • Breed WG, Taylor J (2000) Body mass, testes mass, and sperm size in murine rodents. J Mammal 81:758–768

    Article  Google Scholar 

  • Bronson FH (1979) The reproductive ecology of the house mouse. Q Rev Biol 54:265–299

    Article  PubMed  CAS  Google Scholar 

  • Brown LE (1969) Field experiments on the movements of Apodemus sylvaticus L. using trapping and tracking techniques. Oecologia 2:198–222

    Article  Google Scholar 

  • Bryja J, Řehák Z (1998) Community of small terrestrial mammals (Insectivora, Rodentia) in dominant habitats of the Protected Landscape Area of Poodří (Czech Republic). Folia Zool 47:249–260

    Google Scholar 

  • Bryja J, Stopka P (2005) Facultative promiscuity in a presumably monogamous mouse Apodemus microps. Acta Theriol 50(2):189–196

    Google Scholar 

  • Bryja J, Heroldová M, Zejda J (2002) Effects of deforestation on structure and diversity of small mammal communities in the Moravskoslezské Beskydy Mts (Czech Republic). Acta Theriol 47(3):295–306

    Google Scholar 

  • Čiháková J, Frynta D (1996) Intraspecific and interspecific behaviour interactions in the wood mouse (Apodemus sylvaticus) and the yellow-necked mouse (Apodemus flavicollis) in a neutral cage. Folia Zool 45:105–113

    Google Scholar 

  • Clapham PJ, Palsboll PJ (1997) Molecular analysis of paternity shows promiscuous mating in female humpback whales (Megaptera novaengliae, Borowski). Proc R Soc B 264:95–98

    Article  PubMed  CAS  Google Scholar 

  • Crawley MJ (2002) Statistical computing. An introduction to data analysis using S-Plus. Wiley, New York

    Google Scholar 

  • Dean MD, Ardlie KG, Nachman MW (2006) The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol Ecol 15:4141–4151

    Article  PubMed  CAS  Google Scholar 

  • Dewsbury DA, Baumgardner DJ (1981) Studies of sperm competition in two species of muroid rodents. Behav Ecol Sociobiol 9:121–133

    Article  Google Scholar 

  • Faraway JJ (2005) Extending the linear model with R: generalized linear, mixed effects and nonparametric regression models. Chapman & Hall/CRC, New York

    Google Scholar 

  • Faulkes CG, Abbott DH, O’Brien HP, Lau L, Roy MR, Wayne RK, Bruford MW (1997) Micro- and macrogeographical genetic structure of colonies of naked mole-rats Heterocephalus glaber. Mol Ecol 6:615–628

    Article  PubMed  CAS  Google Scholar 

  • Frynta D, Exnerová A, Nováková A (1995) Intraspecific behaviour interactions in the striped-field mouse (Apodemus agrarius) and its interspecific relationships to the wood mouse (Apodemus sylvaticus): dyadic encounters in a neutral cage. Acta Soc Zool Bohem 59:53–62

    Google Scholar 

  • Griffith SC, Owens IPF, Thuman K (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

    Article  PubMed  CAS  Google Scholar 

  • Gryczyńska-Siemiątkowska A, Gortat T, Kozakiewicz A, Rutkowski R, Pomorski J, Kozakiewicz M (2008) Multiple paternity in a wild population of the yellow-necked mouse Apodemus flavicollis. Acta Theriol 53(3):251–258

    Google Scholar 

  • Heroldová M, Jánová E, Bryja J, Tkadlec E (2005) Set-aside plots—source of small mammal pests? Folia Zool 54(4):337–350

    Google Scholar 

  • Heroldová M, Tkadlec E, Bryja J, Zejda J (2008) Wheat or barley? Feeding preferences affect distribution of three rodent species in agricultural landscape. Appl Anim Behav Sci 110:354–362

    Article  Google Scholar 

  • Heske EJ, Ostfeld RS (1990) Sexual dimorphism in size, relative size of testes, and mating systems in North American voles. J Mammal 71:510–519

    Article  Google Scholar 

  • Hoogland JL (1998) Why do female Gunnison’s prairie dogs copulate with more than one male? Anim Behav 55:351–359

    Article  PubMed  Google Scholar 

  • Huminski S (1969) Biomorphological studies on testes and male accessory glands in some species of the families Muridae and Microtidae found in Poland. Zoolog Pol 19:213–255

    Google Scholar 

  • Immler S, Saint-Jalme M, Lesobre L, Sorci G, Roman Y, Birkhead TR (2007) The evolution of sperm morphometry in pheasants. J Evol Biol 20:1008–1014

    Article  PubMed  CAS  Google Scholar 

  • Inoue N, Ikawa M, Nakanishi T, Matsumoto M, Nomura M, Seya T, Okabe M (2003) Disruption of mouse CD46 causes an accelerated spontaneous acrosome reaction in sperm. Mol Cell Biol 23:2614–2622

    Article  PubMed  CAS  Google Scholar 

  • Johnson PM, Clift LE, Andrlikova P, Jursova M, Flanagan BF, Cummerson JA, Stopka P, Dvorakova-Hortova K (2007) Rapid sperm acrosome reaction in the absence of acrosomal CD46 expression in promiscuous field mice (Apodemus). Reproduction 134:739–747

    Article  PubMed  CAS  Google Scholar 

  • Kenagy GJ, Trombulak SC (1986) Size and function of mammalian testes in relation to body size. J Mamm 67:1–22

    Article  Google Scholar 

  • Kleven O, Laskemoen T, Fossoy F, Robertson RJ, Lifield JT (2008) Intraspecific variation in sperm length is negatively related to sperm competition in passerine birds. Evolution 62:494–499

    Article  PubMed  Google Scholar 

  • Kraaijeveld-Smit FJL, Ward SJ, Temple-Smith PD (2002) Multiple paternity in a field population of a small carnivorous marsupial, the agile antechinus, Antechinus agilis. Behav Ecol Sociobiol 52:84–91

    Article  Google Scholar 

  • Krasnov BR, Stanko M, Miklisová D, Morand S (2006) Habitat variation in species composition of flea assemblages on small mammals in central Europe. Ecol Res 21:460–469

    Article  Google Scholar 

  • Liebgold EB, Cabe PR, Jaeger RG, Leberg PL (2006) Multiple paternity in a salamander with socially monogamous behaviour. Mol Ecol 15:4153–4160

    Article  PubMed  CAS  Google Scholar 

  • Madsen T, Shine R, Loman J, Hakansson T (1992) Why do female adders copulate so frequently. Nature 355:440–441

    Article  Google Scholar 

  • Makova KD, Patton JC, Krysanov EYU, Chesser RK, Baker RJ (1998) Microsatellite markers in wood mouse and striped field mouse (genus Apodemus). Mol Ecol 7:247–255

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • MathSoft, Inc. (2001) S-PLUS version 6.0. Available at www.insightful.com

  • Mays HL, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554–559

    Article  PubMed  Google Scholar 

  • Mazurkiewicz M, Rajska-Jurgiel E (1998) Spatial behavior and population dynamics of woodland rodents. Acta Theriol 43:137–161

    Google Scholar 

  • Moble KB, Jones AG (2007) Geographical variation in the mating system of the dusky pipefish (Syngnathus floridae). Mol Ecol 16:2596–2606

    Article  Google Scholar 

  • Montgomery WI, Gurnell J (1985) The behaviour of Apodemus. Symp Zool Soc London 55:89–115

    Google Scholar 

  • Moore H, Dvorakova K, Jenkins N, Breed W (2002) Exceptional sperm cooperation in the wood mouse. Nature 418:174–177

    Article  PubMed  CAS  Google Scholar 

  • Morand S, Goüy de Bellocq J, Stanko M, Miklisová D (2004) Is sex biased ectoparasitism related to sexual size dimorphism in small mammals of Central Europe? Parasitology 129:505–510

    Article  PubMed  CAS  Google Scholar 

  • Munshi-South J (2007) Extra-pair paternity and the evolution of testis size in a behaviourally monogamous tropical mammal, the large treeshrew (Tupaia tana). Behav Ecol Sociobiol 62:201–212

    Article  Google Scholar 

  • Parker GA, Ball MA, Stockley P, Gage MJG (1997) Sperm competition games: a prospective analysis of risk assessment. Proc R Soc B 264:1793–1802

    Article  PubMed  CAS  Google Scholar 

  • Pelikán J (1966) Comparison of the birth rates in four Apodemus species. Zool listy 15:125–130

    Google Scholar 

  • Pelikán J (1967) Resorption rate in embryos of four Apodemus species. Zool listy 16:325–342

    Google Scholar 

  • Pelikán J (1970) Sex ratio in three Apodemus species. Zool listy 19:23–34

    Google Scholar 

  • Pitcher TE, Dunn PO, Whittingham LA (2005) Sperm competition and the evolution of testes size in birds. J Evol Biol 18:557–567

    Article  PubMed  CAS  Google Scholar 

  • Polechová J, Stopka P (2002) Geometry of social relationships in the Old World wood mouse, Apodemus sylvaticus. Can J Zool 80:1383–1388

    Article  Google Scholar 

  • Ramm SA, Parker GA, Stockley P (2005) Sperm competition and the evolution of male reproductive anatomy in rodents. Proc R Soc B 272:949–955

    Article  PubMed  Google Scholar 

  • Randolph SE (1977) Changing spatial relationships in a population of Apodemus sylvaticus with onset of breeding. J Anim Ecol 46:653–676

    Article  Google Scholar 

  • Reichard M, Smith C, Bryja J (2008) Seasonal change in the opportunity for sexual selection. Mol Ecol 17:642–651

    PubMed  CAS  Google Scholar 

  • Ribble DO, Millar JS (1992) Intraspecific variation in testes size among northern populations of Peromyscus. Funct Ecol 6:455–459

    Article  Google Scholar 

  • Salvioni M (1988) Home range and social behavior of three species of European Pitymys (Mammalia, Rodentia). Behav Ecol Sociobiol 22:203–210

    Article  Google Scholar 

  • Say L, Pontier D, Natoli E (1999) High variation in multiple paternity of domestic cats (Felis catus L.) in relation to environmental conditions. Proc R Soc B 266:2071–2074

    Article  PubMed  CAS  Google Scholar 

  • Simeonovska-Nikolova D (2006) Social interactions of the striped field-mouse Apodemus agrarius (Mammalia: Rodentia, Muridae). Acta Zool Bulg 58:93–100

    Google Scholar 

  • Simeonovska-Nikolova DM (2007) Interspecific social interactions and behavioral responses of Apodemus agrarius and Apodemus flavicollis to conspecific and heterospecific odors. J Ethol 25:41–48

    Article  Google Scholar 

  • Stanko M, Mošanský L, Fričová J, Čisláková L, Schniererová E (2005) Long-time study of natural focus and its structure in eastern Slovakia. In: Buczek A, Blaszak C (eds) Arthropods, a variety of forms and interactions. Lublin, Poland, pp 113–119

    Google Scholar 

  • Stanko M, Krasnov BR, Miklisová D, Morand S (2007) Simple epidemiological model predicts the relationships between prevalence and abundance in ixodid ticks. Parasitology 134:59–68

    Article  PubMed  CAS  Google Scholar 

  • StatSoft, Inc. (2001). STATISTICA (data analysis software system), version 6. www.statsoft.com

  • Stockley P (2003) Female multiple mating behaviour, early reproductive failure and litter size variation in mammals. Proc R Soc B 270:271–278

    Article  PubMed  CAS  Google Scholar 

  • Stopka P, Macdonald DW (1998) Signal interchange during mating in the wood mouse (Apodemus sylvaticus): the concept of active and passive signalling. Behaviour 135:231–249

    Google Scholar 

  • Stopka P, Macdonald DW (1999) The market effect in the wood mouse, Apodemus sylvaticus: Selling information on reproductive status. Ethology 105:969–982

    Article  Google Scholar 

  • Stopka P, Graciasová R (2001) Conditional allogrooming in the herb-field mouse. Behav Ecol 12:584–589

    Article  Google Scholar 

  • Stutchbury BJM (1998) Female mate choice of extra-pair males: breeding synchrony is important. Behav Ecol Sociobiol 43:213–215

    Article  Google Scholar 

  • Suchomelová E, Frynta D (2000) Intraspecific behavioural interactions in Apodemus microps: a peaceful mouse? Acta Theriol 45:201–209

    Google Scholar 

  • Tew TE, Macdonald DW (1994) Dynamics of space use and male vigor amongst wood mice, Apodemus sylvaticus, in the cereal ecosystem. Behav Ecol Sociobiol 34:337–345

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Vieites DR, Nieto-Roman S, Barluenga M, Palanca A, Vences M, Meyer A (2004) Post-mating clutch piracy in an amphibian. Nature 431(7006):305–308

    Article  PubMed  CAS  Google Scholar 

  • Vukicevic-Radic O, Matic R, Kataranovski D, Stamenkovic S (2006) Spatial organization and home range of Apodemus flavicollis and A. agrarius on Mt. Avala, Serbia. Acta Zool Acad Sci H 52(1):81–96

    Google Scholar 

  • Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol S 34:365–396

    Article  Google Scholar 

  • Whitten WK (1958) Modification of the oestrous cycle of the mouse by external stimuli associated with the male. Changes in the oestrous cycle determined by vaginal smears. J Endocrinol 17:307–313

    Article  PubMed  CAS  Google Scholar 

  • Wolff JO, Macdonald DW (2004) Promiscuous females protect their offspring. Trends Ecol Evol 19:127–134

    Article  PubMed  Google Scholar 

  • Wolton RJ, Flowerdew JR (1985) Spatial distribution and movements of wood mice, yellow-necked mice and bank voles. Symp Zool Soc Lond 55:249–275

    Google Scholar 

  • Zeh JA, Zeh DW (1997) The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc R Soc B 264:69–75

    Article  Google Scholar 

  • Zejda J, Pelikán J (1969) Movements and home ranges of some rodents in lowland forests. Zool listy 18:143–162

    Google Scholar 

  • Zgrabszynska E, Pilacinska B (2002) Social relations in family group of wood mice Apodemus sylvaticus under laboratory and enclosure conditions. Acta Ther 47:151–162

    Google Scholar 

Download references

Acknowledgements

We thank M. Heroldová, E. Jánová, and Z. Řehák for their help in the field and H. C. Hauffe for very useful comments on the previous versions of the manuscript and for linguistic correction. The work was supported by the following projects: KONTAKT—Ministry of Education CR, project no. 140 (to JB, MS), Research Centre no. LC06073 (JB, TA), MSM 0021622416 (JB, HP), MSM 0021620828 (TA, PS), Czech Science Foundation 206/07/0779 (PS), and APVV-0108-06 (MS, LM). This work complies with all current laws governing research in the Czech Republic and Slovakia.

Author information

Authors and Affiliations

  1. Department of Population Biology, Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, 67502, Studenec, Czech Republic

    Josef Bryja, Hana Patzenhauerová & Tomáš Albrecht

  2. Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 61137, Brno, Czech Republic

    Josef Bryja & Hana Patzenhauerová

  3. Biodiversity Research Group, Department of Zoology, Faculty of Science, Charles University, 12844, Prague 2, Czech Republic

    Tomáš Albrecht & Pavel Stopka

  4. Institute of Zoology, Slovak Academy of Sciences, 04002, Košice, Slovak Republic

    Ladislav Mošanský & Michal Stanko

Authors
  1. Josef Bryja
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hana Patzenhauerová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tomáš Albrecht
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ladislav Mošanský
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michal Stanko
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pavel Stopka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Josef Bryja.

Additional information

Communicated by A. Schulte-Hostedde.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bryja, J., Patzenhauerová, H., Albrecht, T. et al. Varying levels of female promiscuity in four Apodemus mice species. Behav Ecol Sociobiol 63, 251–260 (2008). https://doi.org/10.1007/s00265-008-0656-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-008-0656-7

Keywords

Search

Navigation