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A matter of time: delayed mate encounter postpones mating window initiation and reduces the strength of female choosiness

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Abstract

Reproductive success is determined by the presence and timing of encounter of mates. The latter depends on species-specific reproductive characteristics (e.g., initiation/duration of the mating window), season, and reproductive strategies (e.g., intensity of choosiness) that may potentially mitigate constraints imposed by mating windows. Despite their potentially crucial role for fitness and population dynamics, limited evidence exists about mating window initiation, duration, and reproductive strategies. Here, we experimentally tested the mechanisms of initiation and the duration of the common lizard's Zootoca vivipara mating window by manipulating the timing of mate encounter and analyzing its effect on (re-)mating probability. We furthermore tested treatment effects on female reproductive strategies by measuring female choosiness. The timing of mate encounter and season did not significantly affect mating probability. However, a longer delay until mate encounter reduced female choosiness. Re-mating probability decreased with re-mating delay and was independent of mating delay. This indicates that mating window initiation depends on mate encounter, that its duration is fixed, and that plastic reproductive strategies exist. These findings contrast with previous beliefs and shows that mating windows per se may not necessarily constrain reproductive success, which is congruent with rapid range expansion and absence of positive density effects on reproductive success (Allee effects). In summary, our results show that predicting the effect of mating windows on reproduction is complex and that experimental evidence is essential for evaluating their effect on reproduction and reproductive strategies, both being important determinants of population dynamics and the colonization of new habitats.

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References

  • Allee WC (1931) Animal aggregations: a study in general sociology, 1st edn. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Arnold TW (2010) Uninformative parameters and model selection using Akaike's information criterion. J Wildl Manag 74:1175–1178

    Article  Google Scholar 

  • Bauwens D, Verheyen RF (1985) The timing of reproduction in the lizard Lacerta vivipara: differences between individual females. J Herpetol 19:353–364

    Article  Google Scholar 

  • Bauwens D, Verheyen RF (1987) Variation of reproductive traits in a population of the lizard Lacerta vivipara. Holarct Ecol 10:120–127

    Google Scholar 

  • Bauwens D, Van Damme R, Verheyen RF (1989) Synchronization of spring molting with the onset of mating behavior in male lizards, Lacerta vivipara. J Herpetol 23:89–91

    Article  Google Scholar 

  • Berec L, Boukal DS, Berec M (2001) Linking the Allee effect, sexual reproduction, and temperature-dependent sex determination via spatial dynamics. Am Nat 157:217–230

    Article  CAS  PubMed  Google Scholar 

  • Bleu J, Le Galliard J-F, Meylan S, Massot M, Fitze PS (2011) Mating does not influence reproductive investment, in a viviparous lizard. J Exp Zool 315A:458–464

    Article  Google Scholar 

  • Bleu J, Bessa-Gomes C, Laloi D (2012) Evolution of female choosiness and mating frequency: effects of mating cost, density and sex ratio. Anim Behav 83:131–136

    Article  Google Scholar 

  • Brockway BF (1965) Stimulation of ovarian development and egg laying by male courtship vocalization in budgerigars (Melopsittacus undulatus). Anim Behav 13:575–578

    Article  CAS  PubMed  Google Scholar 

  • Bronson FH (1989) Mammalian reproductive biology, 1st edn. University of Chicago Press, Chicago

  • Calabrese JM, Fagan WF (2004) Lost in time, lonely, and single: reproductive asynchrony and the Allee effect. Am Nat 164:25–37

    Article  PubMed  Google Scholar 

  • Clobert J, Massot M, Lecomte J, Sorci G, de Fraipont M, Barbault R (1994) Determinants of dispersal behavior: the common lizard as a case study. In: Vitt LJ, Pianka ER (eds) Lizard ecology: historical and experimental perspectives. University Press, Princeton, pp 183–206

    Google Scholar 

  • Courchamp F, Clutton-Brock T, Grenfell B (1999) Inverse density dependence and the Allee effect. Trends Ecol Evol 14:405–410

    Article  PubMed  Google Scholar 

  • Crews D (1975) Effects of different components of male courtship behaviour on environmentally induced ovarian recrudescence and mating preferences in the lizard, Anolis carolinensis. Anim Behav 23:349–356

    Article  Google Scholar 

  • Crews D, Moore MC (1986) Evolution of mechanisms controlling mating behavior. Science 231:121–125

    Article  CAS  PubMed  Google Scholar 

  • DeNardo DF, Autumn K (2001) Effect of male presence on reproductive activity in captive female blood pythons, Python curtus. Copeia 2001:1138–1141

    Article  Google Scholar 

  • Duellman WE, Trueb L (1986) Biology of amphibians. McGraw-Hill, New York

    Google Scholar 

  • Dunham AE, Rudolf VHW (2009) Evolution of sexual size monomorphism: the influence of passive mate guarding. J Evol Biol 22:1376–1386

    Article  CAS  PubMed  Google Scholar 

  • Fitze PS, Le Galliard J-F (2008) Operational sex ratio, sexual conflict and the intensity of sexual selection. Ecol Lett 11:432–439

    Article  PubMed  Google Scholar 

  • Fitze PS, Le Galliard J-F, Federici P, Richard M, Clobert J (2005) Conflict over multiple-partner mating between males and females of the polygynandrous common lizards. Evolution 59:2451–2459

    Article  PubMed  Google Scholar 

  • Fitze PS, Cote J, Martínez-Rica JP, Clobert J (2008) Determinants of male fitness: disentangling intra- and inter-sexual selection. J Evol Biol 21:246–255

    CAS  PubMed  Google Scholar 

  • Fitze PS, Cote J, Clobert J (2010) Mating order-dependent female mate choice in the polygynandrous common lizard Lacerta vivipara. Oecologia 162:331–341

    Article  PubMed  Google Scholar 

  • Gabor CR, Halliday TR (1997) Sequential mate choice by multiply mating smooth newts: females become more choosy. Behav Ecol 8:162–166

    Article  Google Scholar 

  • Gascoigne J, Berec L, Gregory S, Courchamp F (2009) Dangerously few liaisons: a review of mate-finding Allee effects. Popul Ecol 51:355–372

    Article  Google Scholar 

  • Gavaud J (1983) Obligatory hibernation for completion of vitellogenesis in the lizard Lacerta vivipara J. J Exp Zool 225:397–405

    Article  Google Scholar 

  • Gavaud J (1991a) Cold entrainment of the annual cycle of ovarian activity in the lizard Lacerta vivipara: thermoperiodic rhythm versus hibernation. J Biol Rhythms 6:201–215

    Article  CAS  PubMed  Google Scholar 

  • Gavaud J (1991b) Role of cryophase temperature and thermophase duration in thermoperiodic regulation of the testicular cycle in the lizard Lacerta vivipara. J Exp Zool 260:239–246

    Article  Google Scholar 

  • Heulin B (1988) Observations sur l'organisation de la reproduction et sur les comportements sexuels et agonistiques chez Lacerta vivipara. Vie Milieu 38:177–187

    Google Scholar 

  • Jennions MD, Petrie M (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev 72:283–327

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    Article  CAS  PubMed  Google Scholar 

  • Kokko H, Mappes J (2005) Sexual selection when fertilization is not guaranteed. Evolution 59:1876–1885

    Article  PubMed  Google Scholar 

  • Kokko H, Rankin DJ (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philos T Roy Soc B 361:319–334

    Article  Google Scholar 

  • Kokko H, Wong BBM (2007) What determines sex roles in mate searching? Evolution 61:1162–1175

    Article  PubMed  Google Scholar 

  • Laloi D, Richard M, Lecomte J, Massot M, Clobert J (2004) Multiple paternity in clutches of common lizard Lacerta vivipara: data from microsatellite markers. Mol Ecol 13:719–723

    Article  CAS  PubMed  Google Scholar 

  • Laloi D, Eizaguirre C, Fédérici P, Massot M (2011) Female choice for heterozygous mates changes along successive matings in a lizard. Behav Process 88:149–154

    Article  Google Scholar 

  • Leboucher G, Depraz V, Kreutzer M, Nagle L (1998) Male song stimulation of female reproduction in canaries: features relevant to sexual displays are not relevant to nest-building or egg-laying. Ethology 104:613–624

    Article  Google Scholar 

  • Licht P (1972) Environmental physiology of reptilian breeding cycles: role of temperature. Gen Comp Endocrinol 3:477–488

    Article  Google Scholar 

  • Lovern MB (2011) Hormones and reproductive cycles in lizards. In: Norris DO, Lopez KH (eds) Hormones and reproduction of vertebrates, vol 3, reptiles. Academic Press, San Diego, pp pp 321–353

    Google Scholar 

  • Lynch KS, Rand AS, Ryan MJ, Wilczynski W (2005) Plasticity in female mate choice associated with changing reproductive states. Anim Behav 69:689–699

    Article  Google Scholar 

  • Massot M, Clobert J, Pilorge T, Lecomte J, Barbault R (1992) Density dependence in the common lizard: demographic consequences of a density manipulation. Ecology 73:1742–1756

    Article  Google Scholar 

  • Møller AP, Legendre S (2001) Allee effect, sexual selection and demographic stochasticity. Oikos 92:27–34

    Article  Google Scholar 

  • Mugabo M, Perret S, Legendre S, Le Galliard J-F (2013) Density-dependent life history and the dynamics of small populations. J Anim Ecol 82:1227–1239

    Article  PubMed  Google Scholar 

  • Perrins CM (1970) Timing of birds’ breeding seasons. Ibis 112:242–255

    Article  Google Scholar 

  • Richard M, Losdat S, Lecomte J, de Fraipont M, Clobert J (2009) Optimal level of inbreeding in the common lizard. Proc R Soc Lond B 276:2779–2786

    Article  CAS  Google Scholar 

  • Roig JM, Carretero MA, Llorente GA (2000) Reproductive cycle in a pyrenean oviparous population of the common lizard (Zootoca vivipara). Neth J Zool 50:15–27

    Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing,Vienna, Austria, URL http://www.R-project.org/

  • SAS Institute (2009) JMP version 8.0.2. SAS Institute Inc, Cary, NC

  • Sever DM, Hamlett WC (2002) Female sperm storage in reptiles. J Exp Zool 292:187–199

    Article  PubMed  Google Scholar 

  • Short RV (1984) Oestrous and menstrual cycles. In: Austin CR, Short RV, Fuller JR (eds) Reproduction in mammals: volume 3, hormonal control of reproduction. Cambridge University Press, Cambridge, pp 115–153

    Chapter  Google Scholar 

  • Surget-Groba Y, Heulin B, Guillaume C-P, Puky M, Semenov D, Orlova V, Kupriyanova L, Ghira I, Smajda B (2006) Multiple origins of viviparity, or reversal from viviparity to oviparity? The European common lizard (Zootoca vivipara, Lacertidae) and the evolution of parity. Biol J Linn Soc 87:1–11

    Article  Google Scholar 

  • Teuschl Y, Blanckenhorn WU (2007) The reluctant fly: what makes Sepsis cynipsea females willing to copulate? Anim Behav 73:85–97

    Article  Google Scholar 

  • Van Damme R, Bauwens D, Verheyen RF (1987) Thermoregulatory responses to environmental seasonality by the lizard Lacerta vivipara. Herpetologica 43:405–415

    Google Scholar 

  • van Nuland GJ, Strijbosch H (1981) Annual rhythmics of Lacerta vivipara Jacquin and Lacerta agilis agilis L. (Sauria, Lacertidae) in the Netherlands. Amphibia-Reptilia 2:83–95

    Article  Google Scholar 

  • Whittier JM, Tokarz RR (1992) Physiological regulation of sexual behavior in female reptiles. In: Gans C, Crews D (eds) Hormones, brain, and behavior: biology of the reptilia, vol 18. Univerity of Chicago Press, Chicago, pp 24–69

    Google Scholar 

  • Wingfield JC, Hahn TP, Levin R, Honey P (1992) Environmental predictability and control of gonadal cycles in birds. J Exp Zool 261:214–231

    Article  Google Scholar 

Download references

Acknowledgments

We thank Miguel Peñalver Alcázar and Cristina Romero Díaz for field assistance. MCB was supported by a Ph.D. grant (JAEPre_09_01372) from the Consejo Superior de Investigaciones Científicas (CSIC) and co-financed by the European Social Fund as well as PSF by the Spanish Ministry of Education and Science (Programa Ramón y Cajal, RYC-2003-006136). Project funds were provided by the Spanish Ministry of Education and Science (CGL2008-01522 to PSF) and the Swiss National Science Foundation (PPOOP3_128375 to PSF).

Ethical standards

The study conducted complies with the current Spanish laws and with ASAB/ABS Guidelines for the Treatment of Animals in Behavioural Research. Capture and handling of lizards was conducted under licenses provided by the Instituto Aragonés de Gestión Ambiental (Gobierno de Aragón).

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The authors declare that they have no conflict of interest.

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Correspondence to Merel C. Breedveld.

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Communicated by S. J. Downes

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Breedveld, M.C., Fitze, P.S. A matter of time: delayed mate encounter postpones mating window initiation and reduces the strength of female choosiness. Behav Ecol Sociobiol 69, 533–541 (2015). https://doi.org/10.1007/s00265-014-1864-y

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