Abstract
Studies of the effects of mating order on fertilization success, classically analyzed as the proportional paternity of the second male, have advanced our understanding of the relative influences of postcopulatory male–male competition and female choice on sexual selection. However, results from these studies are often difficult to analyze because (1) distributions of offspring per dam rarely follow a normal distribution and (2) proportional paternities are never normally distributed. Previous studies partially account for these limitations by using nonparametric statistics. However, behavioral studies are often plagued by relatively small sample sizes and require a more powerful analytical approach. Here, we develop a new analytical framework for studying fertilization bias. Our Approximate Bayesian Computational (ABC) model overcomes many of the limitations of currently employed methods. We apply our model to analyze the effects of male mating order on paternity success in the brown anole lizard, Anolis sagrei. Using our ABC simulation, we find a marked first-male advantage: first males sired approximately 80 % of the offspring in our study. Next, based on re-analysis of four previously published datasets, we show that traditional statistical methods often over- or underestimate biases related to mating order. Moreover, by comparing our model to more traditional statistical tests, we show that the ABC method is robust to relatively small samples sizes and should therefore be useful for studying mating-order effects in a variety of systems. Our model is implemented as an R package, ABCp2, and is freely available for use.
Similar content being viewed by others
References
Andersson M (1994) Sexual selection. Princeton University Press, Princeton, NJ
Bardeleben C, Palchevskiy V, Calsbeek R, Wayne RK (2004) Isolation of polymorphic tetranucleotide microsatellite markers for the brown anole (Anolis sagrei). Mol Ecol Notes 4:176–178
Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368
Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035
Benken T, Knaak A, Gack C, Eberle M, Peschke K (1999) Variation of sperm precedence in the rove beetle Aleochara curtula (Coleoptera: Staphylinidae). Behaviour 136:1065–1077
Birkhead TR, Hunter FM (1990) Mechanisms of sperm competition. Trends Ecol Evol 5:48–52
Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic, London
Birkhead TR, Wishart GJ, Biggins JD (1995) Sperm precedence in the domestic fowl. P Roy Soc Lond B Bio 261:285–292
Calsbeek R, Bonneaud C (2008) Postcopulatory fertilization bias as a form of cryptic sexual selection. Evolution 62:1137–1148
Calsbeek R, Bonneaud C, Prabhu S, Manoukis N, Smith TB (2007) Multiple paternity and sperm storage lead to increased genetic diversity Anolis lizards. Evol Ecol Res 9:495–503
Carroll SP (1991) The adaptive significance of mate guarding in the soapberry bug, Jadera haematoloma (Hemiptera:Rhopalidae). J Insect Behav 4:509–530
Conner JK (1995) Extreme variability in sperm precedence in the fungus beetle, Bolitotherus cornutus (Coleoptera Tenebrionidae). Ethol Ecol Evol 7:277–280
Cook PA, Harvey IF, Parker GA (1997) Predicting variation in sperm precedence. Philos T Roy Soc B 352:771–780
Corley LS, Cotton S, McConnell E, Chapman T, Fowler K, Pomiankowski A (2006) Highly variable sperm precedence in the stalk-eyed fly, Teleopsis dalmanni. BMC Evol Biol 6:53
Cox RM, Calsbeek R (2010) Cryptic sex-ratio bias provides indirect genetic benefits despite sexual conflict. Science 328:92–94
Cox RM, Duryea MC, Najarro M, Calsbeek R (2011) Paternal condition drives progeny sex-ratio bias in a lizard that lacks parental care. Evolution 65:220–230
Darwin C (1871) The descent of man, and selection in relation to sex. Murray, London
Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton, NJ
Eggert A-K, Reinhardt K, Sakaluk S (2003) Linear models for assessing mechanisms of sperm competition: the trouble with transformations. Evolution 57:173–176
Evanno G, Madec L, Arnaud J-F (2005) Multiple paternity and postcopulatory sexual selection in a hermaphrodite: what influences sperm precedence in the garden snail Helix aspersa? Mol Ecol 14:805–812
Evans JP, Magurran AE (2001) Patterns of sperm precedence and predictors of paternity in the Trinidadian guppy. P Roy Soc Lond B Bio 268:719–724
Friedman N, Linial M, Nachman I, Pe'er D (2000) Using Bayesian networks to analyze expression data. J Comput Biol 7:601–620
Harano T, Nakamoto Y, Miyatake T (2008) Sperm precedence in Callosobruchus chinensis estimated using the sterile male technique. J Ethol 26:201–206
House C, Hunt J, Moore A (2007) Sperm competition, alternative mating tactics and context-dependent fertilization success in the burying beetle, Nicrophorus vespilloides. P Roy Soc Lond B Bio 274:1309–1315
Jones AG, Adams EM, Arnold SJ (2002) Topping off: a mechanism of first-male sperm precedence in a vertebrate. Proc Natl Acad Sci USA 99:2078–2081
Kraaijeveld-Smit FJL, Ward SJ, Temple-Smith PD, Paetkau D (2002) Factors influencing paternity success in Antechinus agilis: last-male sperm precedence, timing of mating and genetic compatibility. J Evolution Biol 15:100–107
Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655
Moreira PL, Birkhead TR (2003) Copulatory plugs in the Iberian Rock Lizard do not prevent insemination by rival males. Funct Ecol 17:796–802
Olsson M, Madsen T (1998) Sexual selection and sperm competition in reptiles. In: Birkhead TR, Möller AP (eds) Sperm Competition and Sexual Selection. Academic, London, p 504
Parker GA, Pizzari T (2010) Sperm competition and ejaculate economics. Biol Rev 85:897–934
Pitcher TE, Neff BD, Rodd FH, Rowe L (2003) Multiple mating and sequential mate choice in guppies: females trade up. P Roy Soc Lond B Bio 270:1623–1629
Pritchard JK, Seielstad MT, Perez-Lezaun A, Feldman MW (1999) Population growth of human Y chromosomes: a study of Y chromosome microsatellites. Mol Biol Evol 16:1791–1798
Radder RS, Elphick MJ, Warner DA, Pike DA, Shine R (2008) Reproductive modes in lizards: measuring fitness consequences of the duration of uterine retention of eggs. Funct Ecol 22:332–339
Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton, NJ
Thornhill R (1983) Cryptic female choice and its implications in the scorpionfly, Harpobittacus nigriceps. Am Nat 122:765–788
Venables W, Ripley B (2002) Modern applied statistics with S, 4th edn. Springer, New York
Wade PR (2000) Bayesian methods in conservation biology. Conserv Biol 14:1308–1316
Zamudio K, Sinervo E (2000) Polygyny, mate-guarding, and posthumous fertilization as alternative male mating strategies. Proc Natl Acad Sci USA 97:14427–14432
Acknowledgments
Research was conducted under permits from the Bahamas Ministry of Agriculture and approval from the Dartmouth College Institutional Animal Care and Use Committee (protocol 07-02-03). An award from the National Science Foundation (DEB 0816862 to R. Calsbeek) and funding from Dartmouth College provided financial support. We thank M. Najarro for the help with laboratory data collection. Genotypes were collected in the Molecular Biology and Proteomics Core Facility at Dartmouth College; we thank C. H. Lytle and S. A. Tyndall for their help with microsatellite fragment analysis. We thank M. A. McPeek and his graduate writing class for feedback on early versions of this manuscript.
Ethical standards
The experiments described in this manuscript comply with the current laws of the countries in which they were conducted.
Conflict of interest
The authors declare no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. J. Downes
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 304 kb)
Rights and permissions
About this article
Cite this article
Duryea, M.C., Kern, A.D., Cox, R.M. et al. A novel application of Approximate Bayesian Computation for detecting male reproductive advantages due to mating order. Behav Ecol Sociobiol 67, 1867–1875 (2013). https://doi.org/10.1007/s00265-013-1612-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-013-1612-8