Female polyandry under male harassment: the case of the common toad (Bufo bufo)

Several recent studies have demonstrated the occurrence of multiple paternity in anuran amphibians, implying that it is more common than previously thought. However, an adaptive explanation for polyandry in anurans is still lacking. The common toad Bufo bufo is an explosively breeding species that releases its eggs in strings. The operational sex ratio (OSR) is male biased, causing strong scramble competition among males; females can even drown through harassment during multiple amplexi. We used microsatellite markers to determine patterns of paternity in natural B. bufo populations and experimentally mated individuals (females exposed to either two or six males). Thirty per cent of field-collected and 22% of experimentally produced egg strings were sired by at least two males; all others were sired by a single father. Multiple paternities arose only from multiple amplexi, and we found no indication of fertilization from non-amplexing males, for example through free-swimming sperm. Our results suggest that polyandry in B. bufo is likely to occur most often at high population densities, and under the most male-biased OSRs. Moreover, polyandry might be interpreted as being the consequence of females spawning when amplexed by a few males, to avoid the risk of drowning by amplexus with multiple males.

[1]  C. Reading Non‐random pairing with respect to past breeding experience in the common toad (Bufo bufo) , 2006 .

[2]  D. Lesbarrères,et al.  Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina , 2005 .

[3]  A. Jones gerud 2.0: a computer program for the reconstruction of parental genotypes from half‐sib progeny arrays with known or unknown parents , 2005 .

[4]  Marc Sztatecsny,et al.  Into thin air : vertical migration, body condition, and quality of terrestrial habitats of alpine common toads, Bufo bufo , 2005 .

[5]  L. Rowe,et al.  Escalation, Retreat, and Female Indifference as Alternative Outcomes of Sexually Antagonistic Coevolution , 2005, The American Naturalist.

[6]  Henrik G. Smith,et al.  Antagonistic Coevolution Under Sexual Conflict , 2005, Evolutionary Ecology.

[7]  G. Hill,et al.  Choosing mates: good genes versus genes that are a good fit. , 2004, Trends in ecology & evolution.

[8]  A. Meyer,et al.  Post-mating clutch piracy in an amphibian , 2004, Nature.

[9]  J. Roberts,et al.  Intrasexual selection and group spawning in quacking frogs (Crinia georgiana) , 2004 .

[10]  Robert Brooks,et al.  What is genetic quality? , 2004, Trends in ecology & evolution.

[11]  G. Hays,et al.  Polyandry in a marine turtle: females make the best of a bad job. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[12]  T. Beebee,et al.  Contrasting population structures in two sympatric anurans: implications for species conservation , 2004, Heredity.

[13]  T. Garner,et al.  Relatedness, body size and paternity in the alpine newt, Triturus alpestris , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[14]  H. Kokko,et al.  The evolution of mate choice and mating biases , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  W. Blanckenhorn,et al.  The costs of copulating in the dung fly Sepsis cynipsea , 2002 .

[16]  T. Beebee,et al.  Polymerase chain reaction primers for microsatellite loci in the Common Toad Bufo bufo , 2001 .

[17]  L. Keller,et al.  How Males Can Gain by Harming Their Mates: Sexual Conflict, Seminal Toxins, and the Cost of Mating , 2000, The American Naturalist.

[18]  P. G. Byrne,et al.  DOES MULTIPLE PATERNITY IMPROVE FITNESS OF THE FROG CRINIA GEORGIANA? , 2000, Evolution; international journal of organic evolution.

[19]  M. Double,et al.  The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae) , 2000 .

[20]  M. Petrie,et al.  Why do females mate multiply? A review of the genetic benefits , 2000, Biological reviews of the Cambridge Philosophical Society.

[21]  J. Roberts,et al.  Simultaneous mating with multiple males reduces fertilization success in the myobatrachid frog Crinia georgiana , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  R. Standish,et al.  Synchronous polyandry and multiple paternity in the frogCrinia georgiana(Anura: Myobatrachidae) , 1999, Animal Behaviour.

[23]  P. Stockley Sperm Competition and Sexual Selection , 1999, Heredity.

[24]  Y. Yasui,et al.  The `genetic benefits' of female multiple mating reconsidered. , 1998, Trends in ecology & evolution.

[25]  T. C. Marshall,et al.  Statistical confidence for likelihood‐based paternity inference in natural populations , 1998, Molecular ecology.

[26]  A. Laurila,et al.  Multiple paternity in the common frog (Rana temporaria): genetic evidence from tadpole kin groups , 1998 .

[27]  T. Halliday,et al.  Atlas of Amphibians and Reptiles in Europe , 1997 .

[28]  T. Burke,et al.  Effective number of breeding adults in Bufo bufo estimated from age‐specific variation at minisatellite loci , 1997, Molecular ecology.

[29]  I. Ahnesjö,et al.  The dynamics of operational sex ratios and competition for mates. , 1996, Trends in ecology & evolution.

[30]  B. Turner,et al.  Multiple paternity in the red‐eyed treefrog Agalychnis callidryas (Cope) , 1995, Molecular ecology.

[31]  J. Höglund Pairing and spawning patterns in the common toad, Bufo bufo: the effects of sex ratios and the time available for male-male competition , 1989, Animal Behaviour.

[32]  N. Davies,et al.  Competitive mate searching in male common toads, Bufo bufo , 1979, Animal Behaviour.

[33]  K. Wells The social behaviour of anuran amphibians , 1977, Animal Behaviour.

[34]  R. D. Semlitsch Evolutionary consequences of non-random mating: do large males increase offspring fitness in the anuran Bufo bufo? , 2004, Behavioral Ecology and Sociobiology.

[35]  D. Lesbarrères,et al.  Multiple paternity in Rana dalmatina, a monogamous territorial breeding anuran , 2003, Naturwissenschaften.

[36]  J. Avise,et al.  Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. , 2002, Annual review of genetics.

[37]  T. Halliday 12 – Sperm Competition in Amphibians , 1998 .

[38]  J. Höglund,et al.  Random mating by size in a population of common toads (Bufo bufo) , 1987 .

[39]  M. Wade,et al.  THE EVOLUTION OF INSECT MATING SYSTEMS. , 1984, Evolution; international journal of organic evolution.