The Economics of Egg Trading: Mating Rate, Sperm Competition and Positive Frequency-Dependence

Egg trading—the alternating exchange of egg parcels during mating by simultaneous hermaphrodites—is one of the best-documented examples of reciprocity between non-relatives. By offering eggs only to partners who reciprocate, traders increase their reproductive success in the male role, but at a potential cost of delaying or reducing fertilisation of their own eggs. Although several authors have considered the evolutionary stability of egg trading once it has evolved, little attention has been paid to how egg trading can invade a population in the first place. We begin to tackle this problem by formally showing that egg trading is under positive frequency-dependent selection: once the proportion of traders in a population exceeds a certain threshold, egg trading will go to fixation. We show that if mate encounters occur frequently, then the cost of withholding eggs from unreciprocating partners is reduced, making it easier for egg trading to evolve. In contrast, the presence of opportunistic ‘streaking’, where unpaired individuals join mating pairs but contribute only sperm, makes it more difficult for egg trading to invade. This is because streakers weaken the link between the number of eggs an individual can offer and its male-role reproductive success.

[1]  Tim Clutton-Brock,et al.  Cooperation between non-kin in animal societies , 2009, Nature.

[2]  M. Landolfa On the adaptive function of gamete trading in the black hamlet Hypoplectrus nigricans , 2002 .

[3]  J. Hutchinson,et al.  Use, misuse and extensions of “ideal gas” models of animal encounter , 2007, Biological reviews of the Cambridge Philosophical Society.

[4]  N. Michiels,et al.  Gender trading in a hermaphrodite , 2005, Current Biology.

[5]  J. Bull,et al.  The Evolution of Cooperation , 2004, The Quarterly Review of Biology.

[6]  Peter Stoett To Trade or Not to Trade , 1997 .

[7]  J. R. Auld,et al.  ANIMALS MIX IT UP TOO: THE DISTRIBUTION OF SELF-FERTILIZATION AMONG HERMAPHRODITIC ANIMALS , 2006, Evolution; international journal of organic evolution.

[8]  Eric A. Fischer,et al.  The Evolution of Sexual Patterns in the Seabasses , 1987 .

[9]  Nico K. Michiels,et al.  Sex role preferences, gender conflict and sperm trading in simultaneous hermaphrodites: a new framework , 2006, Animal Behaviour.

[10]  M. Taborsky Social Evolution: Reciprocity There Is , 2013, Current Biology.

[11]  E. Charnov Simultaneous hermaphroditism and sexual selection. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[12]  J. Silk Reciprocal altruism , 2013, Current Biology.

[13]  T. Pitcher,et al.  Genetic quality and sexual selection: an integrated framework for good genes and compatible genes , 2004, Molecular ecology.

[14]  P. Crowley,et al.  Sexual conflicts along gradients of density and predation risk: insights from an egg-trading fish , 2011, Evolutionary Ecology.

[15]  D. J. Heath Simultaneous hermaphroditism; cost and benefit. , 1977, Journal of theoretical biology.

[16]  N. Anthes Mate choice and reproductive conflict in simultaneous hermaphrodites , 2010 .

[17]  N. Michiels,et al.  Sperm trading by volume in a hermaphroditic flatworm with mutual penis intromission , 1998, Animal Behaviour.

[18]  J. Leonard The Hermaphrodite's Dilemma. , 1990, Journal of theoretical biology.

[19]  W. Hamilton The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[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]  R. Connor Egg‐trading in simultaneous hermaphrodites: an alternative to Tit‐for‐Tat , 1992 .

[22]  P. Hammerstein,et al.  Economics in nature : social dilemmas, mate choice and biological markets , 2001 .

[23]  C. Petersen Reproductive behavior, egg trading, and correlates of male mating success in the simultaneous hermaphrodite, Serranus tabacarius , 1995, Environmental Biology of Fishes.

[24]  Sexual selection and reproductive success in hermaphroditic seabasses. , 2006, Integrative and comparative biology.

[25]  P. Crowley,et al.  Evolutionary stability of egg trading and parceling in simultaneous hermaphrodites: the chalk bass revisited. , 2007, Journal of theoretical biology.

[26]  P. Kappeler Animal Behaviour: Evolution and Mechanisms , 2010 .

[27]  S. M. Eppley,et al.  Moving to mate: the evolution of separate and combined sexes in multicellular organisms , 2008, Journal of evolutionary biology.

[28]  J. Leonard,et al.  Male-Female Conflict in a Simultaneous Hermaphrodite Resolved by Sperm Trading , 1984, The American Naturalist.

[29]  M. Nowak Five Rules for the Evolution of Cooperation , 2006, Science.

[30]  Eric A. Fischer Sexual Allocation in a Simultaneously Hermaphroditic Coral Reef Fish , 1981, The American Naturalist.

[31]  A. Griffin,et al.  Cooperation and Competition Between Relatives , 2002, Science.

[32]  R. Trivers The Evolution of Reciprocal Altruism , 1971, The Quarterly Review of Biology.

[33]  R. Bshary Cooperation between unrelated individuals – a game theoretic approach , 2010 .

[34]  V. Kaitala,et al.  Mate‐Search Efficiency Can Determine the Evolution of Separate Sexes and the Stability of Hermaphroditism in Animals , 2002, The American Naturalist.

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

[36]  Eric A. Fischer Simultaneous hermaphroditism, tit-for-tat, and the evolutionary stability of social systems , 1988 .

[37]  W. Hamilton,et al.  The Evolution of Cooperation , 1984 .

[38]  Eric A. Fischer Egg Trading in the Chalk Bass, Serranus tortugarum, a Simultaneous Hermaphrodite , 2010 .

[39]  R. Noë,et al.  Economics in Nature: Biological markets: partner choice as the driving force behind the evolution of mutualisms , 2001 .

[40]  Jussi Lehtonen,et al.  Positive feedback and alternative stable states in inbreeding, cooperation, sex roles and other evolutionary processes , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[41]  M. Premoli,et al.  Egg trading in the simultaneously hermaphroditic polychaete worm Ophryotrocha gracilis (Huth) , 1997 .

[42]  James W. Friedman,et al.  To trade, or not to trade; that is the question , 1991 .

[43]  Partner fidelity and egg reciprocation in the simultaneously hermaphroditic polychaete worm Ophryotrocha diadema , 2000 .