American Society of Naturalists

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“The evolution of egg trading in simultaneous hermaphrodites”

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Jorge Peña, Georg Nöldeke, and Oscar Puebla (March 2020)

Researchers study the evolutionary dynamics of egg trading in simultaneous hermaphrodites by means of a mathematical model

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The origins of a trading sex game

Two yellowbelly hamlets (<i>Hypoplectrus aberrans</i>) spawning in Dominica. The fish that adopts a U shape spawns in the male role. The hamlets are iconic egg traders. <br />(Photograph © Carlos & Allison Estapé, <a href="https://carlosestape.photoshelter.com">https://carlosestape.photoshelter.com</a>)
Two yellowbelly hamlets (Hypoplectrus aberrans) spawning in Dominica. The fish that adopts a U shape spawns in the male role. The hamlets are iconic egg traders.
(Photograph © Carlos & Allison Estapé, https://carlosestape.photoshelter.com)

The sex life of simultaneous hermaphrodites is complicated by a difficult but necessary choice: who plays the female role and who plays the male role? The male role is tempting as sperm is energetically cheaper to produce than eggs, but things won't go far if no partner plays the more energetically costly female role. Some simultaneously hermaphroditic worms and fishes have found a solution to this problem by trading eggs, that is by mating in each sex role sequentially with the same partner. Yet egg trading is a form of cooperation, and as such it is open to cheating—in this case mating in the male role and parting ways. Being too picky can also be a bad idea if partners are difficult to find: in this case mating with a cheater might be better than rejecting it and risking not mating at all. These subtleties make it unclear how egg trading can evolve and be maintained, a question that has frustrated biologists since the eighties.

To tackle this question, an interdisciplinary group of researchers from the Institute for Advanced Study in Toulouse (France), the University of Basel (Switzerland), and the GEOMAR Helmholtz Centre for Ocean Research Kiel (Germany) built and analyzed a game-theoretic model that captures the most relevant features of this mating system. Their results indicate that egg trading can theoretically evolve and be maintained, but only if eggs are relatively costly to produce, partners are neither too easy nor not too difficult to find, and cheaters can be detected beforehand with some probability and punished by not mating with them. This restrictive set of conditions is consistent with the observation that just a handful of simultaneously hermaphroditic species do trade eggs. For the vast majority of simultaneous hermaphrodites, sex and trade are separate businesses.


Abstract

Egg trading, whereby simultaneous hermaphrodites exchange each other’s eggs for fertilization, constitutes one of the few rigorously documented and most widely cited examples of direct reciprocity among unrelated individuals. Yet how egg trading may initially invade a population of non-trading simultaneous hermaphrodites is still unresolved. Here, we address this question with an analytical model that considers mate encounter rates and costs of egg production in a population that may include traders (who provide eggs for fertilization only if their partners also have eggs to reciprocate), providers (who provide eggs regardless of whether their partners have eggs to reciprocate), and withholders (“cheaters” who only mate in the male role and just use their eggs to elicit egg release from traders). Our results indicate that a combination of intermediate mate encounter rates, sufficiently high costs of egg production, and a sufficiently high probability that traders detect withholders (in which case eggs are not provided) is conducive to the evolution of egg trading. Under these conditions traders can invade—and resist invasion from—providers and withholders alike. The prediction that egg trading evolves only under these specific conditions is consistent with the rare occurrence of this mating system among simultaneous hermaphrodites.