Quantitative Matching of Clutch Size in Reciprocating Hermaphroditic Worms

Reciprocity [1] is one of the most controversial evolutionary explanations of cooperation among non-kin [2, 3]. For some authors, cognitive capacity of non-human organisms is limiting, and more parsimonious mechanisms should apply [3-5]; for others, the debate is mainly semantic [2, 6], and empirical evidence can be found in a wide range of taxa [7]. However, while the ability to alternate cooperative behaviors does not settle the reciprocity controversy, the capacity to adjust cooperative behavior to the value of received help could prove decisive. Marine polychaete worms Ophryotrocha diadema, as several simultaneous hermaphrodites, do not self-fertilize and have unilateral mating (i.e., they behave either as females or as males during each mating event). They are also external fertilizers and thus cannot store allosperm, which contribute to make them ideal model organisms to investigate reciprocity, since partners usually alternate sexual roles with each other, repeatedly exchanging egg clutch of variable size [8-12]. However, whether the alternation of sexual roles is the result of conditional reciprocity rather than by-product reciprocity has never been tested [13]. Here, we show that O. diadema worms reciprocate eggs conditionally to the partner's behavior and adjust the quality of cooperation according to that of their partners. Moreover, only egg reciprocation offers similar fitness returns via both the female and the male function with respect to non-reciprocating laying strategies. These results document that fine-tuned forms of conditional reciprocity can emerge in cognitively unsophisticated animals, broadening the criteria to recognize conditional reciprocity among animals.