Functional males in pair-mating outcrossing hermaphrodites VALERIA DI BONA, MARIA CRISTINA LORENZI* and GABRIELLA SELLA Department of Animal and Human Biology, University of Turin, Via Accademia Albertina 13, 10123 Turin, Italy Received 18 November 2009; revised 23 December 2009; accepted for publication 23 December 2009bij_1435 451..456 In the mating system of simultaneously hermaphroditic animals, sexual allocation is predicted to vary as a function of the number of potential mates. According to the Hermaphrodite’s Dilemma, sexual conflict over the preferred sexual role in hermaphroditic animals is resolved by reciprocity (i.e. by alternating sexual roles), accompanied by the animals’ occasional cheating in the preferred role at a relatively low frequency. In a 350-generation-old laboratory strain of the pair-mating outcrossing hermaphroditic polychaete worm Ophryotrocha diadema, we show that 9% of the individuals mated only in the male role over long periods, indicating a male-role preference (temporary functional males). Furthermore, 2% of the individuals mated for their whole lifetime exclusively as males (permanent functional males). These findings indicate that the sex allocation of some individuals may vary from the predicted optimal sex allocation for the population. Morphologically, functional males exhibited a hermaphroditic phenotype (i.e. they matured a single batch of oocytes that they never laid and acted as functional males). We show that temporary functional males appeared in hermaphroditic populations under promiscuous mating regimes significantly more often than under monogamous ones. Indeed, under promiscuity, there are many mating opportunities and O. diadema hermaphrodites compete for mates, whereas, under monogamy, the two partners regularly take turns in laying cocoons and fertilizing their partner’s cocoon. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 451–456. ADDITIONAL KEYWORDS: conditional reciprocity – role preference – mating opportunities – Ophryotrocha diadema – sex allocation – simultaneous hermaphroditism. INTRODUCTION Sex allocation theory predicts that hermaphrodites have a limited amount of resources to allocate to both sex functions and that sex allocation adjustments are influenced by the local mating-group size (Charnov, 1982). Hence, allocation to the female function is expected to increase in populations of hermaphrodites where mating opportunities are reduced. Likewise, allocation to the male function is expected to increase, until it approaches one-half (Charnov, 1982), in popu- lations where mating opportunities are large to face sperm competition. Several studies document that sex allocation in the hermaphroditic populations adjusts to social conditions very easily (Trouvé et al., 1999; Tan, Govedich & Burd, 2004; Lorenzi et al., 2005; Schärer & Janicke, 2009). The optimal sex allocation is the predicted average for the population as a func- tion of the number of potential mates (Charnov, 1982; Fischer, 1984). Nevertheless, some hermaphroditic individuals can diverge from the predicted average opportunistically. If the distribution of reproductive success in pair- mating simultaneously hermaphroditic animals differs for sperm and for eggs, a conflict arises between mating partners over which partner will play the preferred role (The Hermaphrodite’s Dilemma model; HD) (Leonard, 1990). The solution to the HD lies in a mating system based on conditional reciproc- ity: the alternation of sexual roles more than once within a pair. When reciprocity is conditional, indi- viduals are expected to abandon a partner that cheated them by failing to reciprocate gamete *Corresponding author. E-mail: cristina.lorenzi@unito.it Biological Journal of the Linnean Society, 2010, 100, 451–456. With 1 figure © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 451–456 451 Downloaded from https://academic.oup.com/biolinnean/article/100/2/451/2450669 by guest on 04 December 2022