Polychaete Worms on the Brink Between Hermaphroditism and Separate Sexes

A model for the gradual evolution of dioecy and heterogametic sex determination

“…Most empirical evidence for transitions from hermaphroditism to dioecy comes from flowering plants, where such transitions have occurred thousands of times independently (Renner, 2014; Henry et al, 2018). In animals, our results are directly relevant to a number of taxa in which separate sexes have evolved from hermaphroditism, e.g., the Ophryotrocha genus in polychaete annelids or flatworms of the Schistosoma genus (Ramm, 2016; Picchi and Lorenzi, 2018; Leonard, 2018; Wang et al, 2022). Our model may also be useful to understand ‘split sex-ratios’ in ants and other social Hymenoptera, where colonies produce either male or female sexuals leading to a form of colony-level dioecy (Meunier et al, 2008; Kuemmerli and Keller, 2009).…”

“…Our model is particularly relevant to cases where dioecy evolved from monoecy in flowering plants, with individuals gradually diverging in the number of their male and female flowers (Renner and Ricklefs, 1995; Cronk, 2022). Nonetheless, our predictions should also apply to plants with bisexual flowers, and to animal taxa in which dioecy evolved from hermaphroditism, such as the Ophryotrocha genus in polychaete annelids or flatworms of the Schistosoma genus (Ramm, 2016; Picchi and Lorenzi, 2018; Leonard, 2018; Wang et al, 2022). Our model may also be useful to understand ‘split sex-ratios’ in ants and other social Hymenoptera, where colonies produce either male or female sexuals leading to a form of colony-level dioecy (Meunier et al, 2008; Kuemmerli and Keller, 2009; Lagunas-Robles et al, 2021).…”

“…In fact, taxa comprising closely related dioecious and monoecious species might be particularly well-suited to investigate the evolutionary dynamics outlined in our model, as sex allocation is more easily quantified in monoecious plants (where male and female flowers can be counted) than in species with bisexual flowers. In animals, our model might also be useful to understand the evolution of separate sexes from hermaphroditism in taxa such as polychaete annelids (e.g., in the genus Ophryotrocha ; Picchi and Lorenzi, 2018) and flatworms (e.g., in the genus Schistosoma ; Ramm, 2016), or the evolution of ‘split sex-ratios’ in ants and other social Hymenoptera, where colonies produce either male or female sexuals leading to a form of colony-level dioecy (Meunier et al, 2008; Kuemmerli and Keller, 2009; Lagunas-Robles et al, 2021).…”

Egg-trading worms start reciprocation with caution, respond with confidence and care about partners’ quality

“…For instance, individual A plays male at the first mating and female at the next (and concurrently its partner B plays female at the first mating and male at the next). Typically, such hermaphroditic partners keep switching between sexual roles over repeated mating rounds 28 – 30 , so that in the long-term partners will play female as often as they play male. The alternation of sexual roles has been reported in diverse hermaphroditic organisms, such as fish 31 – 33 and annelid worms 34 , 35 .…”

“…These worms perceive and process crucial social information enabling them to adjust their sex allocation to current mating opportunity. They invest large amount of resources into the female function (egg production and parental care) when they are kept in isolated pairs (only one partner, low mating opportunities), whereas they strongly diminish their female investment in favor of the male function (motility and aggressive competition for mating, and to a smaller extent, sperm number) when multiple partners and more mating opportunities are available 30 , 40 , 49 , 53 – 55 . In this condition, established pairs can divorce and mature worms can withhold eggs and play the male role only for weeks or even their whole life 40 , 56 .…”