Sex Allocation Adjustment to Mating Group Size in a Simultaneous Hermaphrodite

Abstract

Sex allocation theory is considered as a touchstone of evolutionary biology, providing some of the best supported examples for Darwinian adaptation. In particular, Hamilton's local mate competition theory has been shown to generate precise predictions for extraordinary sex ratios observed in many separate-sexed organisms. In analogy to local mate competition, Charnov's mating group size model predicts how sex allocation in simultaneous hermaphrodites is affected by the mating group size (i.e., the number of mating partners plus one). Until now, studies have not directly explored the relationship between mating group size and sex allocation, which we here achieve in the simultaneously hermaphroditic flatworm Macrostomum lignano. Using transgenic focal worms with ubiquitous expression of green-fluorescent protein (GFP), we assessed the number of wild-type mating partners carrying GFP+ sperm from these focal worms when raised in different social group sizes. This allowed us to test directly how mating group size was related to the sex allocation of focal worms. We find that the proportion of male investment initially increases with increasing mating group size, but then saturates as predicted by theory. To our knowledge, this is the first direct test of the mating group size model in a simultaneously hermaphroditic animal. K E Y W O R D S :Local mate competition, Macrostomum lignano, mating group size, phenotypic plasticity, sperm competition.

Genome and transcriptome of the regeneration-competent flatworm, Macrostomum lignano

“…Sequencing efforts were focused on the DV1 line, which was generated through 35 generations of sibling crosses (28). Using a whole-genome shotgun approach, a total of a 170× genomic coverage of Illumina paired-end 101-bp reads were generated.…”

Self-fertilization, sex allocation and spermatogenesis kinetics in the hypodermically-inseminating flatworm Macrostomum pusillum

“…Hatchlings were collected every day and randomly assigned to different social group sizes. Mating group size is a function of social group size in M. lignano (Janicke and Schärer, 2009;Janicke et al, 2013) and a typical way of inducing variation in mating group size and thus sperm competition level involves manipulating social group size. We followed the same practice for M. pusillum, reasoning that social group size could predict mating group size in this species as well, to form three treatment groups potentially differing in outcrossing opportunities and sperm competition level: 'isolated' (one worm -enforced selfing, no sperm competition), 'paired' (two worms -potential outcrossing, low potential sperm competition) and 'octet' (eight wormspotential outcrossing, high potential sperm competition) in individual wells of 24-well plates (TPP, Trasadingen, Switzerland), each containing ca.…”

“…Various studies in animals (see Schärer, 2009, for a review) and plants (Brunet, 1992) have demonstrated that hermaphroditic organisms respond to sperm ( pollen) competition by allocating more of their reproductive resources towards the male function, as predicted by sex allocation (Charnov, 1982(Charnov, , 1996 and sperm competition theory (Parker, 1998). For example, M. lignano individuals increase testes size (Schärer and Ladurner, 2003;Janicke et al, 2013) and speed up spermatogenesis (Giannakara et al, 2016) when kept in large groups [social group size reflects mating group size in this species (Janicke et al, 2013)], presumably in order to cope with higher levels of sperm competition. We now know that this does not occur in M. pusillum.…”

“…Macrostomum lignano is an obligately outcrossing simultaneous hermaphrodite that mates by reciprocal copulation, meaning both mating partners donate and receive sperm during each mating interaction (Schärer et al, 2004). It has a complex sperm morphology (Vizoso et al, 2010;Schärer et al, 2011) and is highly responsive to social environmental conditions, plastically adjusting both its sex allocation (Schärer and Ladurner, 2003;Janicke et al, 2013) and various sperm production traits such as testicular proliferative activity (Schärer et al, 2004), sperm production rate (Schärer and Vizoso, 2007) and spermatogenesis speed (Giannakara et al, 2016), to match the prevailing social group size and thus sperm competition level.…”

“…Additionally, social group size is likely to represent mating group size, and thus worms in larger groups should exhibit higher mating rates owing to more mating encounters. In turn, mating group size is expected to represent sperm competition level, as is the case for other Macrostomum species (Janicke and Schärer, 2009;Janicke et al, 2013). Macrostomum pusillum worms should, therefore, be able to plastically adjust both their sex allocation and sperm production speed accordingly to match the current sperm competition conditions.…”