High multiple paternity and low last‐male sperm precedence in a hermaphroditic planarian flatworm: consequences for reciprocity patterns

Abstract

It is difficult to predict a priori how mating success translates into fertilization success in simultaneous hermaphrodites with internal fertilization. Whereas insemination decisions will be determined by male interests, fertilization will depend on female interests, possibly leading to discrepancies between insemination and fertilization patterns. The planarian flatworm Schmidtea polychroa, a simultaneous hermaphrodite in which mating partners trade sperm was studied. Sperm can be stored for months yet individuals mate frequently. Using microsatellites, maternity and paternity data were obtained from 748 offspring produced in six groups of 10 individuals during four weeks. Adults produced young from four mates on average. Reciprocal fertilization between two mates was found in only 41 out of 110 registered mate combinations, which is clearly less than what is predicted from insemination patterns. Multiple paternity was high: > 80% of all cocoons had two to five fathers for only three to five offspring per cocoon. Because animals were collected from a natural population, 28% of all hatchlings were sired by unknown sperm donors in the field, despite a 10-day period of acclimatization and within-group mating. This percentage decreased only moderately throughout the experiment, showing that sperm can be stored and used for at least a month, despite frequent mating and sperm digestion. The immediate paternity a sperm donor could expect to obtain was only about 25%. Male reproductive success increased linearly with the number of female partners, providing support for Bateman's principle in hermaphrodites. Our results suggest that hermaphrodites do not trade fertilizations when trading sperm during insemination, lending support to the view that such conditional sperm exchange is driven by exchange of resources.

Sources of phenotypic variance in egg and larval traits in a marine invertebrate

“…The 'compatible gene' component emphasizes non-additive genetic effects associated with the interaction between maternal and paternal genomes. Similar to many separate sex species, simultaneous hermaphrodites often have access to sperm from different males within one reproductive season (e.g., Baur 1998;Angeloni et al 2003;Pongratz and Michiels 2003;Evanno et al 2005;Jordaens et al 2007;Marshall and Evans 2007). Although polyandry occurs in systems with both internal and external fertilization, our knowledge of polyandry-mediated fitness consequences in simultaneous hermaphrodites is currently restricted to broadcast spawners (e.g., Evans and Marshall 2005;Marshall and Evans 2007).…”

Sperm movement and morphology in a simultaneous hermaphroditic sea slug

“…The glycogen helix potentially facilitates the formation of sperm bundles, which are appropriate to transport cilia in the penis. Accessory structures in the flagellum, such as the glycogen helix in the sea slug, have also been reported in some internal fertilizers (Wilson & Healy, 2002;Pongratz & Michiels, 2003). Sperm flagella in the gastropod Helix pomatia and the neuropteran insect Mantispa perla, which transfer sperm dermally, also have accessory macrotubules containing large amounts of polysaccharides and proteins (Anderson & Personne, 1969;Dallai et al, 2005).…”

Effects of mating, breeding system and parasites on reproduction in hermaphrodites: pulmonate gastropods (Mollusca)

“…Sometimes, one individual stores received sperm whereas its partner digests the sperm received (Jordaens et al, 2005). This suggests that reciprocal sperm transfer does not a priori imply reciprocal fertilisations and that one individual may gain more paternity than the other individual (as described for a flatworm by Pongratz and Michiels, 2003).…”