Hypodermic self-insemination as a reproductive assurance strategy

Abstract

Self-fertilization occurs in a broad range of hermaphroditic plants and animals, and is often thought to evolve as a reproductive assurance strategy under ecological conditions that disfavour or prevent outcrossing. Nevertheless, selfing ability is far from ubiquitous among hermaphrodites, and may be constrained in taxa where the male and female gametes of the same individual cannot easily meet. Here, we report an extraordinary selfing mechanism in one such species, the free-living flatworm Macrostomum hystrix. To test the hypothesis that adaptations to hypodermic insemination of the mating partner under outcrossing also facilitate selfing, we experimentally manipulated the social environment of these transparent flatworms and then observed the spatial distribution of received sperm in vivo. We find that this distribution differs radically between conditions allowing or preventing outcrossing, implying that isolated individuals use their needle-like stylet (male copulatory organ) to inject own sperm into their anterior body region, including into their own head, from where they then apparently migrate to the site of (self-)fertilization. Conferring the ability to self could thus be an additional consequence of hypodermic insemination, a widespread fertilization mode that is especially prevalent among simultaneously hermaphroditic animals and probably evolves due to sexual conflict over the transfer and subsequent fate of sperm.

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

“…sperm that is short and lacks bristles) that can presumably more easily travel through the parenchyma to the site of fertilization (Schärer et al, 2011). These adaptations to hypodermic insemination are likely also of assistance to the ability to self-fertilize (Ramm et al, 2015). Our study represents the first demonstration that M. pusillum can self-fertilize, rendering it the second species in the Macrostomum clade known to perform this type of mating, the other being M. hystrix (Ramm et al, 2012).…”

“…Our study represents the first demonstration that M. pusillum can self-fertilize, rendering it the second species in the Macrostomum clade known to perform this type of mating, the other being M. hystrix (Ramm et al, 2012). How exactly M. pusillum engages in self-fertilization is currently unknown, but a recent study in the morphologically similar congener M. hystrix revealed that this occurs by hypodermic self-insemination into its body and head regions, presumably because the own anterior part of the body is more easily reached by the copulatory organ located in the tail (Ramm et al, 2015). Given their morphological similarities, we can speculate that an analogous mechanism operates in M. pusillum, though further experiments are needed to confirm whether this is the case, especially given their distant phylogenetic relationship within the clade (Schärer et al, 2011).…”

“…Theory predicts that organisms for which self-fertilization exerts significant costs should delay reproduction under enforced selfing in case potential outcrossing opportunities occur, and such organisms are regarded as preferential outcrossers (Tsitrone et al, 2003a). Such a response has been shown to exist in M. hystrix (Ramm et al, 2012(Ramm et al, , 2015 and a wide range of other taxa (see Introduction). Superficially, the delay exhibited by M. pusillum when isolated resembles the response of a preferential outcrosser and seems to contradict our suggestion of a preferentially self-fertilizing species.…”

“…However, in the extended absence of mating opportunities, isolated M. hystrix individuals can switch to self-fertilization (Ramm et al, 2012) by hypodermic self-insemination (Ramm et al, 2015), despite significant inbreeding depression in the progeny (Ramm et al, 2012).…”

Exploring the sexual diversity of flatworms: Ecology, evolution, and the molecular biology of reproduction

“…Outcrossing in M. hystrix normally occurs by hypodermic insemination of another conspecific, and appears to be the preferred reproductive mode (Ramm et al, ). Flatworms that are isolated for a sufficient period can, however, switch to self‐fertilization (Ramm et al, ), apparently employing hypodermic self‐insemination, including the injection of sperm into its own head region (Ramm et al, ). This occurs only after a significant delay to commence reproduction compared to outcrossing, and at some cost in terms of selfing depression (Ramm et al, ), as predicted by theory (Tsitrone et al, ).…”