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. 2015 Jul 22;282(1811):20150660.
doi: 10.1098/rspb.2015.0660.

Hypodermic Self-Insemination as a Reproductive Assurance Strategy

Free PMC article

Hypodermic Self-Insemination as a Reproductive Assurance Strategy

Steven A Ramm et al. Proc Biol Sci. .
Free PMC article

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.

Figures

Figure 1.
Figure 1.
The male copulatory apparatus in M. hystrix includes a needle-like stylet for sperm injection. (a) An adult M. hystrix flatworm viewed under light microscopy, with both male (testis) and female (ovary) reproductive organs clearly visible through the transparent body wall. Approximate body length 1 mm. (b) Close-up of the tail region of the same worm (region highlighted in (a)) under differential interference contrast light microscopy, to illustrate the needle-like male copulatory stylet, and the seminal vesicle (the male sperm storage organ, here densely packed with sperm). (Online version in colour.)
Figure 2.
Figure 2.
Experimental evidence for hypodermic self-insemination as the mechanism of selfing in M. hystrix. (a) We estimated sperm distributions in worms maintained under different social conditions designed to prevent or allow outcrossing, scoring numbers of received sperm in three body regions (head, gonad and tail) according to morphological landmarks, as shown in this schematic drawing of an adult worm. (b) Boxplots of received sperm scores in worms maintained in the isolated treatment group (open bars) compared with average received sperm scores from groups of worms maintained in triplets (filled bars). Note the radically differing sperm distributions under these two experimental conditions (see main text for statistical analysis of this difference). (c) Received sperm scores in worms that had previously been kept in the triplet treatment until scoring day 1, and that were then randomly split into an isolated (open bars) and paired (filled bars) treatment until scoring day 2 (6 days later; again, see main text for statistical analysis of the differing sperm distributions). In (b,c), each treatment–region combination is plotted as the median sperm score (bold horizontal line), the interquartile range (box), and the minimum and maximum values (whiskers); open circles represent outliers (more than 1.5× the interquartile range above the third quartile or below the first quartile).
Figure 3.
Figure 3.
Self-insemination and the onset of self-fertilization. The plot shows the relationship between the received sperm score in the head and the number of hatchlings each isolated worm had produced by selfing. Sperm scores and number of hatchlings were recorded on scoring day 1 of the experiment, and there was a significant, positive correlation between the two traits (see main text for statistics).

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