Although it is often thought that sexual selection is weaker in simultaneous hermaphrodites than in gonochorists, some simultaneous hermaphrodites exhibit bizarre mating behaviour. In the simultaneously hermaphroditic nudibranch Chromodoris reticulata, we found a peculiar mating behaviour, wherein the nudibranch autotomized its penis after each copulation and was able to copulate again within 24 h. To have sufficient length to be replenished for three copulations, the penis is compressed and spiralled internally. No other animal is known to repeatedly copulate using such 'disposable penes'. Entangled sperm masses were observed on the outer surface of the autotomized penis, which is equipped with many backward-pointed spines. There is a possibility that the nudibranch removes sperm already stored in a mating partner's sperm storage organ(s).

Simultaneous hermaphroditism is, at least initially, favoured by selection under low density-and therefore it can be assumed that sperm competition has little importance in this sexual system. However, many simultaneously hermaphroditic nudibranchs have both an allo-sperm storage organ (the seminal receptacle) and an allo-sperm digesting organ (the copulatory bursa), suggesting the possibility of the occurrence of sperm competition. A nudibranch, Chromodoris reticulata, autotomizes its penis after every copulation and replenishes it within about 24 h to perform another copulation. We observed that the surface of the autotomized penis was covered with many backward-pointing spines and that a sperm mass was often entangled on the spines. This suggests that the nudibranch removes sperm that is already stored in a mating partner's sperm storage organ(s) with its thorny penis. Using six microsatellite markers, we determined that the sperm mass attached to the penis were allo-sperm originating from individual(s) that had participated in prior copulations. We revealed that C. reticulata performed sperm removal using the thorny penis. These results suggest that competition in fertilization is quite intense and mating frequency in the wild is relatively high in this species.

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We described and compared the mating behavior and morphology of the reproductive system in chromodorid nudibranchs, then, examined how extensively the unique usage of the penis (autotomy and sperm removal) evolved among Chromodorids. In addition to Ardeadoris egretta, all of examined five species in Glossodoris autotomized their penises at the last stage of copulation. An interspecific difference was seen in penis autotomy in Noumea and Goniobranchus. A spiral structure was recognized in the vas deferens of autotomized species. This structure is supposed to be undifferentiated “next penises” stored in the vas deferens, which ensure successive copulation in autotomized species. Though the basic mechanism of penis replenishment was consistent, the reason to autotomize their penises may not be the same. Goniobranchus reticulatus is reported to remove sperm already stored in the mating partner’s sperm storage organ(s) with backward-pointing spines on the surface of its penis. Contrary to G. reticulatus, all of ten species that autotomized their penises in the present study did not have thorny but smooth penises. When they autotomized their penises, the tip of the penises still remained in the vagina of the partners. This suggests that autotomized penises in these nudibranchs function as a kind of copulatory plugs.

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The article A nudibranch removes rival sperm with a disposable spiny penis, written by Ayami Sekizawa, Shin G. Goto and Yasuhiro Nakashima, was originally published Online First without Open Access.

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