Precopulatory stabbing, hypodermic injections and unilateral copulations in a hermaphroditic sea slug

Abstract

Reciprocity constitutes the prevalent mating mechanism among simultaneous hermaphrodites. Yet, when copulations in the female role confer fitness costs through male manipulation, it becomes advantageous sometimes to mate unilaterally in the male role only. In the sea slug Siphopteron quadrispinosum, acting males stab their partner with a bipartite penis, which not only hypodermically injects prostate fluids, but also apparently mechanically enforces unilateral male matings. Despite a pronounced male mating drive in both partners, unilaterality ensued when one slug stabbed more rapidly than its partner. The acting male may thus avoid the costs inflicted by traumatic injections and penial spines. While future studies need to elucidate the net fitness consequences of stabbing, our behavioural evidence is in line with the hypothesis that mating in S. quadrispinosum represents conflicting rather than complementary mating interests between mates.

Figure 1

(a) Reproductive anatomy of Siphopteron quadrispinosum (dorsal view). (b) Retracted and everted male copulatory organ. Grey shading indicates the interior body cavity. (c) Unilateral copulation sequence: precopulatory struggle with parapod flapping (arrows), reciprocal stabbing attempts during rapid clockwise circling, unilateral injection and insemination, and withdrawal of the penial bulb (life images in electronic supplementary material, figure S1).

Figure 2

Penial morphology of Siphopteron quadrispinosum. (a) Light microscopy images of (i) the penial papilla and (ii) the penial bulb. (b) Serial sections of the inserted penial bulb showing two proximal spines (i) anchored in the receiver's genital tract and (ii) the deeply inserted penial bulb plus the tip of one spine. Tissue of the acting female is shaded to facilitate orientation.