A nudibranch removes rival sperm with a disposable spiny penis

Abstract

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.

The evolution of female genitalia

“…In some cases, the evolution of genitalia may be influenced by the elaborate genital morphologies that are favoured in males for the removal of sperm stored by females from previous matings (Gage, 1992;Kamimura, 2000;Robinson & Novak, 1997;Sekizawa, Goto, & Nakashima, 2019;Waage, 1979). In removing rival sperm, males can avoid sperm competition, which occurs when the sperm from more than one male overlap temporally in the reproductive tract of a female and compete to fertilize her ova (Parker, 1998;Simmons, 2001).…”

Evidence of sperm removal behaviour in an externally fertilizing species and compensatory behaviour for the risk of self-sperm removal

“…Generally, in species exhibiting male sperm removal behaviour, males remove rival sperm before copulation and ejaculation, and therefore the removal of their own sperm does not occur. However, for example, males of the beetle Tenebrio molitor [32] and nudibranch Chromodoris reticulata [33] remove their own sperm together with rival sperm because copulation and sperm removal occur at the same Figure 2. The relationship between the difference in time spent on sperm release behaviour before and after semen injection and time spent on sperm removal behaviour (n = 12; details in electronic supplementary material, table S1).…”

“…[32]). For example, the nudibranch Chromodoris reticulata removes rival sperm by withdrawing their penis with many backward-pointing spines after ejaculation, with some of their own sperm also being removed [33]. Although it is expected that males attempt to reduce or compensate for this risk, there have been few studies on such compensatory behaviour.…”

Precocious sperm exchange in the simultaneously hermaphroditic nudibranch,Berghia stephanieae

“…Within Heterobranchia, nudibranchs have proven to be useful for studies of development (Bonar and Hadfield 1974; Carroll and Kempf 1990; Kempf et al 1997), animal behavior and neurobiology (Willows 1971; Kriegstein et al 1974; Chase 2002; Katz and Quinlan 2019), nematocyst sequestration (Goodheart and Bely 2017; Goodheart et al 2018, 2022), and reproduction (Rutowski 1983; Rivest 1984; Hall and Todd 1986; Angeloni et al 2003; Sekizawa et al 2019). Nudibranchs are typically described as simultaneous hermaphrodites with concurrently functioning male and female sex organs and reciprocal sperm exchange between conspecifics during mating (Hall and Todd 1986; Karlsson and Haase 2002; Angeloni et al 2003; Sekizawa et al 2019).…”

“…Within Heterobranchia, nudibranchs have proven to be useful for studies of development (Bonar and Hadfield 1974; Carroll and Kempf 1990; Kempf et al 1997), animal behavior and neurobiology (Willows 1971; Kriegstein et al 1974; Chase 2002; Katz and Quinlan 2019), nematocyst sequestration (Goodheart and Bely 2017; Goodheart et al 2018, 2022), and reproduction (Rutowski 1983; Rivest 1984; Hall and Todd 1986; Angeloni et al 2003; Sekizawa et al 2019). Nudibranchs are typically described as simultaneous hermaphrodites with concurrently functioning male and female sex organs and reciprocal sperm exchange between conspecifics during mating (Hall and Todd 1986; Karlsson and Haase 2002; Angeloni et al 2003; Sekizawa et al 2019). However, descriptions of reproduction in most hermaphroditic species are often based on limited sampling of a few adult individuals (Collin 2013), and several sources describe nudibranchs as having a more complex sexual system than simply simultaneous hermaphroditism (Tyrell Smith and Carefoot 1967; Harris 1975; Todd et al 1997; Wägele and Willan 2000).…”