Evolutionary ingenuity often seems a bit weird

by Andrew Farrer

Simultaneous hermaphrodites are fascinating organisms. Unlike the more famous sequential hermaphrodites, such as the clown fish and sea horse (who change sex during their life cycle), simultaneous hermaphrodites are male and female simultaneously. During a single copulation event both partners donate and receive sperm.

C reticulata

Almost all nudibranchs (commonly referred to as sea slugs, despite this term also applying to taxonomic groups not related to nudibranchs) are simultaneous hermaphrodites.  With such an unusual sexual arrangement, our first question would be; why? There are several hypotheses, the most favoured of which is that for organisms living in low population densities and with low mobility it is beneficial to be able to play both roles. Turning that question on its head, we could ask: why not a simultaneous hermaphrodite?

Sex (the “mixing” of DNA between generations) does increase fitness (Lee et al. 2010) but exactly why is contentious. Reversing Muller’s Ratchet (thus preventing mutational meltdown) is commonly cited. However, despite the benefits, there are costs. The “two-fold cost” is incurred because a sexual organism, unlike an asexual organism, must locate a partner (a conspecific) with which to exchange DNA (Otto & Lenormand 2002).

Unfortunately, further problems are caused by mitochondria (and other non-nuclear DNA carrying organelles). Mitochondria with differing genomes do not like being in a cell together and the ensuing war can be catastrophic for the host cell. To avoid this deadly encounter, cells evolved to allow the mitochondria from only one parent into the next generation. The cell who’s mitochondria are passed on are female, the other cell, who’s mitochondria don’t pass on, are male (Lane 2005). Unfortunately, in avoiding the mitochondrial war, organisms have doubled the two-fold cost. Whilst the two-fold cost concentrated on the issue of needing a conspecific partner at all; now only half the conspecifics available are suitable. Two-fold became four-fold.

This leads us neatly back to simultaneous hermaphrodites. Why do it? Well, now all the conspecifics around are potential partners again and they still avoid the mitochondrial death trap. So nudibranchs, as weird as they seem, have solved an evolutionary conundrum quite neatly.

However, a Japanese team (Sekizawa et al. 2013) have observed a behaviour which places one nudibranch, Chromodoris reticulata, back in the realms of weird. This nudibranch is a simultaneous hermaphrodite which, after copulation, disposes of its penis and replaces it with a new one.

Around 20 minutes (20.57 ±7.04 min.) after copulation ends the penis is severed from the body. Within 24 hours (approximately) a new penis is formed from a spiral structure of undifferentiated tissue in the body. Indeed, the individual generally absconds from sex for this period, although on occasion it will play the female role.

C reticulata

The discarded penis is barbed and is sometimes found with sperm clinging to it. The authors hypothesised that this is either a sperm replacement technique, removing sperm from a previous mating, or excess sperm from the mating. They point out that a DNA test is needed to resolve this. I would suspect it is sperm replacement; it is wasteful of an individual to create such excess sperm that it is so clear post-copulation. Also, unless the barbs evolved to remove the individual’s own excess sperm (which seems unlikely), this hypothesis doesn’t explain their presence. The difficulty in removing the penis from the vagina of the partner is also noted as a reason for the discarding. Perhaps damage to the non-muscular penis results in a decreased effectiveness in later copulations. It also seems a risk to insert a penis covered in another individual’s sperm into a partner: the barbs are less effective against any sperm to be removed and there is the possibility of insemination by the trapped sperm.

There is little doubt that the severing of the penis is beneficial to Chromodoris reticulata; that it outweighs the costs of producing a replacement and the loss of mating potential during that period. That’s the beauty of evolution; in context it always makes sense. That doesn’t stop the idea sounding quite “unusual”. I think it keeps the nudibranchs in the bizarre category for now.

Lane, N., 2005. Power, Sex, Suicide. Mitochondria and the Meaning of Life, Oxford University Press.

Lee, S.C. et al., 2010. The evolution of sex: a perspective from the fungal kingdom. Microbiology and molecular biology reviews : MMBR, 74(2), pp.298–340. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2884414&tool=pmcentrez&rendertype=abstract [Accessed August 4, 2011].

Otto, S.P. & Lenormand, T., 2002. Resolving the paradox of sex and recombination. Nature reviews. Genetics, 3(4), pp.252–61. Available at: http://www.ncbi.nlm.nih.gov/pubmed/11967550 [Accessed June 13, 2011].

Sekizawa, A. et al., 2013. Disposable penis and its replenishment in a simultaneous hermaphrodite. Biology Letters, 9(February).

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