Shooting darts: Co-evolution and counter-adaptation in hermaphroditic snails

Abstract

Background: Evolutionary conflicts of interest between the sexes often lead to co-evolutionary arms races consisting of repeated arisal of traits advantageous for one sex but harmful to the other sex, and counter-adaptations by the latter. In hermaphrodites, these antagonistic interactions are at least an equally important driving force. Here, we investigate the evolution of one of the most striking examples of sexual conflict in hermaphrodites, the so-called shooting of love-darts in land snails. Stabbing this calcareous dart through the partner's skin ultimately increases paternity. This trait is obviously beneficial for the shooter, but it manipulates sperm storage in the receiver. Hence, an arms race between the love-dart and the spermatophore receiving organs may be expected. Results: We performed a detailed phylogenetic analysis of 28S ribosomal RNA gene sequences from dart-possessing land snail species. Both the Shimodaira-Hasegawa test and Bayesian posterior probabilities rejected a monophyletic origin of most reproductive structures, including the lovedart, indicating that most traits arose repeatedly. Based on the inferred phylogenetic trees, we calculated phylogenetically independent contrasts for the different reproductive traits. Subsequent principal component and correlation analyses demonstrated that these contrasts covary, meaning that correlated evolution of these traits occurred. Conclusion: Our study represents the first comprehensive comparative analysis of reproductive organ characteristics in simultaneous hermaphrodites. Moreover, it strongly suggests that coevolutionary arms races can result from sexual conflict in these organisms and play a key role in the evolution of hermaphroditic mating systems. © 2005 Koene and Schulenburg; licensee BioMed Central Ltd.