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. 2005 Mar 30:5:25.
doi: 10.1186/1471-2148-5-25.

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

Joris M Koene  1 , Hinrich Schulenburg
Affiliations

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

Joris M Koene et al. BMC Evol Biol. .

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 love-dart, 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 co-evolutionary arms races can result from sexual conflict in these organisms and play a key role in the evolution of hermaphroditic mating systems.

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Figures

Figure 1
Figure 1
Schematic morphological drawing of the reproductive morphology of a land snail with one dart and a diverticulum. The love-dart (D) is produced and stored in the stylophore (S, often called dart sac) and shot by a forceful eversion of this organ. The mucus glands (MG) produce the mucus that is deposited on the dart before shooting. The penis (P) is intromitted to transfer the spermatophore. The sperm container is formed in the epiphallus (EP), while the spermatophore's tail is formed by the flagellum (FL). When a bursa tract diverticulum (BTD) is present, the spermatophore is received in this organ. Together with the bursa tract (BT) and bursa copulatrix (BC) these form the spermatophore-receiving organ (SRO, indicated in grey), which digest sperm and spermatophores. Sperm swim out via the tail of the spermatophore to enter the female tract and reach the sperm storage organ (SP, spermathecae) within the fertilization pouch (FP)-spermathecal complex. Other abbreviations: AG, albumen gland; G, genital pore; HD, hermaphroditic duct; OT, ovotestis; PRM, penis retractor muscle; SO, spermoviduct; V, vaginal duct; VD, vas deferens.
Figure 2
Figure 2
Diversity of love-darts. The different shapes of love-darts are illustrated with electron microscopic photographs of side views and cross sections of darts from different species. Scale bars indicate 500 μm for side views and 50 μm for cross-sections.
Figure 3
Figure 3
Phylogeny of land snails and their love-darts. Cross-section and side views of the darts are shown. For comparability, the line drawings are all at the same size. When two cross-sections are shown, that species possesses two functional darts. The shown phylogeny was obtained by Bayesian inference (BI). Branch lengths correspond to the number of substitutions per site (see scale bar). Maximum likelihood (ML) produced an almost identical tree (see Results). Clade support is given next to the nodes such that values before slashes refer to BI posterior probabilities above 0.5 and values behind slashes to ML bootstrapping results above 50.
Figure 4
Figure 4
Graphs illustrating co-evolution and counter-adaptation. A, Correlated evolution of the darts and glands. B, Correlated evolution between stylophores and glands. C, Counter-adaptation of diverticulum in response to changes in the dart. D, Counter-adaptation of the spermatophore's tail (formed by the flagellum) in response to changes in SRO complexity. The principal components used to create the graphs are those obtained from the independent contrasts based on the BI tree without phylogenetic uncertainty. The ellipses represent the 95% confidence interval, Pearson correlations (R) and P-values are indicated in each graph.
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References

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