Institute of Evolution and Ecology (EvE)

Sexual selection and hermaphroditism

Sexual selection in hermaphrodites and beyond

[--> projects finished]

We are broadly interested in understanding the phylogenetic distribution of hermaphroditism across the animal kingdom, unraveling the social and environmental conditions that favor hermaphroditism over alternative forms of gender expression (such as separate sexes), and experimentally assessing the causes and consequences of sexual selection in hermaphrodite mating strategies.

(1) Phylogenetic distribution of hermaphroditism

Simultaneous hermaphroditism is a widespread form of gender expression among most invertebrate phyla and also occurs among fish. The scattered distribution across the animal phylogeny indicates that alternative forms of gender expression are rather flexible and may be repeatedly gained and lost across evolutionary time scales. A large-scale phylogenetic approach mapping gender expression on an animal phylogeny, accompanied by more fine-tuned assessments within well-studied clades, should greatly help to understand the ecological and social conditions that favor the evolution of simultaneous hermaphroditism.

Work in progress in collaboration with Philippe Jarne & Joris Koene.

(2) Evolution and stability of hermaphroditism

Sex allocation theory is a powerful approach to understand the conditions that favor the evolution and stability of simultaneous hermaphroditism. In this context, we are particularly interested in understanding how sexual selection can modulate patterns of sex allocation as well as the stability of hermaphrodites against the invasion of pure sex individuals. In cooperation with Phil Crowley, we are developing models that assess the extent to which sexual selection may favor sex allocation patterns that make hermaphroditism maladaptive and favor the displacement by pure sex invadors.

Michiels, N.K., P.H. Crowley & N.Anthes (2009):
Accessory male investment can undermine the evolutionary stability of simultaneous hermaphroditism. Biol. Lett. 5: 709-712. [free full text]

(3) Sexual selection in hermaphrodites

The bulk of our research aims at understanding how sexual selection shapes the evolution and expression of hermaphrodite mating strategies (and beyond). Simultaneous hermaphroditism exposes individuals to some unique targets upon which sexual selection can act. Broadly, these targets refer to (i) the necessity that copulating individuals need to agree on who is taking the male or female sexual role during mating ('gender conflict'), (ii) the individual decision about the amount of resources invested in male versus female reproduction ('sex allocation'), and (iii) the option to self-fertilise. It has been suggested that, since hermaphrodites may be inherently motivated to engage in mating, pre-copulatory barriers may be weak. In consequence, copulatory and post-copulatrry selection may be particularly intense in simultaneous hermaphrodites, offering ample scope for sexual conflict. Current work addresses, among other, the following issues:

(i) Hypodermic injection strategies, where sperm donors may attempt to circumvent cryptic female choice mechanisms, seem to be much more widespread among simultaneous hermaphrodites than among gonochorists. In some cases, these strategies can take extreme forms in "hit-and-run" systems that severely damage the partner (e.g. polyclad flatworms). Using the opisthobranch sea slug genus Siphopteron as a test case, we currently reconstruct the evolution of hypodermic injection strategies and quantify the costs and benefits that such strategies involve for the sperm donor and the sperm reciever.

(ii) Differences in costs and benefits associated with matings in the male and female function may generate severe conflicts over mating roles, in particular if two hermaphroditic mates prefer to copulate in the same sex function. For example, if both individuals intend to donate sperm but avoid (potentially costly) sperm receipt, mating interests are incompatible. It has been suggested that such conflicts could be resolved by a mechanism called sperm trading, where both partners accept both mating roles and trade one type of gametes, e.g. eggs, against access to the respective gametes of the partner. Using manipulative experiments in the sea slug genus Chelidonura, we have shown that conditional reciprocity may indeed exist, even though the costs and benefits involved remain to be studied.

(iii) Recent studies have demonstrated that bioactive substances transferred during mating (so-called allohormones) may strongly affect future mating behaviour, fertilisation and egg-laying processes of the partner. These substances, transferred by e.g. dart-shooting landsnails and body-piercing earthworms, may thus increase the male reproductive success and initiate an evolutionary arms-race between male and female functions. Corresponding mechanisms are being investigated in the earthworm Lumbricus terrestris.

(iv) The extent to which sexual selection acts upon male and female functions in a simultaneous hermaphrodite has to date never been quantified. We currently establish the freshwater snail Biomphalaria glabrata as a study system that allows detailed measurements of sexual selection on male and female reproductive traits.

Selected Key Publications

Anthes, N., Häderer, I.K., Michiels, N.K. & Janicke, T. (2016): Measuring and interpreting sexual selection metrics – evaluation and guidelines. Methods in Ecology and Evolution, in press.

Anthes, N., P. David, D. Sprenger et al. (2010): Bateman Gradients in Hermaphrodites: An Extended Approach to Quantify Sexual Selection. The American Naturalist 176:249-263 [full text], DOI:10.1086/655218

Anthes, N., H. Schulenburg & N.K. Michiels (2008): Evolutionary links between reproductive morphology and mating behaviour in opisthobranch gastropods. Evolution 62: 900-916. [free full text]

Anthes, N. & N.K.Michiels (2007): Precopulatory stabbing, hypodermic injections and unilateral copulations in a hermaphroditic sea slug. Biology Letters 3: 121-124. [full text]

Anthes N, Putz A, Michiels NK (2006): Sex role preferences, gender conflict and sperm trading in simultaneous hermaphrodites: a new framework . Animal Behaviour Volume: 72, Issue: 1, Pages: 1-12, [full text]

Anthes N, Putz A, Michiels NK (2005): Gender trading in a hermaphrodite. Current Biology 15: R792-R793, [full text]

Janicke T., Häderer I.K., Lajeunesse M.J., Anthes N. (2016): Darwinian sex roles confirmed across the animal kingdom. Science Advances 2: e1500983.

Koene JM, Pförtner T, Michiels NK (2005): Piercing the partner's skin influences sperm storage in earthworms. Behav. Ecol. Sociobiol. 59:243-249.[full text]

Lange, R., K. Reinhardt, N.K. Michiels & N. Anthes (2013). Functions, diversity, and evolution of traumatic mating. Biological Reviews 88: 585-601.

Lange R et al. (2012): Female Fitness Optimum at Intermediate Mating Rates under Traumatic Mating. PLoS One 7(8): e43234.

Michiels NK, Koene JM (2006): Sexual selection favours harmful mating in hermaphrodites more than in gonochorists. Integrative and Comparative Biology 46: 473-480 [full text]

Michiels NK, Newman LJ (1998): Sex and violence in hermaphrodites. Nature 391(6668): 647.

Michiels NK. (1998): Mating conflicts and sperm competition in simultaneous hermaphrodites. pp. 219-254. In: Birkhead TR, Møller AP (eds), Sperm Competition and Sexual Selection. Academic Press, London.

Reinhardt, K., N. Anthes & R. Lange (2014): Copulatory Wounding and Traumatic Insemination. In: W.R.Rice & S.Gavrilets (eds.) The Genetics and Biology of Sexual Conflict. A subject collection from Cold Spring Harbor Perspectives in Biology. CSH Press, New York

Sprenger, D., R. Lange & N. Anthes (2011). Population density and group size effects on reproductive behavior in a simultaneous hermaphrodite. BMC Evol. Biol. 11: 107

Sprenger, D., J. Faber, N.K. Michiels & N. Anthes (2008): Natural female mating rate maximizes hatchling size in a marine invertebrate. J. Animal Ecol. Volume 77 Issue 4, Pages 696 - 701 [full text]

Also check our publication list

People involved

Nils Anthes, Dennis Sprenger, Nico K. Michiels, Suska Sahm, Rolanda Lange, Ines Häderer


DFG grant AN549/3-1: Sexual selection and Bateman gradients in a
self-fertilizing hermaphrodite, Biomphalaria glabrata

DFG grant AN549/2-1: Evolutionary ecology of sexual reciprocity in a system with complex genitalia and traumatic injections

DFG grant MI482/7-4: Sexual conflicts in hermaphrodite mating behaviour III. The costs and benefits of polyandry

Förderung für Nachwuchswissenschaftler der Universität Tübingen: Evolution und Konsequenzen zwittriger Geschlechtsausprägung im Tierreich