Sperm or eggs?

How hermaphroditic worms distribute their resources.

Hermaphroditic species face a fundamental question: how much energy should they expend on their male and female sides? Flatworms have found various answers to this question over the course of evolution – and the solutions are directly correlated with their mating behavior.

Many plants and animals have both male and female reproductive organs. To ensure that reproduction is successful and that they can pass their genes on to as many offspring as possible, these hermaphrodites are dependent on both sexes. However, the quantity of resources that should go to the male and female sexual functions in order to achieve this aim most effectively remains unclear.

Although this question about sex allocation has long been a subject of research in plants, there is a relative lack of corresponding studies relating to hermaphroditic animals. Now, based on a phylogenetic tree of 120 flatworm species of the genus Macrostomum, evolutionary biologists from the University of Basel have been able to trace the strategy pursued by these hermaphroditic worms.

In doing so, the researchers did not just uncover one solution. “The different species exhibit a highly variable distribution of the resources available for reproduction,” says evolutionary biologist Dr. Lukas Schärer from the Department of Environmental Sciences at the University of Basel. “At the same time, we’re able to explain the various strategies based on differences in mating behavior.”

Bizarre practice

Found worldwide in water and moist locations, Macrostomum worms are what are known as simultaneous hermaphrodites – they are male and female at the same time. The worms are practically transparent, allowing the size of the testes and ovaries to be measured easily in live animals under the microscope.

Many species of this genus usually mate reciprocally in a consensual game of give and take. However, other species resort to a violent practice in which they ram their needle-like penises through their partner’s skin, from where the sperm makes its way through the tissue to the egg cell. The researchers led by Schärer were able to show that this practice – known as “hypodermic mating” – has developed in flatworms several times independently over the course of evolution.

Two strategies

Mating behavior has a significant influence on whether a species invests greater resources into male or female reproduction over the course of evolution, as the researchers report in the journal BMC Biology. The scientists identified two dominant strategies: in species that mate reciprocally, greater resources go to the male reproductive organs. In contrast, most species that are capable of hypodermic mating invest significantly more energy in their female organs.

“This is a surprising finding at first glance,” says Dr. Jeremias Brand, who now carries out research at the Max Planck Institute for Multidisciplinary Sciences. “You might expect hypodermic mating to lead to a male-biased sex allocation.” This is expected when sperm from many animals compete to fertilize the egg cells.

In reciprocally mating species, there are numerous mechanisms that reduce this competition between sperm – for example, if sperm are displaced by competitors or if the sperm recipient influences which sperm are used for fertilization after mating with several partners. However, in the case of hypodermic insemination, these mechanisms do not occur.

Ability to self-fertilize

So why do the species that engage predominantly in hypodermic mating nevertheless invest more in the female side? Here the researchers have developed hypotheses that rely on another crucial observation: population-genetic analysis shows that species that mate hypodermically appear to have an increased tendency to be self-fertilizing.

They do so by injecting sperm into the front section of their own bodies, from where it makes its way to the eggs. This complicated pathway is necessary since although the worms are hermaphrodites, they lack an internal connection between the male and female reproductive organs. As competition with other sperm is ruled out in the case of self-fertilization, the species stand to gain more if they invest more of their energy in their female systems.

Interestingly, a similar relationship exists in plants – plants that frequently or exclusively self-pollinate invest significantly more in their female reproductive components. Although plants and flatworms may look very different, their evolutionary development is actually determined by common principles.

Wissenschaftliche Ansprechpartner:

PD Dr. Lukas Schärer, University of Basel, Department of Environmental Sciences, tel. +41 61 207 03 66, E-Mail: lukas.scharer@unibas.ch

Originalpublikation:

Jeremias N. Brand, Luke J. Harmon and Lukas Schärer
Mating behavior and reproductive morphology predict macroevolution of sex allocation in hermaphroditic flatworms
BMC Biology (2022), doi: 10.1186/s12915-022-01234-1
https://doi.org/10.1186/s12915-022-01234-1

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