Fishes' ancestral sexual system was the separate sexes and not hermaphroditism, as previously proposed

A new study by the Institut de Ciències del Mar (ICM-CSIC) in Barcelona has revealed that gonochorism, or separate sexes, and not hermaphroditism, as proposed by recent phylogenetic work, is the fishes’ ancestral sexual system. This explains why in fish hermaphroditism is a character that has appeared several times independently during their evolutionary history.

All the details are reported in an article published today in the journal Nature Communications. It is the most comprehensive analysis of the evolution of sexual systems in animals, with more than 4,600 species from over 50 orders and more than 300 families of fish from around the world analysed, more than ten times the number of samples used in previous studies.

"Understanding how the sexual systems of animals have evolved is key, as they have a profound influence on the reproductive success of individuals, population dynamics, territory occupation and colonisation events in new habitats. Therefore, sexual systems determine the resilience of populations to natural and anthropogenic changes," explains the ICM-CSIC researcher Francesc Piferrer, who led the study.

For her part, Susanna Pla, another ICM-CSIC researcher and first author of the study, explains that "our study reveals that the evolution of sexual systems is more dynamic and complex than what  is usually assumed".

Firstly, she adds,"it is more dynamic because there are sexual systems that are gained and lost more easily than previously thought" and, secondly, "it is more complex because to evolve rom gonochorism to simultaneous hermaphroditism -in which an organism has both sexes simultaneously throughout its life - it is necessary to go through an intermediate system, sequential hermaphroditism, in which species change sex during their lives".

Sexual systems in fish

Sexual systems in both plants and animals range from systems with fixed, separate sexes between males and females (called dioecy  in plants and gonochorism in animals) to simultaneous hermaphroditism, in which each individual produces both male and female gametes.

According to theoretical models, these two sexual systems can be seen as the extremes of a gradient of intermediate systems to be passed through, such as sequential hermaphroditism, as this study has shown for the first time.

Thus, the study published now reveals that, at least in fish, simultaneous hermaphroditism cannot evolve directly from separate sexes, but requires the intermediate step of sequential hermaphroditism, especially through protandric species, in which male individuals become females.

The latter, however, not a very stable system, since it is almost more easily lost than gained, which would explain why, in fish, it is much more common to find protogynous species, in which females become males, species that are evolutionarily more stable.

Implications of the study

This has a number of evolutionary implications. On the one hand, although gonochorism, the system of separate male-female sexes, is an evolutionarily stable condition, gained faster than it is lost, these results refute the assumption that the transition to gonochorism is irreversible and represent another example against Dollo's law of irreversibility, proposed by the Belgian palaeontologist Louis Dollo in 1893, which states that, in evolution, when you move from one state to another, you can never go back to the previous state.

Moreover, the study recalls that the distribution of fish sexual systems in the tree of life is a mystery. "With current knowledge and distribution, we cannot explain why some sexual forms evolve in some groups, when according to current models they should not, and vice versa," details Piferrer.

This discrepancy between theory and practice is known as the Williams’ Paradox, after the evolutionary biologist George Williams. It was discovered it in 1975, and is a mystery of evolutionary biology as far as sexual systems are concerned.

Therefore, for future research on the evolution of sexual systems, researchers propose using a new theoretical framework that includes features of the life history of individuals such as mating system, spawning behaviour or the diversity of sex determination mechanisms.

"Only in this way will it be possible to obtain a complete picture of the evolution of sexual systems in fish, so that we may finally be able to resolve Williams' paradox and take all this knowledge into account in the conservation and management of marine resources", they conclude.