Hermaphroditism in fish: incidence, distribution and associations with abiotic environmental factors

Susanna Pla,Francesc Piferrer,Francesc Maynou

doi:10.1007/s11160-021-09681-9

Abstract

The distribution of hermaphroditism in fishes has traditionally been mainly explained by its dependence on biotic factors. However, correlates with major abiotic factors have not been investigated on a quantitative basis and at a global scale. Here, we determined the incidence of hermaphroditism in fish at the family and species level, tested the hypothesis that evolutionary relationships account for the poor presence of hermaphroditism in freshwater species, and tested the association of sexual systems with latitude, habitat type and depth. Functional hermaphroditism is reported in 8 orders, 34 families and 370 species of fishes, all teleosts. Sequential hermaphroditism predominates over simultaneous hermaphroditism at a ratio ~ 5:1 and protogyny (female-to-male sex change) predominates ~ 6:1 over protandry (male-to-female). We found 12 hermaphroditic species that can live in freshwater. However, seven of these species are from four primarily marine families while there are only five species from two mostly freshwater families. Protogynous and bi-directional sex changers have a tighter association with reef-associated tropical and subtropical habitats when compared to protandrous species, which tend to be more plastic in terms of distribution requirements. Finally, simultaneous hermaphrodite species live both in the deep sea and shallow waters in similar proportions. This study can be the basis for further research in specific groups for different purposes, including ecological and evolutionary issues as well as conservation and management of exploited species. Understanding the environmental correlates can help to forecast changes in the distribution or phenology of hermaphrodites in a global change scenario.

Highlights

Hermaphroditism, defined as the presence of the male and female function in the same individual, either sequentially or simultaneously, is present in the major taxonomic divisions of plants and is common in several Metazoans (Lewis 1942; Leonard 2013)
The best model to explain when sequential hermaphroditism is favored is the size-advantage model, which predicts that sex change will occur when the reproductive success of one sex increases more rapidly with size than the reproductive success of the opposite sex (Ghiselin 1969; Warner 1975; Charnov 1982)
We collected information on the sexual system of species belonging to 316 families, i.e., * 60% of the 514 families of Actinopterygian fishes according to Fricke et al (2019)

Summary

Introduction

Hermaphroditism, defined as the presence of the male and female function (i.e., sperm and egg production, respectively) in the same individual, either sequentially or simultaneously, is present in the major taxonomic divisions of plants and is common in several Metazoans (Lewis 1942; Leonard 2013). The best model to explain when sequential hermaphroditism is favored is the size-advantage model, which predicts that sex change will occur when the reproductive success of one sex increases more rapidly with size (or age) than the reproductive success of the opposite sex (Ghiselin 1969; Warner 1975; Charnov 1982). The above models do not explain well the distribution of sexual systems in metazoans (Williams 1975). Phylogeny reflects the large-scale distribution of sexual systems better than ecology in plants and metazoans (Leonard 2013 2018). The difference between theory predictions and actual distribution is known as ‘‘Williams’ paradox’’ (Leonard 1990 2013 2018)

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