Hermaphroditism in fishes: an annotated list of species, phylogeny, and mating system

Tetsuo Kuwamura,Yoichi Sakai,Tomoki Sunobe,Kota Sawada,Tatsuru Kadota

doi:10.1007/s10228-020-00754-6

Abstract

Fewer than 1% of vertebrate species are hermaphroditic, and essentially all of these are fishes. Four types of hermaphroditism are known in fishes: simultaneous (or synchronous) hermaphroditism (SH), protandry (male-to-female sex change; PA), protogyny (female-to-male sex change; PG), and bidirectional sex change (BS or reversed sex change in protogynous species). Here we present an annotated list of hermaphroditic fish species from a comprehensive review and careful re-examination of all primary literature. We confirmed functional hermaphroditism in more than 450 species in 41 families of 17 teleost orders. PG is the most abundant type (305 species of 20 families), and the others are much less abundant, BS in 66 species of seven families, SH in 55 species of 13 families, and PA in 54 species of 14 families. The recently proposed phylogenetic tree indicated that SH and PA have evolved several times in not-closely related lineages of Teleostei but that PG (and BS) has evolved only in four lineages of Percomorpha. Examination of the relation between hermaphroditism type and mating system in each species mostly supported the size-advantage model that predicts the evolution of sequential hermaphroditism. Finally, intraspecific variations in sexual pattern are discussed in relation to population density, which may cause variation in mating system.

Highlights

99% of all vertebrate species consist of separate-sex individuals, i.e., pure males and pure females
Reports on bidirectional sex change within a species have increased since the 1990s (Kuwamura and Nakashima 1998; Munday et al 2010), mostly as reversed sex change in
The purpose of this study is to present an annotated species-level list of functional hermaphroditism in fishes, which will enable a wide range of interesting analyses, after a comprehensive review and careful re-examination of all primary literature

Summary

Introduction

Over one-half of the world’s living vertebrates (> 60,000 species) are fishes (> 32,000 species; Nelson et al 2016). The other 1% of vertebrate species are hermaphroditic, and almost all of them are fishes (Avise 2011; Ashman et al 2014). Four major types of hermaphroditism are known (Sadovy de Mitcheson and Liu 2008; Munday et al 2010): simultaneous (or synchronous) hermaphroditism (SH), protandry (PA), protogyny (PG), and bidirectional sex change (BS or reversed sex change in protogynous species; Kuwamura et al 2014). Simultaneous hermaphrodites produce both mature eggs and sperm in their gonads at the same time, but self-fertilization rarely occurs in fishes (Avise 2011). Reports on bidirectional sex change within a species have increased since the 1990s (Kuwamura and Nakashima 1998; Munday et al 2010), mostly as reversed sex change in

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