F I S H and F I S H E R I E S , 2008, 9, 1–43

Functional hermaphroditism in teleosts

Yvonne Sadovy de Mitcheson & Min Liu

Swire Institute of Marine Science, Department of Ecology & Biodiversity, University of Hong Kong, Pokfulam Road,
Hong Kong

Abstract Correspondence:
Teleost fishes are characterized by a diversity of sexual patterns. Hermaphroditism, Yvonne Sadovy de
Mitcheson, Swire
the expression of both male and female reproductive function in a single individual,
Institute of Marine
generates the most curiosity and controversy. Yet diagnosis of this form of sexuality Science, Department
continues to challenge workers, in particular the distinction between functional and of Ecology & Biodi-
non-functional hermaphroditism. This distinction, reflected as it is in the relation- versity, University of
ships between gonad form and function, is important if we wish to improve our Hong Kong, Pokfulam
Road, Hong Kong
understanding of the origin of hermaphroditism in the teleosts and of its highly
Tel.: +852 22990603
sporadic expression today. Although structure can indicate phylogenetic affinities, it Fax: +852 25176082
does not always reflect reproductive function, and function is important for E-mail: yjsadovy@
understanding adaptation. With resurgent interest in hermaphroditism comes the hku.hk
recognition that understanding sexual pattern is not only important for better Received 8 Jun 2007
knowledge of reproductive biology and ecology but may also elucidate phylogenetic Accepted 17 Oct 2007
relationships. On the basis of a conservative and clearly defined set of diagnostic
criteria, which incorporate new accounts of hermaphroditic species, and by applying
an improved understanding of gonadal ontogeny, a comprehensive review and
careful re-examination of all primary literature was conducted. This overview
documents the incidence of hermaphroditism in teleosts and explores its phylogenetic
distribution, possible origin and range of expression. The review confirms functional
hermaphroditism in 27 teleost families in seven orders, predominantly among
tropical, marine perciforms in which its diversity of expression is greatest. In families
with functional hermaphrodites, the sexual pattern is widespread and often highly
variable in expression, even within a single genus or between populations. Based on
our understanding of gonadal ontogeny in teleosts and on known phylogenetic
interrelationships, the origin of functional hermaphroditism is most parsimoniously
explained by a proto-hermaphroditic condition in teleosts and cyclostomes, consti-
tuting a hermaphroditic potential for these groups. Exploitation and expression of this
potential appear to be a response to a suite of environmental and biological factors,
opportunities and constraints that result in the independent appearance of the
hermaphroditic option in many different fish lineages.

Keywords adaptive significance, gonadal morphology, gonadal ontogeny,

phylogeny, sex change, sexual pattern

Introduction 2
Definitions 3
Bisexual 3

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Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu

Sexual pattern 3
Gonochorism 4
Non-functional hermaphroditism 4
Functional hermaphroditism 4
Abnormal hermaphroditism 5
Sexually transitional phase 5
Functional sex 5
Arrhenoidy and gynoidy 5
Families in which functional hermaphroditism is confirmed 5
Elopomorpha – Anguilliformes 12
Muraenidae (Heteromyridae) (moray eels) 12
Euteleostei – Stenopterygii – Stomiiformes 14
Gonostomatidae (bristlemouths) 14
Euteleostei – Cyclosquamata – Aulopiformes 14
Chlorophthalmidae (greeneyes), Ipnopidae (deepsea tripod fishes), 14
Scopelarchidae (pearleyes), Alepisauridae (lancetfishes) and
Bathysauridae (deepsea lizardfishes)
Euteleostei – Acanthopterygii – Cyprinodontiformes 14
Rivulidae (New World rivulines) 14
Euteleostei – Acanthopterygii – Synbranchiformes 14
Synbranchidae (swamp eels) 14
Euteleostei – Acanthopterygii – Scorpaeniformes 15
Caracanthidae (orbicular velvetfishes) 15
Platycephalidae (flatheads) 15
Euteleostei – Acanthopterygii – Perciformes 15
Centropomidae (snooks) 15
Latidae (lates) 15
Serranidae (sea basses) 15
Pseudochromidae (dottybacks) 17
Nemipteridae (threadfin breams) 17
Lethrinidae (emperors or emperor breams) 17
Sparidae (porgies) 17
Centracanthidae (Maenidae) (picarel porgies) 18
Pomacanthidae (angelfishes) 18
Cirrhitidae (hawkfishes) 19
Pomacentridae (damselfishes) 19
Labridae (wrasses) 20
Scaridae (Callyodontidae) (parrotfishes) 20
Pinguipedidae (Mugiloididae) (sandperches) 21
Trichonotidae (sanddivers) 21
Gobiidae (gobies) 21
Families in which hermaphroditism has been reported, but not confirmed 22
Discussion 22
Acknowledgements 29
References 29

(1964) wrote these words hermaphroditism is

Introduction
certainly no longer perceived to be of little signifi-
Hermaphroditic fishes remain somewhat of a cance. This is largely due to the work of Reinboth
‘zoological curiosity’, but 40 years after Atz (1962) and Atz (1964), which firmly established the
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 Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
widespread phylogenetic incidence of hermaphro-
ditism as a normal sexual pattern. Interest during
the 1970s and 1980s in the possible adaptive
significance of hermaphroditism was further stimu-
lated by Ghiselin (1969), Yamamoto (1969), Chan
(1970), Reinboth (1970), Smith (1975), Warner
(1975a, 1978, 1988), Warner et al. (1975), Lepori
(1980), Robertson (1980), Chan and O (1981),
Charnov (1982), Policansky (1982), Shapiro
(1984, 1988) and Nakazono and Kuwamura
(1987). The remarkable discovery of the influence
of exogenous social factors on the expression of
adult sex change further fuelled interest (Fishelson
1970; Robertson 1972; Fricke and Fricke 1977;
Moyer and Nakazono 1978a,b; Shapiro 1980,
1981; Wood 1981; Cole 1983; Ross et al. 1983;
Cole and Robertson 1988). Renewed attention has
been attracted in recent years with reports of yet
further manifestations of the enormous plasticity in
sexual pattern expressed by teleosts in the form of
bi-directional sex change in adults and the influence
of social factors on sexual development in juveniles
of a range of species (reviewed in Munday et al.
2006a).
The incidence of piscine hermaphroditism was
reviewed several times from the 1960s to the 1980s
(Atz 1964; Yamamoto 1969; Chan 1970; Reinboth
1970; Smith 1975; Warner 1978; Lepori 1980;
Policansky 1982; Nakazono and Kuwamura 1987),
and then again more recently with a focus on
mechanisms of sex determination (Devlin and Naga-
hama 2002; Mank et al. 2006) and in relation to
reproductive traits such as sperm competition
(Molloy et al. 2007). However, attempts to account
for general patterns in phylogenetic incidence and
ecological, behavioural and ontogenetic correlates
within the Teleostei have met with limited success.
Possible reasons for this could be that earlier reports
of hermaphroditic species did not distinguish func-
tional from non-functional hermaphroditism. The
distinction is important because structure does not
always reflect function, although structure may
provide critical clues to phylogenetic affinities.
The growing number of reports of hermaphroditic
species over the last decade, new perspectives on
phylogeny in some groups emerging from molecular
studies and clearer criteria for distinguishing func-
tional from non-functional hermaphroditism invite
a re-examination of hermaphroditic sexual patterns
in the group. The following account reviews and
re-evaluates the expression of hermaphroditism in
teleosts by applying a rigorous set of diagnostic
Ó 2008 The Authors
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criteria (Sadovy and Shapiro 1987; Sadovy and
Domeier 2005) to the literature and by distinguish-
ing functional from non-functional hermaphrodit-
ism. The term ‘function’ in this definition refers to
reproductive function as established by the presence
of mature testicular and ovarian tissues either
simultaneously or sequentially in the same individ-
ual. We divide teleost families into those for which
functional hermaphroditism is confirmed from those
in which the phenomenon is reported but remains
in doubt. For consistency family classifications
follow those of Nelson (2006) with species names
cross-checked using FishBase (2007), although the
implications of several recent revisions are addressed
in relation to the Serranidae and Labridae (Westneat
and Alfaro 2005; Smith and Craig 2007). For each
family sexual patterns are identified and gonadal
morphology described. Additionally the evidence by
which diagnosis of hermaphroditism was made is
re-evaluated and diagnostic problems discussed. We
base this review on a careful evaluation of available
literature since Atz’s (1964) landmark review to
ensure a standard approach to identifying function-
ally hermaphroditic species and to identify uncon-
firmed cases, some of which have persisted in the
literature for many years; uncritical citations of
hermaphroditism based on secondary literature can
compound initial misdiagnoses such that they con-
tinue to be cited. For this reason also, reference to
primary literature for this review was important.
Definitions
Bisexual
A gonad consists of some combination of immature
testicular tissue, sometimes together with the sperm
duct system, and immature ovarian tissue. This last
could include primary growth or cortical-alveolus
stage oocytes, and may or may not involve an
ovarian-like lumen. In this review the term ‘bisex-
ual’ is used to describe gonadal morphology and
infers nothing about the potential functional sex of
the individual. Note, however, that bisexual has
been used in other vertebrates to mean that
individuals of a species display both male and
female reproductive function (Tomlinson 1968).
Sexual pattern
The sexual pattern is the characteristic reproductive
type of a species or population, and can be described
3
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
as either gonochorism or hermaphroditism; details are
given below. The only known exceptions are uni-
sexual species, such as Poecilia formosa (Poeciliidae)
in which females reproduce by mating with males of
sympatric, gonochoristic species, such as P. latipinna
and P. mexicana (Yamamoto 1969; Dries 2003).
The terms gonochorism and hermaphroditism only
refer to reproductive function (Sadovy and Shapiro
1987). To most effectively clarify the difference
between function and non-function, the term func-
tional hermaphroditism is used throughout this
review to refer to cases whereby adult sex change or
simultaneous male and female functions are clearly
evident.
Gonochorism
A species or population is considered to be gonoch-
oristic if all individuals reproduce exclusively as
either male or female during their lives, irrespective
of gonadal morphology.
Non-functional hermaphroditism
A proportion of individuals of a species or a
population may exhibit both testicular and ovarian
tissues but only ever reproduce as either male or
female during their lives. From a functional
perspective, which ignores gonadal morphology,
this state is gonochoristic.
Functional hermaphroditism
A species or population is considered to exhibit
functional hermaphroditism if a proportion of indi-
viduals functions as both sexes at some time during
their lives. Two patterns of functional hermaphro-
ditism are recognized in fishes, simultaneous and
sequential. Simultaneous hermaphrodites can repro-
duce both as male and female at the same time, or
within a short span of time. An example would be a
single spawning episode in which gonads simulta-
neously contain mature testicular and ovarian
tissues. Sequential hermaphrodites may be either
protogynous, meaning a functional female to a
functional male sex change, or protandrous, where-
by sex change is brought about by a functional male
changing to a functional female. Since the 1990s,
an increasing number of species, which previously
were mostly identified as protogynous, are reported
to change sex in both directions under field and
laboratory conditions. In this case a functional
4 Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–43
female changes to a functional male and vice versa.
In this review we treat bi-directional sex change as a
form of sequential hermaphroditism. Sequential
hermaphroditism can vary in several ways
(Reinboth 1967a). Protogynous species may show
monandry, in which all males are termed secondary
males, and derive from functional females, or
diandry, in which there are two types of males.
Primary males are males at the first sexual matu-
ration, while secondary males arise from a sex
change in functional females. A similar dichotomy
has been recorded in protandrous species and the
corresponding terms are monogyny with secondary
females only, and digyny with both primary and
secondary females (Reinboth 1967a; Chan and
Yeung 1983).
Morphologically distinct primary and secondary
males were originally recognized in the Labridae
and Scaridae (Reinboth 1962, 1967a). These males
were initially distinguished functionally on the basis
of their colouration, body size and mating type, and
the term ‘diandry’ was proposed to identify species
that had both male forms, and monandry for species
with just one. The testicular morphology of second-
ary males in labrids and scarids was also initially
thought to differ from that of primary males. In
primary males the testes were typically gonochoris-
tic, i.e. solid with a dorsal sperm duct consisting of a
tube chambered by connective tissue septa and no
lumen. In secondary males the testes retained
characteristics of its previous female phase, namely
an ovarian-like lumen and lamellar structure, while
newly formed ‘sperm sinuses’ arose within the walls
of the original ovarian lumen after sex change
(Reinboth 1962). These differences in testicular
morphology were considered to be a more reliable
way to distinguish monandry from diandry than
were external body characteristics such as colour,
as the two did not always correlate (Reinboth
1967a; Roede 1972, 1975; Dipper and Pullin 1979;
Bentivegna and Rasotto 1983; Bentivegna et al.
1985).
More recent research shows that based solely on
testicular morphology it is not always easy to
distinguish between the two developmental path-
ways of males. For example, in a number of
protogynous species in the Serranidae, Labridae
and Scaridae some testes are secondary in config-
uration but do not necessarily pass through a
functional female phase (Robertson and Warner
1978; Warner and Robertson 1978; Robertson
et al. 1982; Shapiro and Rasotto 1993; Siau 1994;
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 Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
De Girolamo et al. 1999; Fennessy and Sadovy
2002; Adams 2003; Liu and Sadovy 2004a,b). In
scarids such males were termed ‘functional ana-
logues’ of primary males (Robertson et al. 1982).
Inasmuch as this review is concerned with sexual
function, whenever there are clearly two distinct
pathways of sexual development in males of a
particular species or population, irrespective of
gonadal morphology, we consider that species to
be diandric. A single pathway of male development
would characterize a monandric species, irrespec-
tive of testicular morphology. We clarify any
confusing cases where there is a mismatch of
sexual function and gonadal morphology; for exam-
ple where a secondary testis is found in a primary
male.
Abnormal hermaphroditism
Abnormal hermaphroditism occurs in a number of
teleost families such as the Clupeidae, Esocidae,
Percidae and Bothidae. Occasionally gonads have
both mature testicular tissue with sperm and
ovarian tissue containing vitellogenic stage oocytes,
but this is unusual, as far as we can determine.
Such gonads arise with low incidence and mature
testicular and ovarian tissue configurations may
be inconsistent between individuals of a species
(Turner 1931; Dence 1938; Lagler and Chin
1951; Gutherz 1969; Dorfman and Heyl 1976;
Dominguez et al. 1989). The occurrence of abnor-
mal hermaphroditism may arise as a consequence
of endocrine-disrupting compounds or from other
chemicals.
Sexually transitional phase
In a sexually transitional phase the gonad shows
clear evidence of both testicular and ovarian tissues
showing degeneration of one sexually mature tissue
such as the breakdown of vitellogenic or later stage
oocytes of females in protogyny, and a proliferation
of the tissue of the other sex (Sadovy and Shapiro
1987). Alternatively, there may be other indications
of previous functioning of the first sex. The term
implies that a change of sex is occurring or
imminent and that the individual is between male
and female function. If no degeneration or indica-
tion of previous function of the first sex were
evident, without additional information it would
be difficult to distinguish a gonad in sexual transi-
tion from one that is a quiescent simultaneous
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hermaphrodite, or from one that is a sporadic
abnormal hermaphrodite.
Functional sex
The functional sex is the reproductive sex of an
individual. In a number of species great care is
needed in the assignment of functional sex if the
gonads are not examined or if egg or sperm release
is not observed. Using colour or behaviour alone to
assess sex can be misleading in some species (Atz
1964; Lodi 1967, 1980a,b; Roede 1972, 1975;
Ohm 1978, 1980; Robertson and Warner 1978;
Dipper and Pullin 1979; Bentivegna and Rasotto
1983; Kallman 1984; Bentivegna et al. 1985;
Carruth 2000).
Arrhenoidy and gynoidy
In arrhenoidy a female exhibits male sexual charac-
teristics while a male exhibits female sexual charac-
teristics in gynoidy. These external characteristics
have been used to infer functional sex or adult sex
change. However, using external sexual character-
istics to assign functional sex can be misleading.
Families in which functional hermaphroditism
is confirmed
Functional hermaphroditism as a naturally occur-
ring phenomenon is confirmed in 27 of 448 families
of teleost; this is in 7 of 40 orders (Table 1 and
Fig. 1). Good diagnostic criteria for functional
hermaphroditism include one or a combination of
the following: detailed gonadal histological series
ideally illustrated with photomicrographs that show
various stages of sexual transition, simultaneous
occurrence of mature testicular and ovarian tissues
in gonads and field or laboratory observations of
functional sex change in identified individuals
(Sadovy and Shapiro 1987; Sadovy and Domeier
2005). Weak diagnostic criteria include a bisexual
gonadal phase, a sex ratio biased by sex and age and
sexual dimorphism, which cannot be used alone. In
the following family accounts we identify sexual
patterns, summarize morphological information and
point to issues that need attention for better assessing
or understanding sexual pattern. Table 1 provides a
complete listing of all genera for which functional
hermaphroditism is confirmed and Table 2 summa-
rizes for each family both strong and weak diagnostic
criteria used in the published literature.
5
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Table 1 Functional hermaphroditism confirmed in 27 families of teleost fishes. For details of terminology see ‘Definitions’ in the text. Family classifications follow those of Nelson
(2006). For each family, both confirmed (+) and unconfirmed (*) genera are listed, and gonochorism is also indicated if it occurs in these genera. Numbers in parentheses indicate
the configurations of testicular and ovarian tissues in the gonads from early gonadal development or during sex change, with tissues of both sexes topographically separated
without connective tissue (1), by connective tissue (2) or not topographically separated at all (3). Whether or not the primary sex tissue remains in the gonads of sex-changed
individuals is not given as a category.

Sexual mode

Order–Family Genus Gonochorism Simultaneous Protogyny Protandry Bi-direction Reference

Anguilliformes
Muraenidae Echidna + *(3) Gonochorism confirmed: Fishelson (1992)
Gymnomuraena + *(3) Simultaneous confirmed: Fishelson (1992)
Gymnothorax +(1) *(3) Protogyny unconfirmed: Fishelson (1990, 1992)
Muraena + *(3) Protandry unconfirmed: Shen et al. (1979)
Rhinomuraena *(3)
Uropterygius *(3)

Stomiiformes
Gonostomatidae Cyclothone *(1) Confirmed: Kawaguchi and Marumo (1967)
Gonostoma *(1) Unconfirmed: Badcock and Merrett (1976), Fisher (1983),
Sigmops +(1) Miya and Nemoto (1985, 1987), Badcock (1986)
Aulopiformes
Chlorophthalmidae Chlorophthalmus +(1) Confirmed: Mead (1960)
Parasudis +(1)
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu

Ipnopidae Bathypterois +(1) Confirmed: Mead (1960), Fishelson and Galil (2001)
Bathytyphlops *(1) Unconfirmed: Merrett (1980)
Scopelarchidae Benthalbella +(1) Confirmed: Merrett et al. (1973)
Scopelarchus +(1)
Alepisauridae Alepisaurus *(1) Confirmed: Mead (1960), Merrett et al. (1973), Smith and
Omosudis +(1) Atz (1973)
Unconfirmed: Gibbs (1960), Mead (1960), Smith and Atz (1973)
Bathysauridae Bathysaurus +(1) Confirmed: Sulak et al. (1985)
Cyprinodontiformes
Rivulidae Kryptolebias +(1) Confirmed: Harrington (1961, 1967, 1971, 1975), Soto et al.
(1992), Cole and Noakes (1997), Sakakura et al. (2006)
Synbranchiformes
Synbranchidae Monopterus + +(1) Gonochorism confirmed: Liem (1968)

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 Table 1 Continued.

Sexual mode

Order–Family Genus Gonochorism Simultaneous Protogyny Protandry Bi-direction Reference

Ó 2008 The Authors

Ophisternon +(1) Protogyny confirmed: Liem (1963, 1968), Okada (1966a),
Synbranchus +(1) Chan and Phillips (1967), Chan et al. (1972), Lo Nostro and
Guerrero (1996)
Scorpaeniformes
Caracanthidae Caracanthus +(3) * Confirmed: Cole (2003), Wong et al. (2005)
Unconfirmed: Cole (2003)
Platycephalidae Cociella +(1) Confirmed: Aoyama et al. (1963), Okada (1966b, 1968),
Inegocia +(1) Fujii (1970, 1971, 1974), Shinomiya et al. (2003)
Kumococius +(1) Unconfirmed: Fujii (1974)
Onigocia +(1)
Rogadius *
Suggrundus +(1)

Perciformes
Centropomidae Centropomus +(1) Confirmed: Taylor et al. (2000)
Latidae Lates +(1) Confirmed: Moore (1979), Davis (1982), Guiguen et al. (1994)
Serranidae Anthias * Gonochorism confirmed: Sadovy and Colin (1995), Posada
Alphestes * (1996), Sadovy and Domeier (2005), Erisman et al. (2007)
Bullisichthys * Simultaneous confirmed: Clark (1959), Smith (1959), Smith
Centropristis +(1) and Atz (1969), Hastings (1973), Bortone (1977), Fischer

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Cephalopholis +(3) + (1980), Hastings and Bortone (1980), Hastings and Petersen
Chelidoperca +(1 & 3) (1986), Petersen and Fischer (1986), Abdel-Aziz and
Diplectrum +(1) Ramadan (1990), Petersen (1990), Garcı́a-Dı́az et al. (1997, 2002)
Epinephelus +(3) +(3) + Protogyny confirmed: Lavenda (1949), Smith (1959, 1965),
Hemanthias +(1) Okada (1965a), Reinboth (1963, 1965, 1967b), Moe (1969),
Hypoplectrodes * +(1 & 3) Fishelson (1970), Suzuki et al. (1974), Hastings (1981), Yogo
Hypoplectrus +(1) (1985), Wenner et al. (1986), Webb and Kingsford (1992),
Mycteroperca + +(3) Ferreira (1993, 1995), Mackie (1993, 2003), Shapiro et al.
Paralabrax +(3) * (1993), Siau (1994), Quinitio et al. (1997), Crabtree and
Plectropomus +(3) Bullock (1998), Fennessy and Sadovy (2002), Adams (2003)
Pseudanthias +(1 & 3) Bi-direction confirmed: Tanaka et al. (1990), Okumura (2001),
Pseudogramma +(1) Liu and Sadovy (2004a,b)
Rypticus * Gonochorism unconfirmed: Jones (1980a)
Sacura +(1) Simultaneous unconfirmed: Smith and Erdman (1973)
Serraniculus +(1) Protogyny unconfirmed: Reinboth (1964), Smith (1959,

7
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu

Serranus +(1) 1965), Nakai and Sano (2002)

 8
Table 1 Continued.

Sexual mode

Order–Family Genus Gonochorism Simultaneous Protogyny Protandry Bi-direction Reference

Pseudochromidae Anisochromis *(3) Bi-direction confirmed: Wittenrich and Munday (2005)

Ogilbyina * Protogyny unconfirmed: Springer et al. (1977), Fishelson
Pseudochromis * +(3) (1989)
Bi-direction unconfirmed: Ferrell (1987)
Nemipteridae Scolopsis +(1 & 3) Confirmed: Young and Martin (1985)
Lethrinidae Lethrinus *(3) +(3) Confirmed: Young and Martin (1982), Ebisawa (1997, 1999,
2006), Bean et al. (2003), Sumpton and Brown (2004)
Unconfirmed: Ebisawa (1990, 1999, 2006)
Sparidae Acanthopagrus +(2) Gonochorism confirmed: D’Ancona (1949), Reinboth (1962),
Boops *(2) *(2) Atz (1964), Penrith (1972), Mehl (1973), Joubert (1981),
Chrysoblephus +(2) +(2) Coetzee (1986), Buxton and Garratt (1990), Booth and Buxton
Dentex +(2) +(2) +(2) (1997), Goncalves and Erzini (2000), Grau et al. (2001),
Diplodus +(2) +(2) Hesp and Potter (2003)
Lithognathus +(2) +(2) Protogyny confirmed: Aoyama (1955), Reinboth (1962),
Pagellus +(2) *(2) +(2) +(2) Okada (1965b,c), Alekseev (1982), Garratt (1986), Lamrini
Pagrus +(2) +(2) (1986), Buxton (1990), Buxton and Garratt (1990), Kokokiris
Pterogymnus +(2) *(2) et al. (1999), Pajuelo and Lorenzo (1999)
Rhabdosargus +(2) *(2) +(2) Protandry confirmed: Kinoshita (1939), D’Ancona (1949),
Sarpa *(2) *(2) Lissia-Frau and Casu (1968), Lissia-Frau et al. (1976),
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu

Sparidentex +(2) Zohar et al. (1978), Abu-Hakima (1984), Coetzee (1986),

Sparus *(2) +(2) Pollock (1985), Yeung and Chan (1987), Buxton and Garratt
Spondyliosoma +(2) +(2) (1990), Chang and Yueh (1990), Krug (1990), Micale and
Perdichizzi (1994), Tobin et al. (1997), Mann and Buxton
(1998), Lone and Al-Marzouk (2000), Lee et al. (2001),
Pajuelo and Lorenzo (2001), Micale et al. (2002), Hesp et al.
(2004)
All unconfirmed: Atz (1964), Buxton and Garratt (1990)
Centracanthidae Spicara +(2) Confirmed: Zei (1949), Reinboth (1962), Sellami and Bruslé
(1979), Zamboni and Relini (1986), Dulčić et al. (2000)

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 Table 1 Continued.

Sexual mode

Order–Family Genus Gonochorism Simultaneous Protogyny Protandry Bi-direction Reference

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Pomacanthidae Centropyge +(1 & 3) + Protogyny confirmed: Moyer and Nakazono (1978a),
Chaetodontoplus * Suzuki et al. (1979), Bruce (1980), Hioki et al. (1982),
Genicanthus +(3) Aldenhoven (1984), Moyer and Zaiser (1984), Lutnesky
Holacanthus * (1994, 1996), Sakai (1997), Sakai et al. (2003b)
Pomacanthus * Bi-direction confirmed: Hioki and Suzuki (1996), Sakai et al.
(2003a)
Protogyny unconfirmed: Hourigan and Kelley (1985), Moyer
(1990), Arellano-Martı́nez (1997)
Cirrhitidae Amblycirrhitus * Protogyny confirmed and unconfirmed: Kobayashi and Suzuki
Cirrhitichthys +(1 or 1 & 3) + (1992), Sadovy and Donaldson (1995)
Cirrhitops * Bi-direction confirmed: Kobayashi and Suzuki (1992)
Cirrhitus *
Cyprinocirrhites *
Neocirrhitus +(1 & 3)
Pomacentridae Amphiprion +(1) Gonochorism confirmed: Godwin (1995), Asoh et al. (2001),
Dascyllus + +(3) Asoh and Kasuya (2002), Asoh (2004)
Protogyny confirmed: Coates (1982), Schwarz and
Smith (1990), Cole (2002), Asoh and Yoshikawa (2003)
Protandry confirmed: Fricke and Holzberg (1974), Fricke and

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Fricke (1977), Moyer and Nakazono (1978b), Fricke (1979,
1983), Wood (1981), Yanagisawa and Ochi (1986), Ochi
(1989), Hattori and Yanagisawa (1991a,b), Shapiro (1992),
Godwin (1994)

9
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
 Table 1 Continued.

10
Sexual mode

Order–Family Genus Gonochorism Simultaneous Protogyny Protandry Bi-direction Reference

Labridae Achoerodus +(3) Gonochorism confirmed: Dipper and Pullin (1979),

Anampses * Hoffman (1980), Bentivegna and Benedetto (1989), Denny
Bodianus + +(3) and Schiel (2002)
Cheilinus +(3) Protogyny confirmed: Okada (1962), Reinboth (1962), Roede
Choerodon +(3) (1972, 1975), Warner (1975b), Davis (1976), Kuhn (1976),
Cirrhilabrus +(3) McPherson (1977), Warner and Robertson (1978), Dipper
Clepticus +(3) and Pullin (1979), Nakazono (1979), Hoffman (1980, 1983),
Coris +(1 & 3) Jones (1980b), Tribble (1982), Bentivegna and Rasotto
Epibulus * (1983), Ross et al. (1983), Bentivegna and Cirino (1984),
Halichoeres +(3) + Ross (1984), Bentivegna et al. (1985), Hoffman et al. (1985),
Hologymnosus +(3) Nemtzov (1985), Warner and Lejeune (1985), Yogo (1985),
Labroides + Kobayashi and Suzuki (1990, 1994), Nakazono and Kusen
Labrus +(3) (1991), Warner and Swearer (1991), Shibuno et al. (1993),
Lachnolaimus +(3) Ebisawa et al. (1995), Gillanders (1995), Andrew et al.
Nelabrichthys +(3) (1996), Leem et al. (1998), McBride et al. (2001), Platten
Notolabrus + +(3) et al. (2002), Sadovy et al. (2003), Candi et al. (2004), Choat
Parajulis +(3) et al. (2006), Munday et al. (2006b)
Pseudolabrus +(3) + Bi-direction confirmed: Nakashima et al. (2000), Kuwamura
Pteragogus +(3) et al. (2002, 2007), Ohta et al. (2003)
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu

Semicossyphus +(3) Protogyny unconfirmed: Warner and Lejeune (1985),

Stethojulis +(3) Leem et al. (1998)
Symphodus + +(3)
Thalassoma +(3)
Xyrichtys +(3)
Scaridae Calotomus +(3) Gonochorism confirmed: Robertson and Warner (1978),
Chlorurus +(3) Gonzales and Lozano (1992), De Girolamo et al. (1999)
Cryptotomus +(3) Protogyny confirmed: Reinboth (1968), Choat and Robertson
Scarus +(3) (1975), Robertson and Warner (1978), Clavijo (1982),
Sparisoma + +(3) Robertson et al. (1982), Yogo (1985), Kusen and Nakazono
(1991), Koltes (1993), Muñoz and Warner (2003)
Pinguipedidae Parapercis +(3) Confirmed: Stroud (1982), Nakazono et al. (1985), Ohta
(1987), Kobayashi et al. (1993)

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 Table 1 Continued.

Sexual mode

Order–Family Genus Gonochorism Simultaneous Protogyny Protandry Bi-direction Reference

Ó 2008 The Authors

Trichonotidae Trichonotus +(3) Confirmed: Kusen et al. (1991)
Gobiidae Bryaninops *(3) *(1) Gonochorism confirmed: Robertson and Justines (1982), Cole
Coryphopterus + +(3) (1988, 1990), Fishelson (1989), Cole et al. (1994)
Elacatinus + +(3) Protogyny confirmed: Robertson and Justines (1982), Cole
Eviota +(3) (1983, 1988, 1990), Cole and Robertson (1988), Fishelson
Fusigobius * (1989), Cole and Shapiro (1990, 1992, 1995)
Gobiodon +(3) + Bi-direction confirmed: Sunobe and Nakazono (1993),
Hetereleotris * Kuwamura et al. (1994), Nakashima et al. (1995, 1996),
Lophogobius + * Munday et al. (1998), Cole and Hoese (2001), Rodgers et al.
Luposicya * (2005, 2007), Lorenzi et al. (2006)
Lythrypnus +(3) +(3) Simultaneous unconfirmed: Cole (1990)
Paragobiodon +(3) + Protogyny unconfirmed: Fishelson (1989), Cole (1990)
Pleurosicya * Bi-direction unconfirmed: Cole (1990), Sunobe and
Priolepis * +(1) * Nakazono (1999), Munday et al. (2002)
Trimma +(1) +

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11
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu

Figure 1 Teleost phylogeny in orders (modified from Nelson 2006) showing the incidence of functional hermaphroditism,
both confirmed and not confirmed, in bold. Data in parentheses represent the total number of species in each order,
and the percentage of those species that are marine. 1, simultaneous hermaphroditism; 2, sequential hermaphroditism.
Superscripts indicate where functional hermaphroditism is confirmed, and subscripts indicate where it is not
confirmed, at family level (see Tables 1 and 2 for details).

Protogyny was proposed, but has not yet been

Elopomorpha – Anguilliformes
Muraenidae (Heteromyridae) (moray eels)
Simultaneous hermaphroditism is confirmed in two
species of the genus Gymnothorax (synonyms
Lycodontis, Rabula), G. griseus (=Siderea grisea) and
G. pictus (=S. picta), and gonochorism in three gen-
era, Echidna, Gymnomuraena and Muraena (Table 1).
12 Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–43
confirmed, in five genera, Echidna, Gymnomuraena,
Gymnothorax, Muraena and Uropterygius. Protandry
is widely cited for Rhinomuraena quaesita on the basis
of colouration, but not confirmed. Interestingly,
gonads exhibiting both testicular and ovarian tissues
were also found in other families of the order living
in similar deep-sea habitats, including Chlopsidae
Ó 2008 The Authors
 Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu

Table 2 All diagnostic criteria, both strong (+) and weak (*) used for determining functional hermaphroditism in both
confirmed and not confirmed (with italics in the first column) families. For details of gonadal morphology, see ‘Definitions’
in text. Family orders and references as in Tables 1 and 3, and also in the text.

Diagnostic criteria

Gonad morphology Observation of sex change

Size/age-biased
Family Bisexual Simultaneous Transition sex ratio Sexual dimorphism Field Laboratory

Muraenidae * + *
Clupeidae * *
Cyprinidae * *
Cobitidae * *
Gonostomatidae * + *
Chlorophthalmidae +
Notosudidae *
Ipnopidae * +
Scopelarchidae +
Evermannellidae *
Alepisauridae * +
Paralepididae *
Bathysauridae +
Rivulidae + +
Poeciliidae * *
Synbranchidae * + * +
Caracanthidae * * +
Platycephalidae + * +
Centropomidae +
Latidae + * + +
Moronidae * *
Serranidae * + + * + +
Pseudochromidae * * +
Grammatidae * *
Malacanthidae * * *
Nemipteridae + *
Lethrinidae + *
Sparidae * + * + +
Centracanthidae + *
Polynemidae * *
Chaetodontidae *
Pomacanthidae + * + +
Terapontidae * *
Cirrhitidae + * +
Cepolidae *
Cichlidae * *
Pomacentridae + * + +
Labridae * + * + +
Odacidae * *
Scaridae * + * +
Eleginopidae * *
Pinguipedidae + * + +
Trichonotidae + * *
Percophidae *
Blenniidae *
Gobiidae + + * + +
Balistidae * * *
Ostraciidae * *

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Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
(Xenocongridae), Congridae, Derichthyidae, Murae-
nesocidae, Serrivomeridae and Syanphobranchidae;
likewise Eurypharyngidae (Saccopharyngiformes,
Elopomorpha) (Fishelson 1994). Whether sequential
hermaphroditism actually occurs in the Elopo-
morpha remains to be determined.
Euteleostei – Stenopterygii – Stomiiformes
Gonostomatidae (bristlemouths)
Protandry is confirmed for Sigmops gracilis (=Gonos-
toma gracile) (Table 1). Immature ovarian tissue
arises from within narrow regions interspersed
between larger active sections of the testis during
sexual transition (Kawaguchi and Marumo 1967).
Protandry was proposed in two genera, Cyclothone
and Gonostoma. Species in the family occur in deep-
sea habitats.
Euteleostei – Cyclosquamata – Aulopiformes
Chlorophthalmidae (greeneyes), Ipnopidae (deepsea
tripod fishes), Scopelarchidae (pearleyes), Alepisauridae
(lancetfishes) and Bathysauridae (deepsea lizardfishes)
Simultaneous hermaphroditism is established in two
genera of chlorophthalmids, Chlorophthalmus brasil-
iensis and Parasudis truculenta (=P. truculentus), in
two scopelarchids, Benthalbella infans (=Neoscopelar-
choides infans) and Scopelarchus guntheri, in one genus
of ipnopid, Bathypterois (synonym Benthosaurus), an
alepisaurid, Omosudis lowii (=O. lowei), and a bathy-
saurid, Bathysaurus (synonym Macristium) (Table 1).
Although the determination of sexual pattern in
some species is based on small sample sizes, gonadal
details provide clear evidence for simultaneous mat-
uration of testicular and ovarian tissues; the deep-sea
distribution of these fishes makes sampling a chal-
lenging task. It would be of interest to study the
sexual pattern of shallow water aulopiforms to test
for possible environmental correlates among related
species across different habitats. Simultaneous her-
maphroditism was also proposed in the ipnopid
Bathytyphlops (synonym Macristiella) sewelli, and
the alepisaurid Alepisaurus ferox (Table 1), but
gonadal tissue was either immature or too poor for
a reliable evaluation of sexual pattern.
Euteleostei – Acanthopterygii – Cyprinodontiformes
Rivulidae (New World rivulines)
Following the remarkable discovery by Harrington
(1961) of all-female populations of Kryptolebias
14 Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–43
marmoratus (=Rivulus marmoratus) in the wild, and
the subsequent reproduction by all-female broods,
simultaneous hermaphroditism with self-fertiliza-
tion was established (Table 1). This is the only
cyprinodontid known to be hermaphroditic and, as
a self-fertilizing species, may be unique amongst
vertebrates; it is also the only family member with
marine affiliations, living in mangrove habitats. In
the paired hermaphroditic gonads sperm sinuses
unite posteriorly to form a sperm duct in the
testicular areas, and the ovarian lumen or the
gonadal lumina from each lobe unite posteriorly to
form an oviduct or common genital sinus in ovarian
areas (Harrington 1967, 1971, 1975; Soto et al.
1992; Cole and Noakes 1997; Sakakura et al.
2006). Free sperm found in the posterior area of
the ovarian lumen suggest where self-fertilization
might occur (Sakakura et al. 2006). Secondary
males derived from simultaneous hermaphrodites
through loss of female function occur under certain
laboratory conditions and are not known from the
wild (Harrington 1971, 1975). Gonochoristic males
derived directly from sexual differentiation at first
maturation are found both in laboratory and
natural conditions (Harrington 1967, 1971). Testes
of gonochoristic males contain no evidence of
oocytes or of an ovarian lumen and testicular tissue
packs solidly, a typical feature of gonochoristic
males in teleosts (Soto et al. 1992).
Euteleostei – Acanthopterygii – Synbranchiformes
Synbranchidae (swamp eels)
Protogyny is confirmed in three genera, Monopterus
albus (=Fluta alba, Monopterus javanensis), M. boueti
(=Typhlosynbranchus boueti), Ophisternon bengalense
(=Synbranchus bengalensis) and Synbranchus marmo-
ratus, with both gonochorism and protogyny occur-
ring in Monopterus (Table 1). Two different
testicular morphologies suggest two male develop-
mental pathways, indicating diandry in these spe-
cies (Liem 1968; Lo Nostro and Guerrero 1996).
The ovary is unusual in being a single lobe
surrounded by a thick connective tissue tunica;
two ovarian lamellae fold to form two ovarian
cavities, suspended within the cavity into which
mature oocytes are released (Okada 1966a; Liem
1968). Testes of secondary males retain the lamellar
organization from the female phase. Ovarian tissue
in the outer half of the lamellae degenerates
during sexual transition (Okada 1966a; Chan and
Phillips 1967; Liem 1968; Lo Nostro and Guerrero
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 Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
1996). The two ovarian cavities do not function
for sperm release; instead, a new sperm duct system
develops within the lamellae (Lo Nostro and
Guerrero 1996). Testes of primary males consist of
a pair of solid lobes and exhibit no ovarian lamellar
organization (Liem 1968; Lo Nostro and Guerrero
1996).
Euteleostei – Acanthopterygii – Scorpaeniformes
Caracanthidae (orbicular velvetfishes)
Protogyny is confirmed in the only caracanthid
genus Caracanthus, for C. typicus and C. unipinna
(Table 1). Testes retain a lumen from the female
phase and form peripheral sperm sinuses within the
ovarian wall. Ovaries exhibit an unusual morphol-
ogy in which a centrally located lobe of ovarian
tissue is completely surrounded by a peripheral
lumen (Cole 2003; Wong et al. 2005). A low
incidence of bi-directional sex change under
laboratory conditions was proposed for C. typicus
(Cole 2003).
Platycephalidae (flatheads)
Protandry is confirmed in five genera of onigociines,
Cociella, Inegocia, Kumococius, Onigocia and Suggrun-
dus; there are several different gonad configurations
in the family (Table 1). In C. crocodila (=Inegocia
crocodilia), K. rodericensis (=K. detrusus) and
S. meerdervoortii (=Inegocia meerdervoorti) juveniles
pass through a bisexual gonadal phase and a lumen
is already present at male maturation before sex
change; this form is termed the Kumococius type
(Aoyama et al. 1963; Okada 1966b, 1968; Fujii
1970, 1971, 1974). In Inegocia and Onigocia the
ovarian lumen forms de novo during sexual transi-
tion through structural re-organization of the gonad
whereby ovarian tissue develops ventrally by out-
folding. In Onigocia juveniles have a bisexual
gonadal phase and sex change occurs by the
appearance of an ovarian lumen, degeneration of
testicular tissue and development of ovarian tissue;
this is termed the Onigocia type (Fujii 1974). In
I. japonica the testes do not contain ovarian tissue in
the juvenile phase and sex change occurs through
the appearance of ovarian tissue and by the
formation of an ovarian lumen, termed the Inegocia
type (Fujii 1971). Protandry was also proposed for
Rogadius asper, but without histological details.
Phylogenetically (Imamura 1996), gonadal
development and sexual pattern vary among the
species, from protandrous hermaphroditism, which
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varies from the Kumococius type to the Onigocia type
to the Inegocia type, to gonochorism (Fujii 1974).
Fujii (1974) noted that gonochorism tends to be
found in larger or more specialized species. Consis-
tent with this pattern the more derived Platycephalus
indicus is gonochoristic (Fujii 1974; V.C.M. Ho,
personal communication).
Euteleostei – Acanthopterygii – Perciformes
Centropomidae (snooks)
Protandry is confirmed for Centropomus undecimalis
(Table 1). The ovarian lumen forms de novo through
structural re-organization of the gonad during
sexual transition; the testicular tissue degenerates
within the solid lobes of the testes and the ovarian
tissue subsequently develops from the ventral areas
of the lobes (Taylor et al. 2000).
Latidae (lates)
Protandry is confirmed for Lates calcarifer (Table 1).
The ovarian lumen forms de novo through structural
re-organization of the gonad during sexual transi-
tion; the testicular tissue degenerates within the
solid lobes of the testes and the ovarian tissue arises
from ventral areas of the lobes (Guiguen et al.
1994). When it occurs, sex change proceeds rapidly
in the species but may occur infrequently (Moore
1979; Davis 1982).
Serranidae (sea basses)
Serranids exhibit great diversity in sexual patterns
even within certain genera. Simultaneous hermaph-
roditism, protogyny and bi-directional sex change
are well documented and gonochorism also occurs;
there are no reports of protandry in the family
(Table 1). Simultaneous hermaphroditism is con-
firmed in four genera of serranines, Diplectrum,
Hypoplectrus, Serraniculus and Serranus, and one
genus of epinepheline, Pseudogramma. In these
species sperm duct and oviduct are separate sug-
gesting that internal self-fertilization does not occur.
An example of the complexities of sexual expression
in the family is evident in Serranus baldwini and
S. fasciatus which exhibit a combination of simulta-
neous and sequential hermaphroditism; smaller
individuals within a social group are simultaneous
hermaphrodites, while the largest often lose female
function and reproduce exclusively as a male
(Hastings and Petersen 1986; Petersen and
Fischer 1986). Similarly, larger individuals of the
simultaneous P. gregoryi (=P. bermudensis) show
15
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
progressive masculinization of ovarian lobes (Smith
and Atz 1969). In such cases direct observation of
reproductive activity may be the only way to
determine the functional sex of specific individuals.
In P. gregoryi testicular tissue arises as a single
median lobe within the dorsal oviduct, a unique
reproductive structure in the family (Smith and Atz
1969). It is most likely that simultaneous hermaph-
roditism is also present in one genus of serranine
Bullisichthys (Smith and Erdman 1973).
Protogyny is confirmed in two genera of serra-
nines, Centropristis and Chelidoperca (Lavenda 1949;
Reinboth 1965, 1967b; Wenner et al. 1986), four
genera of anthiines, Hemanthias, Hypoplectrodes,
Pseudanthias and Sacura (Reinboth 1963; Okada
1965a; Fishelson 1970; Suzuki et al. 1974;
Hastings 1981; Shapiro 1981; Yogo 1985; Webb
and Kingsford 1992), and four genera of epineph-
elines, Cephalopholis, Epinephelus, Mycteroperca and
Plectropomus (Smith 1959, 1965; Moe 1969; Ferre-
ira 1993, 1995; Mackie 1993, 2003; Shapiro et al.
1993; Siau 1994; Crabtree and Bullock 1998;
Fennessy and Sadovy 2002; Adams 2003). In most
protogynous serranids the testes exhibit the mor-
phology of secondarily derived males with a lumen
and lamellar configuration of the earlier ovarian
phase, and sperm sinuses within the gonadal wall
irrespective of the male pathway of development.
Males can develop from adult females through sex
change or from the juvenile phase. The only possible
exception to this pattern is Pseudanthias squamipinnis
(=Anthias squamipinnis, Franzia squamipinnis), in
which approximately half of the testes showed no
evidence of a former ovarian morphology because
the lumen becomes occluded in some ripe testes
(Shapiro 1981). Most protogynous species appear to
be monandrous, although diandry is confirmed for
Cephalopholis taeniops, Epinephelus andersoni,
Plectropomus leopardus and P. maculatus (Siau
1994; Fennessy and Sadovy 2002; Adams 2003),
and bi-directional sex change occurs in C. boenak
and E. akaara under laboratory conditions (Tanaka
et al. 1990; Okumura 2001; Liu and Sadovy
2004a). In E. striatus although the studied popula-
tion was gonochoristic through being non-func-
tional hermaphroditic, the authors suggested that
the species might also have exhibited diandry had
not overfishing eliminated the largest males, which
are those most likely to be secondarily derived
(Sadovy and Colin 1995). Protogyny is unconfirmed
for the anthiine Anthias anthias (Reinboth 1964)
and the epinephelines Alphestes afer, Cephalopholis
16 Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–43
urodeta and Rypticus species (Smith 1959, 1965;
Nakai and Sano 2002).
In protogynous serranids there are three ways in
which testicular tissue arises within the ovary. The
relationship between testicular and ovarian tissues
ranges from topographical separation to complete
integration (Smith 1965; Yamamoto 1969;
Hastings 1981; Sadovy and Shapiro 1987; Baldwin
and Johnson 1993; Sadovy and Domeier 2005). In
the serranine Centropristis striatus, and the anthiines
Hemanthias vivanus and Sacura margaritacea, testic-
ular tissue proliferates from discrete testicular islets
that are present from early gonadal development at
the junction of the alamellar ovarian wall and
lamellae of functional ovaries. This replaces regress-
ing ovarian tissue during sexual transition. In this
way testicular tissue does not intermix with ovarian
tissue (Reinboth 1963, 1965; Okada 1965a;
Hastings 1981; Wenner et al. 1986). By contrast,
in the serranine Chelidoperca hirundinacea, and the
anthiines Hypoplectrodes maccullochi (=Ellerkeldia
maccullochi) and Pseudanthias squamipinnis, testicu-
lar tissue is located both along the germinal
epithelia of ovarian lamellae as well as in distinct
testicular islets from the ovarian wall (Reinboth
1967b; Shapiro 1981; Webb and Kingsford 1992).
In the epinephelines Cephalopholis, Epinephelus,
Mycteroperca and Plectropomus, testicular tissue
arises sporadically throughout the germinal epi-
thelia of ovarian lamellae rather than from dis-
crete islets (Smith 1965). In some Cephalopholis,
Epinephelus and Plectropomus species, testicular
tissue is occasionally visible in ovarian lamellae
scattered throughout the juvenile and female
phases, and primary-growth stage oocytes some-
times remain in the testes after sex change (Smith
1965; Moe 1969; Tanaka et al. 1990; Siau 1994;
Chan and Sadovy 2002; Fennessy and Sadovy
2002; Adams 2003; Liu and Sadovy 2004a,b).
A principal reason for the difficulty in distin-
guishing gonochorism in the family is the lack of a
morphological distinction in testicular structure
between primary and secondary males. Gonocho-
rism is known in the serranine Paralabrax species,
and the epinephelines E. striatus, Mycteroperca
rosacea and Paranthias furcifer (Sadovy and Colin
1995; Posada 1996; Sadovy and Domeier 2005;
Erisman et al. 2007). Paralabrax is particularly
interesting because over 40 years both protogyny
and gonochorism were variously proposed (Smith
and Young 1966; Borquez et al. 1988; Hastings
1989; Oda et al. 1993; Hovey and Allen 2000).
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 Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
A more detailed study on several species of the
genus confirmed all to be gonochoristic; it is the
early juvenile bisexual phase that has caused much
of the confusion (Sadovy and Domeier 2005).
Sexual pattern in the temperate anthiine Hypoplec-
trodes huntii (=Ellerkaldia huntii) is uncertain; testes
appeared to be solid with no ovarian lumen and
contained primary-growth stages oocytes (Jones
1980a).
Confirmation of functional sexual pattern in ser-
ranids requires considerable care. A wide-size range
of adult and juvenile individuals needs to be exam-
ined histologically. Deciding on the functional sexual
pattern demands the detection of gonads in transition
between female and male function, together with, if
possible, the observation of sex change under field or
laboratory conditions (Sadovy and Shapiro 1987;
Adams 2003; Liu and Sadovy 2004a,b).
Pseudochromidae (dottybacks)
Following earlier reports of protogyny (Fishelson
1989) bi-directional sex change has been confirmed
for three species of the pseudochromine genus
Pseudochromis, P. aldabraensis, P. cyanotaenia
and P. flavivertex under laboratory conditions
(Wittenrich and Munday 2005) (Table 1). Bi-direc-
tional sex change was also proposed for the
pseudochromine Ogilbyina queenslandiae on the basis
of changes in body colouration of tagged fish under
field conditions (Ferrell 1987). Protogyny was
proposed for the anisochromine Anisochromis stra-
ussi (Springer et al. 1977). Histological analysis of
more specimens is needed for confirmation in the
latter two species.
Nemipteridae (threadfin breams)
Monandric protogyny is confirmed for two species
of the genus Scolopsis, S. monogramma and
S. taenioptera (=S. taeniopterus) (Table 1). Within
the family testicular morphology varies along
phylogenetic lines. In protogynous Scolopsis species
testes exhibit the typical configuration of a second-
ary male with lamellar structure and an ovarian
lumen. The ovaries themselves do not contain
testicular tissue (Young and Martin 1985). During
sexual transition there are two ways in which
testicular tissue may arise within the ovary,
sporadically throughout the germinal epithelia
in S. monogramma, and from the junction of
the alamellar ovarian wall and lamellae in
S. taenioptera. In the gonochoristic Nemipterus pero-
nii, Parascolopsis species and Pentapodus porosus,
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testes are typical of gonochoristic males (Young and
Martin 1985). However, among other gonochoristic
Nemipterus species, although the testes are solid,
there is an accessory duct with lamellar structure
remnants located on the dorsal side of a solid testis
and separated from the testicular tissue by connec-
tive tissue (Young and Martin 1985; Takahashi
et al. 1989; Lau and Sadovy 2001). The dorsal
accessory duct appears to be homologous to the
ovary and persists from the juvenile phase with
occasional primary-growth stage oocytes occurring
in the lamellae of the duct (Takahashi et al. 1989;
Lau and Sadovy 2001). The testicular morphology
in these Nemipterus species shows similarities to that
of sparids and centracanthids, which are closely
related families.
Lethrinidae (emperors or emperor breams)
Protogyny is confirmed for six species of the genus
Lethrinus, L. atkinsoni, L. genivittatus, L. lentjan,
L. miniatus, L. rubrioperculatus and L. variegatus
(Table 1). In most species, small crypts of gonia
occur adjacent to the germinal epithelia of the
lamellae in mature ovaries and proliferation of
testicular tissue occurs within these crypts as
oocytes degenerate during sexual transition.
Although some species showed the typical size-
specific sex ratios for a monandric protogynous
species, with larger males and smaller females on
average, in many cases there was considerable
male–female overlap in size. There may be primary
males with testes having an ovarian structure with
a lumen. Gonochorism was inferred for three
species, L. atkinsoni, L. nebulosus and L. obsoletus as
sizes of males and females overlapped and male
gonad morphology is typical of secondarily derived
testes (Ebisawa 1990, 1999, 2006).
Sparidae (porgies)
This family is one of the most sexually diverse of
all teleosts, exhibiting gonochorism to sequential
hermaphroditism and regularly including both
protogyny and protandry within a single genus,
and a bisexual gonadal phase during juvenile sexual
development. They possibly also exhibit simulta-
neous hermaphroditism (Table 1). Protogyny is
confirmed in five genera, Chrysoblephus, Dentex,
Pagellus, Pagrus and Spondyliosoma, and protandry
in eight genera, Acanthopagrus, Dentex, Diplodus,
Lithognathus, Pagellus, Rhabdosargus, Sparidentex and
Sparus. In each of the genera Dentex and Pagellus,
gonochorism, protogyny and protandry occur; in
17
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
others, either protogyny or protandry and gonoch-
orism. Both simultaneous and protandrous her-
maphroditism are suggested for Pagellus bogaraveo
(=P. centrodontus) and Sparus aurata (=Sparus aura-
tus, Chrysophrys aurata) (Atz 1964; Buxton and
Garratt 1990), but only protandry is confirmed
(D’Ancona 1949; Zohar et al. 1978; Krug 1990;
Micale et al. 2002).
Variations in early development and gonadal
configuration within the family make diagnosis of
sexual pattern particularly challenging. Both testic-
ular and ovarian tissues are usually present.
Depending on the sexual phase, one portion of the
gonad predominates while the other is visible as a
small crest or degenerated rudiment of testicular
tissue in protandrous species or as a peripheral
remnant with a residual ovarian lumen in those
species that are protogynous. Largely due to
gonadal configuration and the variable rigour of
histological studies conducted, workers differed in
their conclusions on sexual pattern, variously
proposing protogyny or protandry and possible
gonochorism for species such as Boops boops, Litho-
gnathus mormyrus (=Pagellus mormyrus), Rhabdosar-
gus globiceps and Sarpa salpa (=Boops salpa)
(reviewed in Buxton and Garratt 1990).
Differing diagnoses may also arise due to
geographical variation in sexual pattern. For
example, in the protogynous Pagrus caeruleostictus
(=P. ehrenbergi, Sparus caeruleostictus), the propor-
tion of the total population changing sex varies
geographically (Alekseev 1983). In Diplodus annu-
laris (=Dilodus annularis and Sargus annularis) the
sexual pattern was proposed to be gonochorism or
protandry in individual fish from the Mediterranean
Sea (D’Ancona 1949; Reinboth 1962) and protan-
dry in the Black Sea (Salekhova 1961). In Rhabdo-
sargus sarba (=Sparus aries) gonochorism is
confirmed in Australian waters (Hesp and Potter
2003) and protandry in Asia (Kinoshita 1939;
Yeung and Chan 1987).
Clarifications on sexual pattern in the family will
emerge with more detailed studies, especially when
these include early gonadal development, a wide
range of sizes and experimental observation. For
example, Pagrus major (=Chrysophrys major) and
Pterogymnus laniarius were initially proposed as
protogynous (Huang et al. 1974; Hecht and Baird
1977), but later confirmed as gonochoristic
(Matsuyama et al. 1988; Booth and Buxton 1997).
Gonochorism was initially proposed for Diplodus
sargus (D’Ancona 1949; Joubert 1981); however,
18 Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–43
protandry with possible digyny was later confirmed
(Coetzee 1986; Micale and Perdichizzi 1994; Mann
and Buxton 1998; Pajuelo and Lorenzo 2001).
Centracanthidae (Maenidae) (picarel porgies)
Protogyny is confirmed for two species of the genus
Spicara, S. maena (=Maena maena, S. chrysalis,
S. flexuosa) and S. smaris (Table 1). As in the
sparids, testicular and ovarian tissues in the Centr-
acanthidae are topographically separated by con-
nective tissue. Most individuals mature as females,
and contain presumptive testicular tissue as an
aggregation of undifferentiated germ cells. During
sexual transition, ovarian tissue degenerates and
testicular tissue proliferates while an ovarian lumen
and lamellar structure remnant may persist in
testes. It is possible that some males develop directly
from the juvenile phase and do not undergo sex
change (Reinboth 1962; Sellami and Bruslé 1979;
Zamboni and Relini 1986).
Pomacanthidae (angelfishes)
Sequential hermaphroditism, which can be both
protogynous and bi-directional, is confirmed in the
family (Table 1). Protogyny was first reported for
Genicanthus semifasciatus (Shen and Liu 1976) and
is now confirmed in two genera, Centropyge (syno-
nym Sumireyakko) and Genicanthus species.
Although testes typically exhibit the morphology
of secondarily derived males there are exceptions.
For example, in C. bicolor, although a residual
ovarian lumen is found in all testes the gonad often
loses its lamellar form (Aldenhoven 1984). Inter-
estingly, in C. interruptus, unlike in other pom-
acanthids, testicular tissue develops from a
labyrinth-like structure at the periphery of the
gonad that has not been seen in any other fish
species (Moyer and Nakazono 1978a). During
sexual transition the testicular tissue proliferates
within this structure and the ovarian tissue subse-
quently diminishes. Bi-directional sex change is
confirmed in four species of the genus Centropyge,
C. acanthops, C. ferrugata, C. fisheri and C. flavissima
(=C. flavissimus), by demonstrating functional
female to male and then back to female sex change
under laboratory conditions, changes diagnosed on
the basis of gonadal histology and gamete release
(Hioki and Suzuki 1996; Sakai et al. 2003a).
Protogyny was proposed in several species within
three genera, Chaetodontoplus mesoleucus, Holacan-
thus tricolor, H. passer and Pomacanthus zonipectus.
The evidence came mainly from the skewed sex
Ó 2008 The Authors
 Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
ratio towards females and the fact that males
are larger than females on average (Table 1). In
H. tricolor, the only promising evidence was the
existence of sperm sinuses within the gonadal wall,
reminiscent of secondarily derived sperm transport
systems, and a single possible sexual transitional
individual identified on the basis of cell clusters
tentatively recognized as early testicular tissue;
small lumina were apparent in some gonadal
sections (Hourigan and Kelley 1985). The sexual
pattern in these genera awaits confirmation.
Cirrhitidae (hawkfishes)
Protogyny is confirmed in two genera, Cirrhitichthys
and Neocirrhitus (Table 1). The testes typically
exhibit the testicular morphology of secondarily
derived males with an ovarian lumen and with
peripheral sperm sinuses (Kobayashi and Suzuki
1992; Sadovy and Donaldson 1995). Bi-directional
sex change is confirmed for C. aureus following sex
change in both directions under laboratory condi-
tions (Kobayashi and Suzuki 1992). Protogyny also
seems likely in four other genera, Amblycirrhitus
pinos, Cirrhitops hubbardi, Cirrhitus pinnulatus and
Cyprinocirrhites polyactis (Kobayashi and Suzuki
1992; Sadovy and Donaldson 1995). In these species
few samples were examined and further histological
evidence is needed to establish protogyny.
Histological evidence for protogyny indicates that
in some Cirrhitichthys species the gonads are
initially entirely ovarian and that testicular tissue
arises later in discrete islets at the junction between
the lamellar and alamellar zones of the ovary.
Eventually testicular tissue invades the ovaries with
primary-growth stage oocytes remaining present
(Kobayashi and Suzuki 1992; Sadovy and Donald-
son 1995). In Neocirrhitus armatus and some other
Cirrhitichthys species, on the other hand, testicular
tissue arises sporadically throughout the ovarian
lamellae as well as at the junction between the
lamellar and alamellar zones of the ovary (Sadovy
and Donaldson 1995).
Pomacentridae (damselfishes)
The pomacentrids exhibit both protandry and pro-
togyny (Table 1). Protandry is confirmed for about
10 anemonefish species of the amphiprionine genus
Amphiprion, which includes Premnas (Nelson 2006).
The gonads of juveniles exhibit a bisexual phase
containing distinct testicular and ovarian tissue
areas; the testicular tissue matures first and the
ovarian area remains in the form of primary-growth
Ó 2008 The Authors
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stage oocytes. During sexual transition the ovarian
lumen forms de novo through structural re-organi-
zation of the gonad and testicular tissue disappears
from the functional ovaries after the sex change
(Fricke and Fricke 1977; Moyer and Nakazono
1978b; Bruslé-Sicard and Reinboth 1990; Hattori
and Yanagisawa 1991a; Shapiro 1992; Godwin
1994).
Protogyny is now confirmed for three damselfish
species of the chromine genus Dascyllus, D. aruanus,
D. carneus and D. reticulatus (Table 1). In these
species testes exhibit the typical configuration of a
secondary male but do not contain ovarian tissue.
During sexual transition testicular tissue develops
throughout the germinal epithelia of the ovarian
lamellae and finally displaces ovarian tissue. The
existence of small males in these species with body
size similar to the smallest mature females indicates
possible diandry (Schwarz and Smith 1990; Cole
2002; Asoh and Yoshikawa 2003). While protog-
yny was proposed for three other species of the
genus Dascyllus, D. albisella, D. trimaculatus and
D. marginatus (Shpigel and Fishelson 1986), more
recent studies confirmed gonochorism in the form of
non-functional hermaphroditism for the first two
and for D. flavicaudus (Godwin 1995; Asoh et al.
2001; Asoh and Kasuya 2002; Asoh 2004).
Assessment of sexual pattern is difficult in the
damselfishes and needs care for two reasons. First,
pomacentrids for which there are sufficiently
detailed histological studies appear to pass through
a bisexual gonadal phase with or without a lumen.
Such a bisexual phase is found in some juveniles of
both functional hermaphrodites and gonochores;
Stegastes partitus and Parma macrolepis are gonoch-
ores, with the former having a juvenile bisexual
condition and a typical gonochore testis (Sadovy
1986; Tzioumis and Kingsford 1999; Asoh et al.
2001; Asoh and Kasuya 2002; Asoh 2003, 2004).
On the other hand, the gonochoristic Acanthochr-
omis polyacanthus does not have a juvenile bisexual
phase and all males have the typical testicular
morphology of gonochores (P.L. Munday, personal
communication). Moreover, the influence of social
factors on initial functional sex development as
opposed to adult sex change is indicated in several
species: A. bicinctus (Von Brandt 1979; Shapiro
1992), A. biaculeatus (Wood 1986), and D. aruanus
and D. marginatus (Shpigel and Fishelson 1986).
The second reason why assessing sexual
pattern in these species is difficult is that the pre-
dominant sexual pattern may vary geographically.
19
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
As examples, A. clarkii, living in tropical areas, has
access to a relatively low density of host sea
anemones and all females derive from functional
males. The species lives obligately with the anem-
one. However, in the temperate waters of Japan host
anemone density is high and migration between
anemones relatively easy. Although functional sex
change does occur under these conditions, its
incidence appears to be relatively low; functional
females lost from a group are most commonly
replaced by females migrating from elsewhere and
far less frequently than by the sex change of
functional males (Moyer 1980; Ochi 1989; Hattori
and Yanagisawa 1991b). Such geographical varia-
tion means that the identification of functional sex
change may require careful assessment of typical
adult sexual function in different places. Dascyllus
aruanus living in an area of continuous coral cover
and forming large groups of males and females is
confirmed to be gonochoristic, or non-functionally
hermaphroditic (Asoh 2003), whereas protogyny
occurs where small groups live in widely spaced
coral colonies and are relatively isolated from one
another (Cole 2002). A similar pattern is proposed
for D. flavicaudus (Godwin 1995; Asoh 2004).
Labridae (wrasses)
In the labrids sexual patterns exhibit many forms of
expression. This is, perhaps, unsurprising for such a
large, diverse and advanced perciform family that is
also the second largest marine fish family and the
third largest of the perciforms with about 68 genera
and 453 species (Nelson 2006) (Table 1). Protog-
yny is confirmed for one or more species from 21
genera. Protogyny was proposed but unconfirmed
for Anampses geographicus and Epibulus insidiator
(Warner and Lejeune 1985; Leem et al. 1998).
Bi-directional sex change is confirmed for
Halichoeres trimaculatus, Labroides dimidiatus and
Pseudolabrus sieboldi under field and laboratory
conditions (Nakashima et al. 2000; Kuwamura
et al. 2002, 2007; Ohta et al. 2003). Gonochorism
is confirmed for one or more species in seven genera
that are Bodianus, Centrolabrus exoletus, Ctenolabrus
rupestris, Notolabrus fucicola, Oxyjulis californica,
Symphodus and Tautoga onitis (Diener 1976; Dipper
and Pullin 1979; Hoffman 1980; Warner and
Lejeune 1985; Bentivegna and Benedetto 1989;
Hostetter and Munroe 1993; Denny and Schiel
2002). In three genera both gonochorism and
protogyny occur and notably many of these are
temperate species (Table 1).
20 Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–43
Challenges to assessing sexual pattern in labrids
first arise from the occasional mismatch of testicular
morphology with reproductive function, body col-
our and form. It was among the labrids and scarids
that Reinboth (1962, 1967a) first distinguished
between monandry and diandry, and elucidated
different testicular morphological types between
primary males developing from juveniles, and sec-
ondary males developing from functional females.
As indicated in the ‘Definitions’ section, however,
subsequent work showed that gonadal morphology,
body colour and reproductive function do not
always match, and therefore much care is needed
in using testicular morphology or body colour as an
indication of function (e.g. Reinboth 1975; Roede
1975; Shapiro and Rasotto 1993). More recently, it
has been demonstrated that the development of
primary males in the diandric Thalassoma bifascia-
tum is labile and controlled by environmental
factors during early gonadal development and
sexual differentiation (Munday et al. 2006b).
Challenges also arise from the different ways in
which testicular tissue develops during or prior to
sexual transition. For example, in the diandric
Cirrhilabrus temminckii testicular morphology is
similar in all males whether derived from functional
females through sex change or from an ovarian-like
juvenile phase (Kobayashi and Suzuki 1990). The
protogynous Cheilinus undulatus may be diandric on
the basis of the occurrence of small males, similar
in size to small females, although the species shows
the typical testicular configuration of secondary
males (Sadovy et al. 2003). In the gonochore
Bodianus eclancheri all males derive from bisexual
juveniles and all testes resemble gonads of imma-
ture females containing oocytes and an ovarian
lumen (Hoffman 1980). In Coris julis testicular
tissue proliferates from preformed areas at the
periphery of the gonad in early gonadal develop-
ment rather than from scattered areas within the
gonads, and during sexual transition this tissue
spreads inwards. As a result, although the former
ovarian lumen is retained within the testis, the
transformed gonad does not exhibit a lamellar
configuration (Reinboth 1962).
Scaridae (Callyodontidae) (parrotfishes)
Protogyny is confirmed in five genera, Calotomus,
Chlorurus, Cryptotomus, Scarus (synonym Callyodon)
and Sparisoma (Table 1). In many scarids, primary
males have the typical testicular configuration of
gonochoristic species while the testes of function-
Ó 2008 The Authors
 Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
ally secondary males have an ovarian lumen, a
lamellar form and peripheral sperm sinuses. This
makes sexual pattern relatively easy to determine,
although care might be needed in a few cases such
as in the monandric Sparisoma aurofrenatum in
which the lumen occurs in males but becomes
occluded (Clavijo 1982). Gonochorism is confirmed
for Bolbometopon muricatum and Leptoscarus vaigi-
ensis; the body size ranges of males and females
show considerable overlap (Robertson et al. 1982;
Hamilton et al. 2007). In B. muricatum all males
have the secondarily derived testicular morphology
and develop from a bisexual phase with the sexual
pattern being gonochoristic (Hamilton et al. 2007).
In L. vaigiensis males only have the typical testic-
ular configuration of gonochoristic species (Robert-
son et al. 1982).
Because body colour, testicular morphology and
reproductive function do not always match in this
family, there has been some confusion over sexual
pattern, as there has been in the related labrids. For
example, in certain species of Chlorurus, Scarus and
Sparisoma some males with testes showing ovarian
structure were smaller than females in the same
population, indicating that they may not derive
from functional females (Choat and Robertson
1975; Robertson and Warner 1978). These males
were considered to be ‘functional analogues’ of
primary males (Robertson et al. 1982). In Sparisoma
chrysopterum (=Scarus chrysopterus), S. cretense and
S. rubripinne (=Scarus rubripinnis), although all
testes showed a secondary structure characteristic
of sex-changed males, the sex ratio was close to
unity, the size ranges of males and females
overlapped, and males matured at the same ages
and sizes as did females (Robertson and Warner
1978; Gonzales and Lozano 1992; De Girolamo
et al. 1999). Collectively, these features strongly
suggest gonochorism.
Pinguipedidae (Mugiloididae) (sandperches)
Protogyny is confirmed for seven species of the
genus Parapercis (Table 1). Testicular tissue may
arise during sexual transition, or be present from
the time of sexual differentiation (Stroud 1982;
Nakazono et al. 1985; Ohta 1987; Kobayashi et al.
1993). Testes exhibit the typical testicular configu-
ration of secondary males. While monandrous
protogyny is suggested to be the rule for this group
(Stroud 1982), some small P. snyderi males may
develop directly from juveniles indicating diandry
(Nakazono et al. 1985).
Ó 2008 The Authors
Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–43
Trichonotidae (sanddivers)
Protogyny is confirmed for Trichonotus filamentosus,
belonging to the only genus in the family (Table 1).
Males are not only larger and older than females,
but also have a different body form and colour
(Kusen et al. 1991). Testicular tissue arises along
the germinal epithelia of ovarian lamellae during
sexual transition. Sexually transitional individuals
overlap in size between females and males, which is
suggestive of monandry.
Gobiidae (gobies)
Hermaphroditism in gobiids was first proposed for
the oxudercine Periophthalmus on the basis of
juvenile gonads with early stages of testicular tissue
and an ovarian-like lumen (reviewed in Atz 1964).
Lassig (1977) reported protogyny for several gobiine
Paragobiodon species. However, functional hermaph-
roditism was not confirmed until the early 1980s
when protogyny was discovered in tropical and
temperate species (Robertson and Justines 1982;
Cole 1983).
The gobies exhibit gonochorism as well as
protogynous hermaphroditism, including bi-direc-
tional sex change (Table 1). Protogyny is confirmed
for one or more species of eight gobiine genera,
Coryphopterus, Elacatinus (Gobiosoma), Eviota, Gobi-
odon, Lythrypnus, Paragobiodon, Priolepis and Trim-
ma, among which gonochorism occurs in
Coryphopterus, Elacatinus (e.g. Gobiosoma illecebro-
sum and G. saucrum) and Trimma. Bi-directional sex
change is confirmed for several species of Gobiodon,
and for Lythrypnus dalli, Paragobiodon echinocephalus
and Trimma okinawae. For L. dalli both simultaneous
(Fishelson 1989; St. Mary 1993) and protogynous
hermaphroditism were proposed (Reavis and Grober
1999; Drilling and Grober 2005). In more recent
studies, bi-directional sex change is confirmed by
demonstrating both female-to-male and male-to-
female sex change in known individuals (Rodgers
et al. 2005, 2007; Lorenzi et al. 2006). Difficulties
in assessing sexual pattern in Lythrypnus species
arise from the high degree of variation of testic-
ular and ovarian tissue allocation within gonads
(St. Mary 1998, 2000). Protogyny was also pro-
posed but not confirmed, in six genera, Bryaninops,
Fusigobius, Hetereleotris, Lophogobius, Luposicya and
Pleurosicya (Fishelson 1989; Cole 1990). For Brya-
ninops yongei bi-directional sex change may occur as
suggested by a monogamous mating system and
a bisexual gonadal phase (Munday et al. 2002).
The sexual pattern of Priolepis hipoliti (=Quisquilius
21
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
hipolites) may also include both simultaneous and
protogynous hermaphroditism (Cole 1990).
Species differ markedly regarding testicular and
ovarian tissue configuration before and during sex
change (Cole 1990). For example, in Coryphopterus
species small crypts of spermatocytes appear within
the ovarian stroma and subsequently replace all
ovarian tissue during and after sex change. In
T. unisquamis presumptive testicular tissue is present
in females in the medio-lateral wall of the ovary
long before sex change. In P. hipoliti, testicular and
ovarian tissues are topographically separated and
both are likely to be active simultaneously for some
period of time before becoming exclusively male in
function (Cole 1990). In Priolepis cinctus (=P. cincta,
P. naraharae) mature ovaries contained testicular
tissue and undeveloped ‘precursive accessory gona-
dal structures’ (pAGSs) while mature testes con-
tained primary-growth stage oocytes and fully
developed pAGSs; bi-directional sex change was
proposed for the species (Sunobe and Nakazono
1999).
Confirming sex change has proved problematic in
this family because of the variability in testicular
and ovarian tissue configurations. Also, the testes
of protogynous species do not always reflect
the preceding ovarian morphology (Cole 1983,
1990; Cole and Robertson 1988). For example, in
C. personatus, testicular tissue arises throughout the
body of the gonad and the peripheral ovarian lumen
disappears soon after sex change. In C. nicholsi
testicular tissue arises uniformly around the periph-
ery of the old ovarian lumen, and then proliferates
outwards finally compressing it completely (Cole
and Robertson 1988). In both cases the resulting
testes are solid and traces of the former female phase
quickly disappear following sex change. Sperm is
not carried by peripheral sperm sinuses but typically
exits the body via a newly formed anastomosing
network of tubules lined with spermatogenic crypts
(Cole and Robertson 1988).
Although hermaphroditism is difficult to identify
inasmuch as there is often extensive overlap in male
and female sizes, pAGSs are one morphological
feature associated with the gonads that appear
useful for detecting hermaphroditism in certain
protogynous gobiids. During sexual transition these
structures develop in males, although their function
is unknown. They appear as small distinctive tissue
masses associated with the ventral wall and subse-
quently develop into secretory accessory gonadal
structures lined by a single layer of secretory cells
22 Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–43
associated with the secondary testis (Cole 1988,
1990; Cole and Robertson 1988). As pAGSs, they
appear in conjunction with the ovaries of functional
females of protogynous species and could prove
invaluable for the diagnosis of hermaphroditism in
this family (Cole 1988, 1990; Cole and Shapiro
1990). In general differences in gonadal morphol-
ogy tend to follow phylogenetic lines (Cole 1990;
St. Mary 1998).
Families in which hermaphroditism has been
reported, but not confirmed
In addition to the preceding 27 families in which
functional hermaphroditism has been confirmed,
hermaphroditism was proposed or inferred, but not
confirmed, in an additional 21 families distributed
across six orders (Table 3 and Fig. 1). Tables 2 and
3 provide weak diagnostic criteria used for each of
these families and a complete listing of all genera for
which hermaphroditism has been proposed. Among
these, gonochorism or non-functional hermaphro-
ditism is confirmed in at least six families. These
families are of particular interest for the insights
they provide into many of the difficulties in
confirming sexual pattern.
Discussion
By applying a rigorous set of criteria to data
gathered from over 400 primary studies we sum-
marize the currently known incidence of functional
hermaphroditism in teleosts, identify specific prob-
lems in the assessment of hermaphroditism, hypoth-
esize on its possible origin in this group, briefly
discuss general ecological correlates and phyloge-
netic patterns, and identify promising directions for
research and analysis. The major focus of this
comprehensive review is to provide a foundation for
further analyses on hermaphroditism in fishes from
developmental, functional and phylogenetic per-
spectives, and encourage better diagnoses for con-
servation, management and aquaculture-related
activities. In particular, we highlight the need for
careful diagnosis of sexual pattern and emphasize
the importance of clearly distinguishing gonadal
form from reproductive function. Form is relevant
for studies of development and phylogeny and
function relates to questions about adaptation and
environmental correlates.
The existence of functional hermaphroditism is
confirmed for teleosts belonging to 27 families in 94
Ó 2008 The Authors
 Table 3 Additional 21 families of teleost fishes in which hermaphroditism is proposed but not confirmed. For details of terminology see ‘Definitions’ in the text. Family classifications
follow those of Nelson (2006). For each family, proposed genera (*) are listed, and gonochorism is also given if occurs in these genera. Arrhenoidy, a female exhibiting male
sexual characteristics, and gynoidy, a male exhibiting female sexual characteristics, inferred sex change respectively. Numbers in parentheses refer to Table 1, with testicular and
ovarian tissues in the gonads topographically separated without connective tissue (1), by connective tissue (2) or not topographically separated at all (3).

Ó 2008 The Authors

Sexual mode

Order–Family Genus Gonochorism Simultaneous Protogyny Protandry Bi-direction Reference

Clupeiformes
Clupeidae Tenualosa *(3) Blaber et al. (1996, 1999, 2005)

Cypriniformes
Cyprinidae Gymnocypris Arrhenoidy Bullough (1940), Atz (1964)
Phoxinus + Arrhenoidy Gonochorism confirmed: Rasotto et al. (1987)
Schizopygopsis Arrhenoidy
Cobitidae Cobitis + Arrhenoidy *, Gynoidy Lodi (1967, 1980a)
Gonochorism confirmed: Lodi (1980a), Rasotto
(1992)
Aulopiformes
Notosudidae Scopelosaurus * Bertelsen et al. (1976)
Evermannellidae Coccorella * Merrett et al. (1973)
Paralepididae Lestidiops * Mead (1960)

Cyprinodontiformes

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Poeciliidae Xiphophorus *, Arrhenoidy Gordon (1956), Atz (1964), Yamamoto (1969),
Lodi (1979, 1980b), Kallman (1984)
Perciformes
Moronidae Morone * Moser et al. (1983), Berlinsky et al. (1995),
Holland et al. (2000)
Grammatidae Gramma +(1) * See citation in Asoh and Shapiro (1997)
Gonochorism confirmed: Asoh and Shapiro
(1997)
Malacanthidae Branchiostegus + *(3) Dooley (1978), Ross and Merriner (1983),
Caulolatilus *(3) Baird (1988), Erickson and Grossman (1986),
Malacanthus * Ceballos-Vázquez et al. (1996), Ceballos-
Vázquez and Elorduy-Garay (1998), Harris
et al. (2004)
Gonochorism confirmed: Watanabe and
Suzuki (1996)

23
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
 Table 3 Continued.

24
Sexual mode

Order–Family Genus Gonochorism Simultaneous Protogyny Protandry Bi-direction Reference

Polynemidae Filimanus * Longhurst (1965), Kagwade (1968, 1976),

Galeoides *(2) Szyper et al. (1991), Motomura et al. (2002)
Leptomelanosoma *(2)
Polydactylus *
Chaetodontidae Chaetodon + *(3) Irons (1989), Tricas and Hiramoto (1989),
Suzuki et al. (1996)
Gonochorism confirmed: Fowler (1991)
Terapontidae Terapon *(3) Liu (1979), Moiseeva et al. (2001)
Bidyanus *(3)
Cepolidae Cepola + *(2) Vives et al. (1959)
Gonochorism confirmed: Atkinson et al.
(1977), Stergiou et al. (1996)
Cichlidae Cichlasoma * Polder (1971), Peters (1975), Ohm (1978,
Crenicara * 1980), Zupanc (1985), Naish and Ribbink
Pseudotropheus *(3) (1990), Carruth (2000)
Odacidae Odax * Ayling and Paxton (1983), Gomon and Paxton
(1985)
Eleginopidae Eleginops *(2) Clavo et al. (1992), Brickle et al. (2005)
Percophidae Matsubaraea * Noichi et al. (1991)
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu

Blenniidae Salaria * Heymer (1980, 1985)

Tetraodontiformes
Balistidae Sufflamen *(2) Takamoto et al. (2003)
Ostraciidae Ostracion * Richard (1989)

Ó 2008 The Authors

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 Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
genera, while for an additional 21 families in 31
genera, including several widely cited to contain
functional hermaphroditic representatives, the evi-
dence presented is not sufficiently conclusive to rule
out alternative explanations. Among these, six
families and many genera are newly confirmed
over the last decade. Problems with possible misdi-
agnoses of sexual pattern in 21 families largely stem
from confusion over gonadal form in relation to its
reproductive function. Specific difficulties arose
especially from three areas: (i) incomplete or lack
of histological analysis of gonads especially with
respect to the juvenile phase and the failure to
eliminate possible juvenile bisexuality in gonocho-
ristic or non-functional hermaphroditic species;
(ii) the common assumption that any testis con-
taining a lumen must be functionally secondary,
suggesting that the sex has changed from functional
female to male, and (iii) an unclear or inappropriate
definition of the transitional phase between func-
tional male and functional female. As an example
transitional individuals in protogynous species were
often assigned with no indication of the degenera-
tion of vitellogenic stage oocytes, or any other
sign of prior female function. The presence of
cortical-alveolar stage oocytes cannot be used as
indication of prior or future female maturation as
they can arise in developing males and then regress
in gonochoristic species (Asoh et al. 2001; Asoh and
Kasuya 2002; Asoh 2004). Less common problems
stem from possible misdiagnoses of the functional
sex when gender was assigned solely on the basis of
external morphology, colouration or behaviour and
sometimes, albeit rarely, on the occurrence of
abnormal hermaphroditism, arrhenoidy or gynoidy.
Families in which the identification of a sex change
has not been confirmed merit a reexamination of
their sexual pattern.
Consistent with earlier reviews we confirm that
the functional hermaphroditic trait in teleosts is
widespread and extremely patchy in its phylogenetic
distribution and is notably more common in some
environments than in others. However, we also
caution that many families and genera remain
untested. Functional hermaphroditism occurs in at
least 6% of all teleost families. Amongst the perci-
forms it is exhibited in more than 10% of families,
encompassing both large and small species, employ-
ing both demersal and pelagic spawning and
occurring in a range of habitats. Based on its
phylogenetic distribution, many workers have pro-
posed that the variety of hermaphroditism in
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teleosts must be a derived trait that originated
independently in different groups of fishes from a
gonochoristic condition (Atz 1964; Liem 1968;
Smith 1975; Ota et al. 2000). Smith (1975) for
example, considered that fundamental differences in
the anatomy of the gonad in various fish groups
provide decisive evidence that hermaphroditism
arose repeatedly in unrelated groups as a result of
convergent evolution. We now explore some of
these ideas based on the outcomes of our review.
Regarding the apparently unique capacity of
teleosts to exhibit functional hermaphroditism
among vertebrates, both morphological and cellular
considerations of gonadal development are relevant
to its presence and, possibly, also to its absence. On
the one hand, as proposed by D’Ancona (1945,
1956) and supported by others (Atz 1964; Hoar
1969; Nieuwkoop and Sutasurya 1979; Reinboth
1983; Roblin and Bruslé 1983; Nieuwkoop 1991;
Nakamura et al. 1998; Pieau et al. 1999), among
the lower vertebrates, teleosts and cyclostomes differ
from elasmobranch amphibians and reptiles in the
nature of the origin of the gonadal primordium. In
the latter three groups the gonad has a cortex and
medulla with a dual origin. When a genetic sex
determination mechanism occurs in amphibians
and reptiles and teleosts sexual differentiation is
sometimes found to be sensitive to temperature or
pH during a critical period of embryonic develop-
ment. This indicates plasticity during sexual differ-
entiation even when there is no adult sex change
(Pieau et al. 1999; Wallace et al. 1999; Devlin and
Nagahama 2002; Oldfield 2005). In the teleosts and
cyclostomes the gonadal primordium is believed to
have a single origin arising from the peritoneal
epithelium and corresponding to the cortex of other
vertebrates. Although the cyclostomes have no
known functional hermaphrodites they regularly
exhibit non-functional hermaphroditism in the form
of gonochorism with a gonadal bisexual phase in
juveniles (Hardisty 1979; Fukayama and Takahashi
1982, 1983; Gorbman 1983, 1990).
Rather than hermaphroditism being a derived
condition and gonochorism a primitive state it is
possible that the distinctive gonadal origin may
have afforded the teleosts and cyclostomes a proto-
hermaphroditic condition with the potential to
exhibit various forms of hermaphroditism (Nakam-
ura et al. 1998; Strüssmann and Nakamura 2002).
Physical, environmental and developmental con-
straints as discussed by Warner (1978), Reinboth
(1982, 1983, 1988), Nakazono and Kuwamura
25
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
(1987), Francis (1992), Ota et al. (2000), Devlin and
Nagahama (2002), Godwin et al. (2003), Mank et al.
(2006), Munday et al. (2006a) and Molloy et al.
(2007) may, on the other hand, have precluded the
exploitation of this potential in certain fish groups.
This does not mean that teleosts have a hermaphro-
ditic ancestry, only and that the potential for its
functional expression is associated with the proto-
hermaphroditic condition. The plasticity during
sexual differentiation exhibited by amphibians and
reptiles in which sex is genetically determined
further supports the hypothesis of a basal proto-
hermaphroditic condition.
For functional hermaphroditism to occur either
germ cell lines need to be sexually bipotential and
retain this capacity for an extended period, or
tissues of both sexes co-exist and function in a
gonad. Alternatively some combination of these two
conditions may occur. One recent study showed
that a single gonium can produce germ cells of both
sexes in the protogynous Synbranchus marmoratus
(Lo Nostro et al. 2003). The ovarian germinal
epithelium, which forms follicles containing an
oocyte and encompassing follicle cells during female
function, subsequently produces numerous invag-
inations, or acini, in the ovarian stroma during
sexual transition (Grier 2002). Within the acini, the
gonia, which formerly produced oocytes, become
spermatogonia, enter meiosis and produce sperm,
suggesting sexual bipotentiality of gonia. Further
support for sexual bipotentiality of the gonia comes
from the gobiid Gobiodon erythrospilus, a species with
bi-directional sex change and in which sex-changed
individuals exhibit little or no remnant tissue of
the alternative sex (P.L. Munday, personal
communication).
On the other hand, although descriptive work on
the earliest stages of gonadal development is
severely limited by difficulties in distinguishing the
sex of early germ cells, even under an electron
microscope (Harrington 1974; Reinboth 1982),
there are at least some gross descriptive data
showing that both testicular and ovarian tissues
can be maintained simultaneously in the gonads of
both gonochores and hermaphrodites from early
gonadal development. For example, in a taxonom-
ically wide range of protogynous and protandrous
species tissues of both sexes, or the presumptive
tissue of the second sex, are present in various
configurations. The taxa showing this include
species belonging to the synbranchid, platycephalid,
serranid, sparid and centracanthid families, and to
26 Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–43
Centropyge interruptus, Amphiprion spp. and Coris
julis. In these examples tissues of both sexes can be
topographically separated with or without a
connective tissue membrane. In some species, such
as Cephalopholis boenak and Epinephelus akaara in
which distinct areas of testicular tissue are generally
not reported to be present in functional females and
males, small spermatogenic cysts or clusters are
detected from early gonadal development (Tanaka
et al. 1990; Liu and Sadovy 2004b). Hence, in such
cases intermixed tissues of both sexes can be
maintained for extended periods of time. In some
protogynous species, such as Centropyge bicolor and
Thalassoma bifasciatum, in which no testicular tissue
was noted in the ovarian phase prior to sex change,
it is not clear whether testicular tissue develops
de novo or arises from an undiscovered line of male
germ cells (Reinboth 1982).
What factors determined which taxa ran with
this option, how does non-functional hermaphro-
ditism fit into the picture and how did one form of
functional hermaphroditism evolve into another,
once the potential for functional hermaphroditism
arose? To answer such questions we need informa-
tion on phylogenetic interrelationships, environ-
mental and biological correlates, and on sex
determination mechanisms and capabilities of spe-
cies exhibiting different sexual patterns. A full
analysis of this type is outside the scope of this
review but a brief examination is instructive,
focusing on several perciform examples in which
functional hermaphroditism is most diversely and
widely expressed and in which phylogenetic rela-
tionships have been at least partially resolved. This
examination will also make it possible to
develop hypotheses about ultimate and proximate
causation.
From an ecological perspective, functionally her-
maphroditic species identified by this and earlier
studies hint at a number of provocative environ-
mental correlates in both the presence and absence
of this sexual pattern (e.g. Ghiselin 1969; Warner
1975a, 1984; Charnov 1982; Policansky 1982).
Taken together, the studies suggest that sequential
hermaphroditism, especially protogyny, is particu-
larly common in shallow tropical marine reef
habitats and among the perciforms. Simultaneous
hermaphroditism typifies many species examined
from the deep-sea environment, although a few are
found in shallow waters. Hermaphroditism is nota-
bly absent or rare in certain groups such as
epipelagic fishes and soft-bottom ground fishes of
Ó 2008 The Authors
 Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
the continental shelf and estuaries and, if it does
occur in these habitats, it tends to be protandry.
More studies on mating and social systems of
protandric species are needed to understand its
possible adaptative significance in these environ-
ments. Within the most speciose of the freshwater
families, Cyprinidae, Characidae and Cichlidae, not
one case of functional hermaphroditism is con-
firmed. This is noteworthy inasmuch as the cypri-
nids and cichlids are popular aquarium and
experimental animals and thus functional her-
maphroditism is unlikely to have been missed in
either group. The freshwater cichlids exhibit exam-
ples of a juvenile bisexual phase and social deter-
mination of juvenile sexual expression (reviewed in
Oldfield 2005). Apart from the synbranchid eels,
functional hermaphrodites are absent from all
primary freshwater groups. Future work on the
adaptive significance of diandry in synbranchid eels
would be interesting.
How do we account for these apparent patterns
of distribution and expression of functional her-
maphroditism in teleosts? Is its absence from some
environments instructive and what can we say
about its adaptive significance? At the ultimate level
and where enough is known of the mating and
social systems, the expression of functional her-
maphroditism appears to occur when it can
increase an individual’s reproductive success (Ghis-
elin 1969; Munday et al. 2006a). Simultaneous
hermaphroditism is proposed to be adaptive under
conditions of low population density where it
enhances the probability that individuals will
encounter a mate, for example in many deep-sea
fishes (Ghiselin 1969). It could also be a response to
male–female conflict (Charnov 1979). Sequential
hermaphroditism is proposed to be adaptive by the
size-advantage model (Ghiselin 1969; Warner
1975a, 1988; Charnov 1982) when there is
differential production of offspring by sex with body
size. While Ghiselin’s theory has proved to be
relatively robust it cannot address all cases of
sequential hermaphroditism. More studies are
needed to quantitatively test the theory and con-
duct comparative studies between related species
(Warner 1984; Warner and Lejeune 1985;
Charnov 1986; Munday et al. 2006a; Molloy et al.
2007).
At the proximate level, the control of functional
hermaphroditism appears to have a strong behavio-
ural component with little known influence from
genetic or abiotic factors. Social and mating
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systems, therefore, are likely to strongly influence
the opportunities for individuals to increase their
reproductive success through expressing some form
of it. It is of interest to explore such traits in species
that exhibit functional hermaphroditism as well as
in those where the sexual pattern is notably absent,
while keeping in mind that the non-appearance
of a characteristic where it might reasonably be
expected to be adaptive may not necessarily reveal
much due to other constraints or life history
tradeoffs (Warner 1975a, 1984; Reinboth 1982;
Shapiro 1984; Hoffman et al. 1985; Warner and
Lejeune 1985; Charnov 1986; Munday et al.
2006b).
Given the clear behavioural control of sex change
identified in many sequential hermaphrodites it is
likely that its incidence is associated with species
that have a high potential for repeated and complex
social interactions that relate to opportunities for
mating and where the social or mating systems also
confer differential advantages by sex under certain
conditions. The highly derived coral reef fishes, for
example, which exhibit the greatest range and
highest incidence of functional hermaphroditism,
include many species that are sedentary, long-lived
and display a complex range of social structures and
behaviours. Such characteristics could be key fac-
tors in creating opportunities for size specific or
other socially mediated advantages for changing sex
(reviewed in Munday et al. 2006a). In protogynous
species, for example, there are many instances of
social and mating systems associated with protog-
yny related to the ability of larger males to control
resources that are themselves stable and predictable
on coral reefs (e.g. Robertson and Hoffman 1977;
Moyer and Yogo 1982). In male–female pairs of the
protandrous anemonefish isolated on sparsely dis-
tributed anemones, the larger fish is a female which
would appear to take advantage of the general
relationship in female fish between large size and
high fecundity and the confinement of the habitat to
a single breeding pair. Among coastal and ground
fish species that exhibit protandry, such as certain
platycephalids and sparids, Centropomus undecimalis
and Lates calcarifer, relatively little is known of their
social and mating systems. Haphazard pairing is
predicted for species living in large schools but this
remains to be tested (Warner 1984). In such cases
the higher fecundity associated with larger female
size might be important but we need to understand
the mating system to be able to test hypotheses and
explore possible advantages.
27
Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
Insights might emerge from examining unex-
pected expressions of functional hermaphroditism.
For example, among the serranids, it is unclear why
simultaneous hermaphroditism should have arisen
among the shallow water serranines such as
Hypoplectrus spp., yet many monogamous species
such as some butterflyfishes do not appear to be
hermaphroditic (Fischer and Petersen 1987). In
certain epinepheline serranids, such as Epinephelus
guttatus, which aggregate to spawn for brief periods
once a year but otherwise apparently lead a
generally solitary existence (Shapiro et al. 1993),
it is unclear why protogyny is expressed. One
possible explanation is that the temporary territories
guarded by males in their brief spawning aggrega-
tions enhance reproductive success; if so, why are
the other aggregating congenors, such as E. striatus,
gonochoristic (Sadovy and Colin 1995)? Conversely,
given the apparent plasticity of sexual pattern in
teleosts, when the mating system would appear to
confer a reproductive advantage on large males, as
in the coral reef grammatid Gramma loreto
(Perciformes), and the tetraodontiforms, Sufflamen
chrysopterus (Balistidae) and Ostracion spp. (Ostra-
ciontidae), why is protogyny apparently not
expressed (Richard 1989; Asoh and Shapiro 1997;
Takamoto et al. 2003). Interestingly, the juvenile
gonads in both G. loreto and S. chrysopterus exhibit
a bisexual phase (Asoh and Shapiro 1997; Taka-
moto et al. 2003). Clearly we need to understand
much more of the biology and sexual development
of such cases.
Functional hermaphroditism is typically absent in
epipelagic and in estuarine and soft-bottom ground
fishes. It is also absent in freshwater fishes and is
generally uncommon in temperate species even in
families that have hermaphroditic relatives in the
tropics. The absence of hermaphroditism from most
freshwater habitats may be attributable to both
developmental factors and the balance between
costs and benefits of a life history. The relatively
large eggs or young produced by many freshwater
species tend to accentuate the physical differences in
male and female anatomy possibly forming a barrier
or physical constraint to hermaphroditism (Warner
1978). From a theoretical standpoint, the fewer,
larger eggs and higher incidence of egg care in
parents (Baylis 1981) may reduce the potential for
large differentials between the sexes in reproductive
success by size as proposed by the size-advantage
model. In the case of epipelagic species, many are
short-lived, may have limited social interactions and
28 Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–43
co-exist in schools of similar-sized individuals with
high mate availability and little opportunity for
control of resources or for gaining relative advan-
tage as a result of size. Among temperate species
with shorter spawning seasons, metabolic factors
associated with the relationship between tempera-
ture, egg production or rates of sex change may
mean that male–female differentials with size are
small or that sex change is energetically too
expensive. Such speculations can be used as the
basis of hypotheses for comparative tests of the
proximate basis of the expression or otherwise of
functional hermaphroditism in different environ-
ments, especially within taxonomic groups occupy-
ing a range of habitats and exhibiting a diversity of
sexual patterns.
The variation in functional sexual patterns with-
in families, genera and even species is highlighted in
this review. Such variation is an indication of the
plasticity of sexual development and expression in
fishes and provides excellent opportunities for com-
parative studies. Examples are provided in the
results of 18 genera that exhibit both functional
hermaphroditism and gonochorism (Table 1). Par-
ticularly striking are the differences among related
families and species in the expression of sexual
pattern between tropical and temperate marine
environments offering considerable promise for
comparative analyses of ecological and geographical
traits. In this respect, families of particular interest
are the sparids, pomacentrids, labrids and gobiids.
For example, the Labridae exhibit a diverse range of
sexual patterns. This group has recently been
resolved as monophyletic and includes the odacines
and scarines, or the Odacidae and Scaridae of this
review (Westneat and Alfaro 2005). Gonadal mor-
phology in wrasses and parrotfishes show many
similarities and it is of interest to examine odacines
for sexual pattern; we predict that these temperate
species are likely to be gonochoristic, because
functional hermaphroditism is uncommon under
temperate conditions, but will show hermaphroditic
affinities. Deep and shallow water representatives
and marine and freshwater species of a family also
provide opportunities for testing hypotheses of
possible adaptive significance of variations in sexual
pattern; examples include the muraenids, aulopi-
form families and the rivulids.
Finally, what can we say about the distribution
and expression of functional hermaphroditism in
those taxonomic groups for which the phylogenetic
relationships are at least partially resolved? Over
Ó 2008 The Authors
 Functional hermaphroditism in teleosts Yvonne Sadovy de Mitcheson and Min Liu
the past 15 years, understanding has grown sub-
stantially of acanthomorph relationships through
comparative anatomy and molecular systematic
studies (Dettai and Lecointre 2005). While there is
much to resolve at higher levels, patterns are
emerging that are consistent with a proto-her-
maphroditic hypothesis. In the Platycephalidae
Fujii (1974) suggested a possible trend from simul-
taneous hermaphroditism to gonochorism via prot-
andry. In the Serranidae (as in Nelson 2006) Smith
(1965, 1975) noted differences in gonadal mor-
phology among the serranines, anthiines and
epinephelines, while Sadovy and Domeier (2005)
suggested that the serranine Paralabrax species,
basal to the Serranidae, are non-functional her-
maphrodites reflecting a possible proto-hermaphro-
ditic ancestry. Recent molecular studies strongly
suggest that the Serranidae (sensu Nelson 2006) is
paraphyletic and should now be resolved as the
Serranidae, composed of the Anthiinae, Serraninae
and Trachininae, less Acanthistius and Niphon and
the higher Epinephelidae (Smith and Craig 2007)
and a shift between simultaneous and protogynous
hermaphroditism has probably been confined to the
restricted Serranidae. In the sparoid fishes likewise,
simultaneous hermaphroditism was proposed as the
primitive condition, with sequential hermaphrodit-
ism derived, and secondary gonochorism the most
advanced state (D’Ancona 1949; Buxton and
Garratt 1990). In the gobiid genus Coryphopterus,
protogyny is widespread despite apparent broad
differences among species in ecology and social
systems. This led to the suggestion that hermaph-
roditism in this family is likely to be an ancestral
state, rather than having been recently derived
(Cole and Shapiro 1990; St. Mary 1998). It is
unlikely that any single evolutionary model will
satisfactorily explain protogyny equally well in all
species of Coryphopterus.
We conclude by proposing that the unique form
of development of the teleost and cyclostome
gonadal primordium provided the substrate for the
origin and potential expression of hermaphroditism
in these groups through a proto-hermaphroditic
condition. Which taxa express this option today is,
to some extent, determined by a range of environ-
mental conditions and by life history traits that
create opportunities for enhancing reproductive
success by being hermaphroditic. Other factors that
might also be important in the expression of
functional hermaphroditism but which are little
understood are possible mediators of sex change
Ó 2008 The Authors
Journal compilation Ó 2008 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 9, 1–43
such as genetic sex determination, the developmen-
tal polarity of the brain-pituitary-gonadal axis and
endocrine systems (Francis 1992; Ota et al. 2000;
Devlin and Nagahama 2002; Godwin et al. 2003).
Functional hermaphroditism exhibits its greatest
diversification within the more derived perciforms
and mainly in marine and tropical species, with
simultaneous hermaphroditism typically a less
derived condition compared to expressions of
sequential hermaphroditism. The rapidly improving
resolution in teleost phylogeny, the more rigorous
approach to determination of sexual patterns pro-
posed herein, the testing of hypotheses identified
and a growing understanding of environmental and
biological characteristics in a wider range of species
will greatly advance our understanding of the
patterns that appear to be emerging today.
Acknowledgements
We wish to acknowledge the contribution of the
following people to this manuscript. For translation
of material, we thank S. Steiner, K. Asoh and T.
Toshikawa. For access to translated material and
other literature, we thank J.W. Atz, H. Grier, P.L.
Munday, D.Y. Shapiro and K.J. Sulak. For critical
comments and clarifications on various drafts of the
manuscript, we are particularly grateful to J.W. Atz,
K.S. Cole, M.T. Craig, D.A. Hensley, G.R. Mitcheson,
P.L. Munday, C.W. Petersen, M.B. Rasotto, D.Y.
Shapiro, K.J. Sulak, R.R. Warner and anonymous
reviewers. We especially acknowledge J.W. Atz for
helping in the development of this review, and for
his encouragement, inspiration and support to Y.S.
on a much earlier draft of this work. The Research
Grants Council partially funded this work.
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