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

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

     

True hermaphroditism: a new case with complex mosaicism

True hermaphroditism is a very rare disorder of human sexual differentiation. In the medical literature, more than 450 cases are described, and about 250 true hermaphrodites have been subjected to chromosome studies. A 21-year-old "man" was examined because of genital and phenotypic abnormalities: clinical, surgical and laboratory investigations showed a true hermaphroditism, with a quadruple mosaicism 45,X/46,XX/46,XY/47,XXY. We believe that this is the first case in which this peculiar type of multiple mosaicism has been documented.     

The Evolution of Hermaphroditism from Dioecy in Crustaceans: Selfing Hermaphroditism Described in a Fourth Spinicaudatan Genus

The evolution of reproductive systems has intrigued evolutionary biologists for well over a century. Recent empirical and theoretical work has elucidated the evolution of dioecy (separate males and females) from hermaphroditism in many plant species. The reverse transition, evolving hermaphroditism from dioecy, has occurred many times in animals, and yet is poorly studied relative to its reverse analog in plants. Crustaceans in the sub-order Spinicaudata have evolved hermaphroditism from dioecy three separate times, in some cases forming all-hermaphroditic species and in others forming androdioecious (males + hermaphrodites) species. Herein we report evidence of hermaphroditism in a fourth spinicaudatan genus: the newly described Calalimnadia. We present sex ratio and anatomical evidence that Calalimnadia mahei comprises selfing hermaphrodites, with no males being found in over 10,000 offspring reared. We combine these reproductive results with those of other Spinicaudata to estimate the evolution of hermaphroditism in this crustacean sub-order. We use these genetic data combined with anatomical evidence to suggest that C. mahei represents a fourth, independent derivation of hermaphroditism from dioecy in these reproductively labile crustaceans.     

GENETIC EVIDENCE FOR MULTIPLE ORIGINS OF DIOECY IN THE HAWAIIAN SHRUB WIKSTROEMIA (THYMELAEACEAE)

Dioecy is unusually common in the Hawaiian Islands, yet little is known about the evolutionary biology of this breeding system. A native shrub, Wikstroemia, has an unusually diverse array of breeding systems: two forms of dioecy, cryptic and morphological dioecy, as well as hermaphroditism (perfect flowers). The existence of two forms of dioecy is significant for three reasons: 1) the presence of cryptic unisexuals that are functionally unisexual, but retain the appearance of hermaphroditism in both sexes, is strong evidence for the ancestral status of hermaphroditism; 2) the production of nonfunctional pollen, by female cryptic unisexuals, is a new instance of a phenomenon which has previously been reported for a few other species; 3) the two forms of dioecy are morphological markers which are useful in hybridization studies for tracing the genetic basis of their inheritance. Crosses were made between cryptically unisexual individuals (C), between morphologically unisexual individuals (M), and between the two types of unisexuality. The offspring of crosses between individuals with the same sex type usually resulted in offspring with that sex type, but most of the progeny of between-sex type crosses were, unexpectedly, perfect-flowered hermaphrodites. These results show that genetic control of sex determination is not homologous in all populations, suggesting that dioecy has evolved at least twice in Hawaiian Wikstroemia. The genetic data further suggest that males are the heterozygous sex.     

Hermaphroditism and gonochorism. a new hypothesis on the evolution of sexuality in crustacea

Most crustaceans are gonochoristic but hermaphroditism occurs in primitive classes as well as in different orders of higher Crustacea. Though studies have been carried out in plants and animals on the advantages of these two types of sexuality, it is not known how hermaphroditism can change into gonochorism and vice versa. The new hypothesis we report here is based on recent results on biased sex ratio in Crustacea. We suggest that ancestral sexuality was a simultaneous hermaphroditism as it exists still today in primitive groups. Gonochorism may have appeared following integration in the host genome of a parasitic xenogenous DNA inhibiting expression of ‘male genes’. Female sex would be anterior to male sex, and male heterogamety can be seen as a by-product of an intragenomic conflict in a species with an ancestral female heterogamety. Sequential hermaphroditism in higher Crustacea would be a secondary hermaphroditism resulting from other genetic conflicts between host genes and repressing heterochromosomic genes (parasitic DNA from xenogenous origin?)     

Hermaphroditism in the dash‐and‐dot goatfish Parupeneus barberinus

Presence of bisexual individuals and a sex‐specific bimodal size distribution are suggestive of protogyny in the dash‐and‐dot goatfish Parupeneus barberinus, but the most parsimonious interpretation of histological analysis is juvenile hermaphroditism. This is the first report of hermaphroditism in the Mullidae.     

Female gonad of moles, genus Talpa (Insectivora, mammalia): ovary or ovotestis?

The female gonads of moles (genus Talpa) are composed of a cortex, functioning as an ovary, and a medulla, which is structurally similar to that of the testis. In the female reproductive apparatus there are masculine glandular annexes, such as a bilobate prostate, two Cowper glands, and a penis-like clitoris. All these features have recently led to the hypothesis of the presence of hermaphroditism due to sex-reversal in Talpa. The purpose of this study is to understand the functional significance of the structural organization of the female gonads in order to verify this hypothesis. Histological, histochemical and ultrastructural analyses have been carried out on several gonads of both sexes of two species: T. europaea and T. romana, including three fetuses. In both species, the cortical region of the female gonad shows a regular oogenetic activity. While the medulla is composed of interstitial cells that are partly organized in cord-like structures, no spermatogenetic activity has been ever observed inside of them. A histochemical analysis shows that in both sexes the interstitial cells secrete steroids, presumably estrogens as well as androgens. The presence of androgens in the female gonads would therefore explain the persistence of male glandular annexes in the female reproductive apparatus and both the sexual and behavioral monomorphism typical of the genus Talpa. Nonetheless, the female gonad of moles is a real ovary and a well-defined gonochorism exists. Therefore, there is no reason to assert the presence of hermaphroditism due to sex reversal.     

A COMPARATIVE ANALYSIS OF SEX CHANGE IN LABRIDAE SUPPORTS THE SIZE ADVANTAGE HYPOTHESIS

The size advantage hypothesis (SAH) predicts that the rate of increase in male and female fitness with size (the size advantage) drives the evolution of sequential hermaphroditism or sex change. Despite qualitative agreement between empirical patterns and SAH, only one comparative study tested SAH quantitatively. Here, we perform the first comparative analysis of sex change in Labridae, a group of hermaphroditic and dioecious (non–sex changer) fish with several model sex‐changing species. We also estimate, for the first time, rates of evolutionary transitions between sex change and dioecy. Our analyses support SAH and indicate that the evolution of hermaphroditism is correlated to the size advantage. Furthermore, we find that transitions from sex change to dioecy are less likely under stronger size advantage. We cannot determine, however, how the size advantage affects transitions from dioecy to sex change. Finally, contrary to what is generally expected, we find that transitions from dioecy to sex change are more likely than transitions from sex change to dioecy. The similarity of sexual differentiation in hermaphroditic and dioecious labrids might underlie this pattern. We suggest that elucidating the developmental basis of sex change is critical to predict and explain patterns of the evolutionary history of sequential hermaphroditism.     

Direct reciprocity stabilizes simultaneous hermaphroditism at high mating rates: A model of sex allocation with egg trading

Simultaneous hermaphroditism is predicted to be unstable at high mating rates given an associated increase in sperm competition. The existence of reciprocal egg trading, which requires both hermaphroditism and high mating rates to evolve, is consequently hard to explain. We show using mathematical models that the presence of a trading economy creates an additional fitness benefit to egg production, which selects for traders to bias their sex allocation toward the female function. This female‐biased sex allocation prevents pure females from invading a trading population, thereby allowing simultaneous hermaphroditism to persist stably at much higher levels of sperm competition than would otherwise be expected. More generally, our model highlights that simultaneous hermaphroditism can persist stably when mating opportunities are abundant, as long as sperm competition remains low. It also predicts that reciprocity will select for heavier investment in the traded resource.     

Sex ratios and hermaphroditism in nemipterid fish from northern Australia

Of 13 nemipterid species from coastal waters around northern Australia, nine show size-related differences in sex ratio with males predominating at larger sizes. Histological examination of gonads shows that in Scolopsis monogramma S. taeniopterus and S. bilineatus this size-related skew in sex ratio results from protogynous hermaphroditism and not from sexually differentiated growth rates as has been reported for other nemipterid species. There is also evidence that, in two other species, Nemipterus peronii and Pentapodus porosus , hermaphroditism may occur. Although the mechanism by which the gonads are transformed in S monogramma and S. taeniopterus differ markedly, there is evidence to suggest that in both species sex change is a post spawning event, successful initiation of which may require females to have achieved an advanced stage of vitellogenisis.     

Breeding systems in the clam shrimp family Limnadiidae (Branchiopoda, Spinicaudata)

Abstract. Crustaceans in the class Branchiopoda exhibit a wide range of breeding systems, including dioecy (gonochorism), androdioecy, parthenogenesis, cyclic parthenogenesis, and hermaphroditism. The largest subgroup of the Branchiopods, the Diplostraca, is reported to encompass all five of these breeding systems. However, many of these reports are based primarily on simple observations of sex ratios in natural populations. Herein we report the beginnings of a more rigorous approach to breeding system determination in the Diplostraca, starting with the family Limnadiidae. We combine measurements of sex ratio, offspring rearings, and behavior to identify three breeding systems within the Limnadiidae: dioecy, androdioecy, and selfing hermaphroditism. To date, no instances of parthenogenetic reproduction have been identified in this family. Comparisons of breeding system determination via simple population sex ratios with our more controlled studies show that simple sex ratios can be useful when these sex ratios are ∼50% males (=dioecy) or 5–30% males (androdioecy). However, population sex ratios of 0–5% males or 35–45% males necessitate further investigation because estimates in these ranges cannot distinguish selfing hermaphroditism from androdioecy or androdioecy from dioecy, respectively. We conclude by noting that the genetic sex-determining system outlined for one of these limnadiid species, Eulimnadia texana , provides a parsimonious framework to describe the evolution of the three breeding systems observed within the Limnadiidae.     

Sex change strategy and the aromatase genes

Sequential hermaphroditism is a common reproductive strategy in many teleosts. Steroid production is known to mediate both the natural and induced sex change, yet beyond this the physiology directing this process has received little attention. Cytochrome P450 aromatase is a key enzyme in the hormonal pathway catalysing the conversion of sex steroids, androgens to oestrogens, and thus is highly relevant to the process of sex change. This study reports the isolation of cDNA sequences for aromatase isoforms CYP19A1 and CYP19A2 from teleost species representing three forms of sexual hermaphroditism: Lates calcarifer (protandry), Cromileptes altivelis (protogyny), and Gobiodon histrio (bi-directional). Deduced amino acid analysis of these isoforms with other reported isoforms from gonochoristic (single sex) teleosts revealed 56–95% identity within the same isoform while only 48–65% identity between isoforms irrespective of species and sexual strategy. Phylogenetic analysis supported this result separating sequences into isoform exclusive clades in spite of species apparent evolutionary distance. Furthermore, this study isolates 5′ flanking regions of all above genes and describes putative cis-acting elements therein. Elements identified include steroidogenic factor 1 binding site (SF-1), oestrogen response element (ERE), progesterone response element (PRE), androgen response element (ARE), glucocorticoid response elements (GRE), peroxisome proliferator-activated receptor /retinoid X receptor heterodimer responsive element (PPAR/RXR), nuclear factor kappaβ (NF-kappaβ), SOX 5, SOX 9, and Wilms tumor suppressor (WTI). A hypothetical in vivo model was constructed for both isoforms highlighting potential roles of these putative cis-acting elements with reference to normal function and sexual hermaphroditism.     

Alternative reproductive styles in seabreams (Pisces: Sparidae)

Synopsis A review of sexuality in the Sparidae shows that protandrous, protogynous, simultaneous and rudimentary hermaphroditism have all been reported in the family. Careful histological study shows that even in those species reputed to have separate sexes, intersexuality is found in the juvenile condition. We suggest that two reproductive styles, sex change and late gonochorism are found in the family. The bi-potentiality of the sparid gonad is considered to be a pre-adaptation for the development of sequential hermaphroditism in species in which reproductive success is size related. In these species sex change is an alternative reproductive style that enables individuals to maximise their lifetime reproductive success by functioning as one sex when small and the other sex when large.     

A review of MHC‐based mate preferences and fostering experiments in two congenic strains of mice

We review our studies of mate choice with two MHC‐congenic strains of mice. This work was stimulated by findings from Yamazaki and colleagues showing that male mice exhibited mate preferences for females whose MHC‐haplotype was different from their own, while female mice exhibited either no preference or a weak preference for males of a particular MHC‐haplotype (see Beauchamp et al., 1988). Since these findings were unexpected (mate choice theory predicts that females will be more selective than males), we studied the preferences of mice from two additional MHC‐congenic strains to assess the generality of the previous findings. Specifically, the goals of our research were: (1) to determine the mate preferences of congenic mice with MHC‐haplotypes derived from wild populations, (2) to compare the mate preferences of male and female mice in a test situation where each sex has a clear opportunity to make a choice, and (3) to estimate effects of cross‐fostering on each sex. This revised version was published online in July 2006 with corrections to the Cover Date.     

The use of pulse‐echo acoustic microscopy to non‐invasively determine the sex of living larval sea lampreys

A rapid, accurate and non‐invasive method to determine the sex of larval sea lampreys Petromyzon marinus , using wide‐field pulse‐scanning acoustic microscopy, is described. Cross‐sectional pulse‐echo scans were made with a high‐resolution acoustic microscope in 48 larvae (110–130 mm total length, L _T), and the acoustic images generated showed such internal body structures as the gonad, intestine, kidneys, cardinal veins, notochord and musculature. Females were identified by the presence of a relatively large (1–1·5 mm diameter) ovary, which was considerably less reflective to the 15 to 25 MHz acoustic signals than the surrounding kidney tissue. Males were recognized by the lack of the large non‐reflective ovary and, in some cases, the appearance of a small (0·2–0·3 mm) testis with slightly stronger reflective properties than the kidney. Identification of sex was confirmed by optical microscopy following dissection, and in a blind test on an additional 10 specimens (121–168 mm L _T), the acoustic method reliably identified sex in 100% of the larvae. These results indicate that acoustic microscopy can determine the sex of live sea lamprey larvae in c . 30 s per animal, a process which until now required dissection or invasive surgery.     

Toxicological effects and storage of cadmium and mercury in an insect Locusta migratoria (Orthoptera)

Toxicity of cadmium and mercury depends on the age and sex of contaminated locust imagoes. Both metals produce fat body injury, consisting in a reduction of energy reserves. They also disturb the function of the female genital apparatus. It is suggested that Hg has a direct effect on the germinal and the somatic cells of the reproductive system, whereas Cd inhibits the differentiation of the fat body cells and therefore the synthesis of the yolk products. No metallothionein has been detected; but Cd induces the production of a Cd-binding glycoprotein with a binding of Cd in the stoichiometric ratio 1 glycoprotein/1 metal. Besides the glycoprotein, mineralized ommochrome granules are important storage sites for Cd.     

Body shape variation and colour change during growth in a protogynous fish

Protogynous sequential hermaphroditism is very common in marine fish. Despite a large number of studies on various aspects of sequential hermaphroditism in fish, the relationship between body shape and colour during growth in dichromatic species has not been assessed. Using geometric morphometrics, the present study explores the relationship between growth, body shape and colouration in Coris julis (L. 1758), a small protogynous labrid species with distinct colour phases. Results show that body shape change during growth is independent of change in colour phase, a result which can be explained by the biology of the species and by the social control of sex change. Also, during growth the body grows deeper and the head has a steeper profile. It is hypothesized that a deeper body and a steeper profile might have a function in agonistic interactions between terminal phase males and that the marked chromatic difference between colour phases allows the lack of strict interdependence of body shape and colour during growth.     

Protogynous sex change in the haremic triggerfish Sufflamen chrysopterus (Tetraodontiformes)

The size-advantage model predicts that protogyny is likely to evolve in polygynous species. Polygynous mating systems have been reported from several species of triggerfishes (Balistidae), but sex change has never been confirmed among them. We performed male-removal experiments in the haremic triggerfish Sufflamen chrysopterus on the coral reefs of Sesoko Island, Okinawa. After removal and movement of territorial males, some females became single and later changed body color and sex. This is the first report of sequential hermaphroditism from Tetraodontiformes.     

The relationship between mating system and simultaneous hermaphroditism in the coral reef fish, Hypoplectrus nigricans (Serranidae)

The behaviour and reproductive ecology of the simultaneously hermaphroditic coral reef fish, Hypoplectrus nigricans (Serranidae), the black hamlet, was investigated in an effort to elucidate the relationship between simultaneous hermaphroditism and mating behaviour. The major features of the mating system are as follows. (1) Hamlets spawn only in pairs, one partner releasing eggs and the other fertilizing them. There is no selfing. (2) Eggs are planktonic. There is no parental care. (3) The major courtship display serves to advertise that an individual has ripe eggs. (4) A clutch is not released in a single spawn but is parcelled over several, usually with the same partner. (5) Partners generally alternate sex roles with each spawn: that is, they take turns giving up parcels to be fertilized. This active reciprocation of release of eggs, called egg trading, means that reproductive success as a male depends upon the ability to reproduce as a female. Since most of the reproductive effort of an individual is spent on female functions, egg trading provides a fecundity advantage to hermaphroditism, making it evolutionarily stable relative to dioecy (separate sexes). The advantage is analogous to that which parthenogenetic organisms have over sexual ones. The fecundity advantage under egg trading can account for the maintenance, but not the origin of simultaneous hermaphroditism, since hermaphroditism must be established before egg trading can evolve.     

Hermaphroditism as a reproductive strategy for metazoans; some correlated benefits

Abstract

The concept of hermaphroditism is examined, the terminology is reviewed, and several new terms are proposed: EUHERMAPHRODITISM for the occurrence together of eggs and sperm in the individual that produced them; TEMPORARY HERMAPHRODITISM for the few instances where euhermaphroditism is a brief transitional phase between sexes in protandry and protogyny, and opsiautogamy to designate the condition where sperm saved from an early male phase are used to fertilise eggs produced in a later female phase. An animal that functions successively in the different sex roles is considered to be quite distinct from one that functions as both male and female simultaneously. Further, the circumstances in which these different sexual modes are appropriate and the advantages that accrue from them are quite different. For this reason protandry, protogyny, and consecutive sexuality are not considered to be part of hermaphroditism, but rather aspects of labile gonochorism.

A major idea advanced in this paper is that hermaphroditism is of primary importance as a reproductive strategy of very small metazoans. In such animals, whose eggs are so disproportionately large that very few can be produced, hermaphroditism ensures that through having the maximal number of females the maximal number of eggs are produced and fertilised economically. For very small hermaphrodites the mate-finding difficulties associated with small size and limited motility are reduced by converting each meeting into a potential mating. Further, in hermaphroditism not only is the frequency of mating maximised. but through sperm storage the effects of matings last for a long time. and through multiple reciprocal copulations genetically diverse progenies are produced. The effective size of the gene pool is maximised, and the risk of genetic drift in sex ratio in small populations is avoided. Very small animals do not have the energetic resources to produce large numbers of large, yolky eggs, nor do they have the space in which to store them before release. Thus tiny hermaphrodites tend to produce a few eggs at a time, but over extended or continuous breeding seasons. The effects of their reduced fecundity may be further offset by precise methods of fertilisation, brooding, and commonly the suppression of pelagic phases, thus minimising losses from larval predation and overdispersal.

It is also argued that hermaphroditism may have been advantageous because of features often associated with it. Copulation with protected sperm transfer may have been especially important, not only because of economies in gamete production and use, but also in the exploitation of new habitats. In freshwater hermanhrodites copulatory or spermatophore exchange habits protect sperm from osmotic death: in endoparasites copulation protects sperm from digestive enzymes and osmotic stress in the host’s gut, and from antibodies and phagocytosis in the bloodstream.