Protogynous Wrasse Research Articles

Female spawning migrations of the protogynous wrasse,Halichoeres marginatus

Spawning sites and spawning migration paths of tagged females of the protogynous wrasse,Halichoeres marginatus, were studied on the shallow reefs at Kuchierabu-jima Island, Japan. Males set up mating territories above prominent rocks on the offshore reef slope in the late afternoon, and pair-spawned with females, which had migrated there from their home ranges located in inshore areas. Small females migrated to the spawning sites near their home ranges, whereas large females migrated to various spawning sites located within a wide area, including downcurrent sites. Spawning at the downcurrent sites favors transport of eggs offshore, thereby increasing the female’s fitness. The spawning sites where an individual had spawned as a female were subsequently used for mating after it had changed sex. It is suggested that the wide migration of females to various spawning sites, enables the storing up of information on those sites, which later helps in the acquisition of mating territories after changing sex.

Sex differentiation and gonadal development in the diandric, protogynous wrasse, Thalassoma bifasciatum (Pisces, Labridae)

One hypothesis that would unify many of the apparently diverse patterns of gonadal differentiation in teleost fishes under a single conceptual scheme is that individuals develop in a female direction unless a masculinizing mechanism intervenes. We provided a descriptive test of this hypothesis in a diandric, protogynous wrasse in which males are produced through two, apparently different developmental sequences: ‘primary males’ develop testes as juveniles and remain male throughout life, while ‘secondary males’ develop ovaries as juveniles and later in adult life the functional ovary redifferentiates into a functional testis. The gonads of 128 individuals, from the smallest juveniles to full‐sized adults, were examined histologically. Gonads of the smallest juveniles were undifferentiated or contained young oocytes with no ovarian cavity and no testicular tissue. As individuals increased in size, the proportion of oocytic gonads increased. The distribution of gonad types for larger individuals suggested that a portion ofthese oocytic gonads developed into ovaries, while another portion lost its oocytic elements and became testes. These patterns supported the hypothesis that the gonads of all individuals, including primary males, passed through an initial female phase prior to differentiating into an ovary or testis. The structure of primary testes was not identical to the structure of secondary testes. The critical difference between the two types lay in the presence of a large central cavity in the latter that was not present in the former. Positional differences in the duct system were only found in the posterior region of the gonad and were the consequence of a lateral internal split in the secondary gonad resulting from confluence of the central cavity.

Histology, ultrastructure, and in vitro steroidogenesis of the testes of two male phenotypes of the protogynous fish, Thalassoma duperrey (labridae)

Species with multiple male reproductive phenotypes may serve as model systems to study the relationship between form and function in reproduction. Large and small males of the protogynous wrasse, Thalassoma duperrey differ in reproductive behavior, gonad morphology, and gonadal steroid production. Initial-phase (IP) males are small males that spawn in groups. They have large testes with high sperm production. Terminal-phase (TP) males are large, defend temporary spawning territories, and spawn individually with females. TP males are derived from either IP males or from sex-changed females. Regardless of origin, TP males have much smaller testes than do IP males, but steroid-producing Leydig cells in the gonads of TP males appear more numerous and better developed. Testes of TP males produce more testosterone (T) and especially 11-ketotestosterone (11-KT) in vitro than do testes of IP males, and the production is more responsive to salmon gonadotropin. 11-KT was the major metabolite produced by incubating the gonads of TP males with 14C-labeled steroid precursors. In vitro 11-KT production was correlated with plasma levels of 11-KT in TP males and these levels were significantly higher than those of IP males. The in vitro conversion of 17α-hydroxyprogesterone to 17α,20β-progestogen (17α,20β-P) for both types of males was similar, and was highest in winter when spawning occurred every day. Basal production of 17α,20β-P was similar in IP and TP male testes, and was enhanced by gonadotropin. The enzyme 20β-hydroxysteroid dehydrogenase, responsible for the conversion of 17α-hydroxyprogesterone to 17α,20β-P resided in the sperm. These results indicate a function of 17α,20β-P in male reproductive function, probably spermiation, and a relationship of Leydig cell development and high levels of 11-KT production to the terminal male phenotype, perhaps reproductive or aggressive behavior, rather than to male gametogenesis per se.

Histological and ultrastructural evidence for the role of gonadal steroid hormones in sex change in the protogynous wrasse Thalassoma duperrey

The process of sex change in the protogynous wrasse, Thalassoma duperrey, was investigated through histological and ultrastructural observations on the gonads of females changing sex to male. Changes in plasma steroid levels concomitant with structural changes were measured by radioimmunoassay. The process of sex change from ovary to testis was divided into six stages on the basis of changes in the structure of the germinal and somatic elements. Ovaries of females were filled with vitellogenic oocytes during the breeding season, but contained no spermatogenic tissue (Stage 1). At the commencement of sex change (Stage 2), vitellogenic oocytes began to degenerate, and were ingested by macrophagous cells. This stage was accompanied by a rapid drop in plasma levels of estradiol-17β. Thereafter, previtellogenic oocytes (Stage 3) also began to degenerate, and aggregations of stromal tissue, and loose connective tissue were observed in the central region of the lamellae. Steroid producing cells (Leydig cells), developed at the border of this loose connective tissue. Presumed spermatogonia proliferated on the periphery of the lamellae, and Leydig cells increased in size and number (Stage 4). Spermatogonia formed cysts, and underwent spermatogenesis (Stage 5). Finally, sex change to male was considered complete, with the beginning of active spermatogenesis and spermiation (Stage 6). Plasma levels of testosterone remained low throughout the sex change, but a second androgen, 11-ketotestosterone increased gradually in parallel to the increased numbers of Leydig cells and spermatogonia. Preliminary in vitro incubation of gonads with salmon gonadotropin, revealed that sex-changed males had higher levels of 11-ketotestosterone production than did females, while females had higher levels of estradiol-17β production than did males. Production of both these steroids increased in a dose-related fashion with increasing doses of gonadotropin.

THE COSTS OF CHANGING SEX AND THE ONTOGENY OF MALES UNDER CONTEST COMPETITION FOR MATES

In its simplest form, the size-advantage hypothesis predicts that individuals should change sex in order to increase their reproductive success. In terms of lifetime expectations, this must be true for the hypothesis to hold. However, as we review here, some loss of reproductive success may occur immediately after sex change. Unavoidable costs (e.g., those resulting from a restructuring of the gonad) have not been adequately distinguished from adaptive allocations of resources which diminish current reproduction in favor of large increases in future mating success. This strategy can become particularly important for species in which a few males monopolize matings. To illustrate this idea, we describe the changes in mating frequency as mature females become sexually active males in three species of protogynous wrasses. In one species, a male defends a permanent, all-purpose territory composed of up to 12 females. When he is removed, a single female changes sex and successfully completes mating sequences with all females in the territory within an average of 5.6 days. This duration roughly corresponds to the time required for functional transformation of gonads; thus, individuals in this species suffer few reproductive losses as a result of changing sex. The largest males in two other species mate with an average of 25 to 50 females per day, but only by successfully defending reproductive territories. In one of those species, individuals that changed sex mated infrequently over a two-year period after sexual transformation and, by the end of the study, were still well below the average size of males that consistently obtained territories. Sex-changed individuals in the other species had very low reproductive success for up to 45% of the maximum lifespan as a male. It is improbable that the substantial cost of changing sex in the latter two species results from gonad restructuring or from mistakes due to imprecise cues for sex change. Instead, the cost appears to represent an investment in growth rather than current reproduction as a means of rapidly attaining a size advantage when individuals face intense competition for extraordinarily successful mating territories.

In vitro studies on steroid metabolism by gonadal tissues from ambisexual teleosts. I. Conversion of [ 14C]testosterone by males and females of the protogynous wrasse Coris julis L

Gonadal tissue of females, and primary and secondary males of the protogynous wrasse Coris julis were incubated with labeled [ 14C]testosterone. The large majority of metabolic products consisted of free, neutral steroid. Marked 11β-hydroxylation was restricted to testes from secondary males. 5β-Reduction of ring A was predominant in both types of males, whereas ovarian tissue from normal females produced a larger share of 5α-androstanes. The metabolic products of ovaries from females that were injected with testosterone 7 days before incubation were similar to those of untreated females, although the ratio of 5α 5β reduced steroids was changed toward the “male type”.

Spawning-site choice by female Pseudolabrus celidotus (Pisces: Labridae) and its influence on the mating system

1. The mating system and seasonal patterns of behaviour of the protogynous wrasse Pseudolabrus celidotus were studied for 2 years in a shallow reef habitat in north-eastern New Zealand, with the purpose of determining how site-specific spawning by females influences the behaviour and spawning success of terminal phase (TP) males. 2. Females were home ranging but made temporary trips into deeper areas during the breeding season solely for the purpose of spawning. Most TP males defended territories from other TP males, but nonterritorial, wide-ranging males commonly moved through the study area in the spaces between territories. The number of territories was highly variable, with only certain deeper sites being occupied consistently. Home ranges overlapped considerably with each other and with territories, but females were never actively confined to their ranges by TP males. 3. Spawning success of TP males was not related to body size, age, coloration, or territory size. Successful males were generally resident for longer periods, spent more time swimming, courting and behaving aggressively towards initial phase (IP) fish, and less time feeding during the spawning season. Testis weight: body weight ratios were positively correlated with spawning success. Spawning rate increased exponentially with the depth of the territory and was highest on territories with large patches of shelter centred on bare rock areas. 4. Experimental removal of TP males established that females were choosing particular sites to spawn at, and spawned only with TP males possessing these sites. Females presumably chose to spawn deep because egg-eating planktivorous fish were more abundant in shallow areas. The restriction of spawnings to areas adjacent to shelter sites suggests that females were vulnerable to predators during the spawning act. 5. The mating system is classified as ‘resource defence polygyny’ (Emlen and Oring 1977) since TP males defending preferred spawning sites accounted for the large majority of the spawnings. The influence of spawning-site selection on the territorial system is discussed.

Age, growth and feeding in the ballan wrasse Labrus bergylta Ascanius 1767

A study of the age, growth and feeding of the protogynous wrasse Labrus bergylta (Teleostei: Labridae) was made on 25 male and 316 female specimens taken from the southern coasts of the Isle of Man from October 1972 to October 1974. Age determination and back‐calculations for length were made from the opercular bones. The oldest male and female specimens were 29 and 25 years old respectively. The growth curves showed only a slight increase in growth rate after sexual inversion, and a pattern of slow irregular increase, with no pronounced levelling off in old fish. The time of sexual inversion varied widely: intersexual specimens of 5 and 14 years were found. The youngest functional male was 6 years old. The weight/length relationships of males and females were very similar and the following equation, derived from all individuals, was used to calculate weights for age utilizing the back‐calculated lengths: image The mouth, pharyngeal teeth and gut length to fish length ratio (0.622) suggested an omnivorous diet. Analysis of gut contents confirmed this, with decapod Crustacea, isopods and molluscs the dominant food items. There were seasonal changes in feeding intensity and composition of the diet, related to temperature changes, onshore‐offshore migration patterns, availability of food items, and changes in habitat associated with maturation.

Dualistic reproductive behavior in the protogynous wrasseThalassoma bifasciatum and some observations on its day-night changeover

1.Thalassoma bifasciatum is a protogynous wrasse with (partial) sexual dimorphism and male dichromatism. Sex-inversion takes place without affecting the color pattern. 2. Males with female-like color dress indulge in group spawning; males with the bright color pattern perform pair spawning. 3. Among the brightly colored males exists a well-established hierarchy. Dominant males only have a particular spawning area in which they spawn daily at a certain time around noon. The spawning area is optically marked by conspicuous behavior of the bright male. Courtship activities towards individual partners are rather superficial. 4. The female has the leading role in pair spawning. In the extremely short spawning act a female may release, simultaneously, more than 2000 eggs. 5. Group spawning occurs in well-populated reef areas only. The basic pattern of group spawning has many similarities to pair spawning. 6. Day-night changeover ofT. bifasciatum is closely correlated to the time of sunset and sunrise. 7. The possible biological significance of the dualistic spawning behavior is discussed, and advantages as well as drawbacks of studies in the sea and in aquaria are considered.

Some remarks on secondary sex characters, sex and sexual behavior in teleosts

After castration, males of the mouth-breeding cichlid fish, Hemihaplochromis multicolor, lose their sexual and aggressive behavior but return to full activity a few days after an injection of testosterone. The behavior of females becomes completely masculinized after treatment with testosterone. Thus, the influence of androgens on male behavior of this cichlid is similar to that found in many other vertebrates. Data on the endocrine control of behavior in cichlid fish are scanty compared with the extensive knowledge of behavioral adaptations within this group. A discussion of the hypothetical role of eye-spots in the anal fin of mouth-breeding cichlids, and some data on the influence of androgens on the formation of color marks should caution against generalized conclusions on the relationship between hormone-dependent secondary sex characters and their role in the hormonal regulation of behavior. Similar considerations apply to color change and sexual behavior in protogynous wrasses. Present knowledge of the effects of exogenous testosterone does not agree with observations on the relations among spontaneous sexual transformation, changes of the livery, and different types of reproductive behavior.

Protogynie bei Papageifischen (Scaridae)

Histological investigation of the gonads of 24 specimens of parrotfishes, belonging to several species, revealed the existence of secondary males and of females changing into males in this family. These findings are very similar to those having been described in protogynous wrasses. Considering various data in the literature on sexual dichromatism and spawning behavior, it may be concluded that parrotfishes are protogynous, just as some wrasses, to which they are closely related.