Diurnal dynamics of S‐phase entry of germ cells in the secondary testis of the bambooleaf wrasse (Pseudolabrus sieboldi)
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Abstract The diversity of reproductive strategies found in fish is attributed to the adaptation of gametogenesis to different habitats. To date, however, information about the dynamics of male gametogenesis and its molecular mechanisms of control by the brain–pituitary–gonadal (BPG) axis, a well‐known facet of the endocrine system in vertebrates, is not sufficient to explain the variation in spawning and regulatory mechanisms among species. The bambooleaf wrasse ( Pseudolabrus sieboldi ) is a protogynous hermaphrodite fish that shows clear diurnal fluctuations in gonadotropin gene expression and serum sex steroid levels associated with spawning. In this study, morphometrical and histological analyses were performed to determine the number of spermatogonial generations in the testis of the sex‐changed male (secondary testis). In addition, the diurnal dynamics of S‐phase entry of germ cells was explored by measuring the frequency of BrdU‐incorporating germ cells at different times of day. We found that the bambooleaf wrasse spermatozoa were generated through nine spermatogonial generations, followed by meiotic divisions accompanied by loss of some spermatocytes and spermatids through apoptosis. BrdU analyses revealed a high frequency of entry into S‐phase of undifferentiated type A spermatogonia at 03:00 hr. On the other hand, the frequency of spermatocytes at S‐phase of the cell cycle decreased during 00:00–09:00 hr. This study demonstrates for the first time the daily fluctuations of S‐phase entry of male germ cells in fish. These results will provide a useful foundation for understanding the roles of endocrinological and cytological regulation of fish spermatogenesis. J. Exp. Zool. 315A:232–241, 2011 . © 2011 Wiley‐Liss, Inc.Keywords:
Hermaphrodite
Wrasse
Sex change
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For many fish populations reproductive patterns remain unknown, which often results in inadequate management strategies. Timing and intraspecific variability in the main reproductive traits of ballan wrasse (Labrus bergylta) were investigated based on microscopic analysis of gonads sampled from NW Spain in 2009–2012. This species displays two main body colour patterns, plain and spotted, which coexist in sympatry. Females spawned from January to April whereas spawning capable males were present almost year-round. Length at 50% maturity did not differ between colour patterns and was above the minimum catch size. Plain individuals attained the length and age at 50% sex change earlier than spotted individuals, which might be explained by differences in growth patterns, mortality rates or by an evolutionary genetic divergence between populations. Individuals with gonads infected by encysted trematode metacercariae were associated with an earlier timing of sex change, which represents one of the few examples of a possible parasitic influence on the sex allocation of its host. Our findings provide a framework for scientific-based management of this hermaphrodite fish.
Hermaphrodite
Sex change
Wrasse
Harem
Juvenile fish
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The gonadal organization and cytological characteristics of gametogenesis in a population of the freshwater clam Musculium argentinum (d'Orbigny, 1835) are described. Sections of the rather small gonad demonstrate the existence of hermaphroditic specimens, and is composed of hermaphrodite follicles among the intestine coils in the posterior dorsal region of the body. Follicles contain male and female germ cells at different stages of maturation, which can be recognized by their shape, size, and nuclear features. Male germ cells are organized in cysts, and spermatocytes do carry out meiosis. Within follicles, male and female germ cells occupy different regions. Gonad activity throughout the year is coincident with the life cycle pattern of the M. argentinum population studied previously.
Hermaphrodite
Germ plasm
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Hermaphrodite
Sex change
Sex allocation
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Wild Ballan wrasse Labrus bergylta were sampled monthly over 2 years in western Norway to identify the natural process of sex change in this species. Light microscopy of standard histological‐stained and immunohistochemistry‐treated gonad tissue showed that spermatogonial germ cells tended to proliferate around the periphery of the lamellae before filling into the slowly receding, apoptotic central areas of the lamellae. Sex change occurred following the breeding season. From July to September, fish were most often in an early state of gonadal transition ( ET ), characterized by degenerating previtellogenic oocytes and pockets of proliferating spermatogonia in the germinative epithelia. The majority of fish with late transitional gonads, that were typically dominated by spermatogenic cells, developing efferent ducts and the beginning of lobule formation, were found between October and November. Sex steroid profiles of fish representing the different sexual phases showed that breeding females had the highest concentrations of 17β oestradiol ( E 2 ) and the lowest concentration of 11 ketotestosterone ( 11KT ). Concentrations of E 2 decreased greatly in ET fish at the beginning of sex change and remained low in all subsequent phases. The opposite trend was demonstrated in 11KT profiles. Initial‐phase female fish had minimal concentrations of 11KT, but these increased during subsequent transitions. Sex change occurred most often in fish 34–41 cm total length ( L T ) and the median of fish in the size‐frequency overlap of female and male fish was 36 cm L T .
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A set of sex chromosomes is required for gametogenesis in both males and females, as represented by sex chromosome disorders causing agametic phenotypes. Although studies using model animals have investigated the functional requirement of sex chromosomes, involvement of these chromosomes in gametogenesis remains elusive. Here, we elicit a germ cell-intrinsic effect of sex chromosomes on oogenesis, using a novel culture system in which oocytes were induced from embryonic stem cells (ESCs) harboring XX, XO or XY. In the culture system, oogenesis using XO and XY ESCs was severely disturbed, with XY ESCs being more strongly affected. The culture system revealed multiple defects in the oogenesis of XO and XY ESCs, such as delayed meiotic entry and progression, and mispairing of the homologous chromosomes. Interestingly, Eif2s3y, a Y-linked gene that promotes proliferation of spermatogonia, had an inhibitory effect on oogenesis. This led us to the concept that male and female gametogenesis appear to be in mutual conflict at an early stage. This study provides a deeper understanding of oogenesis under a sex-reversal condition.
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Wrasse
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This study describes the seasonal reproductive cycle, gonad structure, and sex ratio of the Anodonta gabillotia pseudodopsis. A total of 300 individuals was collected in monthly samples from September 2005 to August 2006 in Göolbaşi Lake, Turkey. Calculation of the gonadosomatic index and histological examination of the gonads showed that gametogenesis began in winter and spawning occurred in summer and early autumn. Although, sex ratios of Anodonta gabillotia pseudodopsis were not significantly different from the expected 1:1 ratio (P > 0.05), slightly female biased sex ration were recorded. Although mature oocytes and spermatozoa were present for almost the entire year, gonadal activity seemed lowest in October and December, when gonad recovery and reorganization were more evident than gametogenesis. Both sexes displayed greatest gonad activity during the summer months of the year. Three types of gonads were identified, which varied according to the proportion of gametogenic tissue. According to our morphologic and histologic observation, Anodonta gabillotia pseudodopsis were classified as accidental or abnormal hermaphrodite (typically in dioecious species) species. The hermaphroditic specimens of A. pseudodopsis had gonads composed predominately of tissue of only female. These results suggest that under certain environmental conditions females may become hermaphrodites and self-fertilization occur.
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Unionidae
Gonadosomatic Index
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Abstract Relatively few studies have addressed fishery-induced-evolution of sequential hermaphrodites although declines in the mean size-at-maturation and/or sex change have been documented for several species. We sought to explore the evolutionary impacts of size-selective exploitation on maturation and sex change of a protogynous hermaphrodite using an individual-based model accounting for growth, survival, maturation, sex change, and reproduction. Because sex change rules are unknown for many exploited species, critical size-at-sex change (static and genetic control) and social control of sex change were evaluated to determine how life-history-traits (maturation, sex change) and population reference points change due in part to evolution. When simulating critical size-at-sex change, mean length-at-maturation increased, contrary to typical predictions for dioecious species, and mean length-at-sex change decreased (when under genetic control) from exploitation. These changes occurred slowly and resulted in lower male: female sex ratios, sperm limitation, and extirpation at high exploitation rates. Under social control of sex change, both the mean lengths-at-maturation and sex change decreased relatively rapidly from exploitation. These populations maintained high male: female sex ratios, avoided sperm limitation, and withstood higher exploitation rates than critical size-at-sex change populations. Results from these models highlight the need for a better understanding of sex change rules for exploited hermaphrodites.
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Environmental change
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