skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: A case of hermaphroditism in the gonochoristic sea urchin, Strongylocentrotus purpuratus , reveals key mechanisms of sex determination
Abstract Sea urchins are usually gonochoristic, with all of their five gonads either testes or ovaries. Here, we report an unusual case of hermaphroditism in the purple sea urchin, Strongylocentrotus purpuratus. The hermaphrodite is self-fertile, and one of the gonads is an ovotestis; it is largely an ovary with a small segment containing fully mature sperm. Molecular analysis demonstrated that each gonad producedviable gametes, and we identified for the first time a somatic sex-specific marker in this phylum: Doublesex and mab-3 related transcription factor 1 (DMRT1). This finding also enabled us to analyze the somatic tissues of the hermaphrodite, and we found that the oral tissues (including gut) were out of register with the aboral tissues (including tube feet) enabling a genetic lineage analysis. Results from this study support a genetic basis of sex determination in sea urchins, the viability of hermaphroditism, and distinguish gonad determination from somatic tissue organization in the adult.  more » « less
Award ID(s):
1923445
PAR ID:
10542328
Author(s) / Creator(s):
; ;
Publisher / Repository:
Wiley
Date Published:
Journal Name:
Biology of Reproduction
Volume:
108
Issue:
6
ISSN:
0006-3363
Page Range / eLocation ID:
960 to 973
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Li, Jaimei (Ed.)
    Abstract Sex determination (SD) involves mechanisms that determine whether an individual will develop into a male, female, or in rare cases, hermaphrodite. Crustaceans harbor extremely diverse SD systems, including hermaphroditism, environmental sex determination (ESD), genetic sex determination (GSD), and cytoplasmic sex determination (e.g.,Wolbachiacontrolled SD systems). Such diversity lays the groundwork for researching the evolution of SD in crustaceans, i.e., transitions among different SD systems. However, most previous research has focused on understanding the mechanism of SD within a single lineage or species, overlooking the transition across different SD systems. To help bridge this gap, we summarize the understanding of SD in various clades of crustaceans, and discuss how different SD systems might evolve from one another. Furthermore, we review the genetic basis for transitions between different SD systems (i.e.,Dmrtgenes) and propose the microcrustaceanDaphnia(clade Branchiopoda) as a model to study the transition from ESD to GSD. 
    more » « less
  2. Schartl, Manfred (Ed.)
    Sex is determined by multiple factors derived from somatic and germ cells in vertebrates. We have identifiedamhy,dmrt1,gsdfas male andfoxl2,foxl3,cyp19a1aas female sex determination pathway genes in Nile tilapia. However, the relationship among these genes is largely unclear. Here, we found that the gonads ofdmrt1;cyp19a1adouble mutants developed as ovaries or underdeveloped testes with no germ cells irrespective of their genetic sex. In addition, the gonads ofdmrt1;cyp19a1a;cyp19a1btriple mutants still developed as ovaries. The gonads offoxl3;cyp19a1adouble mutants developed as testes, while the gonads ofdmrt1;cyp19a1a;foxl3triple mutants eventually developed as ovaries. In contrast, the gonads ofamhy;cyp19a1a,gsdf;cyp19a1a,amhy;foxl2,gsdf;foxl2double andamhy;cyp19a1a;cyp19a1b,gsdf;cyp19a1a;cyp19a1btriple mutants developed as testes with spermatogenesis via up-regulation ofdmrt1in both somatic and germ cells. The gonads ofamhy;foxl3andgsdf;foxl3double mutants developed as ovaries but with germ cells in spermatogenesis due to up-regulation ofdmrt1. Taking the respective ovary and underdeveloped testis ofdmrt1;foxl3anddmrt1;foxl2double mutants reported previously into consideration, we demonstrated that oncedmrt1mutated, the gonad could not be rescued to functional testis by mutating any female pathway gene. The sex reversal caused by mutation of male pathway genes other thandmrt1, including its upstreamamhyand downstreamgsdf, could be rescued by mutating female pathway gene. Overall, our data suggested thatdmrt1is the only male pathway gene tested indispensable for sex determination and functional testis development in tilapia. 
    more » « less
  3. Animal taxa show remarkable variability in sexual reproduction, where separate sexes, or gonochorism, is thought to have evolved from hermaphroditism for most cases. Hermaphroditism accounts for 5% in animals, and sequential hermaphroditism has been found in teleost. In this study, we characterized a novel form of the transient hermaphroditic stage in little yellow croaker ( Larimichthys polyactis ) during early gonadal development. The ovary and testis were indistinguishable from 7 to 40 days post-hatching (dph). Morphological and histological examinations revealed an intersex stage of male gonads between 43 and 80 dph, which consist of germ cells, somatic cells, efferent duct, and early primary oocytes (EPOs). These EPOs in testis degenerate completely by 90 dph through apoptosis yet can be rescued by exogenous 17- β -estradiol. Male germ cells enter the mitotic flourishing stage before meiosis is initiated at 180 dph, and they undergo normal spermatogenesis to produce functional sperms. This transient hermaphroditic stage is male-specific, and the ovary development appears to be normal in females. This developmental pattern is not found in the sister species Larimichthys crocea or any other closely related species. Further examinations of serum hormone levels indicate that the absence of 11-ketotestosterone and elevated levels of 17- β -estradiol delineate the male intersex gonad stage, providing mechanistic insights on this unique phenomenon. Our research is the first report on male-specific transient hermaphroditism and will advance the current understanding of fish reproductive biology. This unique gonadal development pattern can serve as a useful model for studying the evolutionary relationship between hermaphroditism and gonochorism, as well as teleost sex determination and differentiation strategies. 
    more » « less
  4. Conradt, B (Ed.)
    Abstract Sexual characteristics and reproductive systems are dynamic traits in many taxa, but the developmental modifications that allow change and innovation are largely unknown. A leading model for this process is the evolution of self-fertile hermaphrodites from male/female ancestors. However, these studies require direct analysis of sex determination in male/female species, as well as in the hermaphroditic species that are related to them. In Caenorhabditis nematodes, this has only become possible recently, with the discovery of new species. Here, we use gene editing to characterize major sex determination genes in Caenorhabditis nigoni, a sister to the widely studied hermaphroditic species Caenorhabditis briggsae. These 2 species are close enough to mate and form partially fertile hybrids. First, we find that tra-1 functions as the master regulator of sex in C. nigoni, in both the soma and the germ line. Surprisingly, these mutants make only sperm, in contrast to tra-1 mutants in related hermaphroditic species. Moreover, the XX mutants display a unique defect in somatic gonad development that is not seen elsewhere in the genus. Second, the fem-3 gene acts upstream of tra-1 in C. nigoni, and the mutants are females, unlike in the sister species C. briggsae, where they develop as hermaphrodites. This result points to a divergence in the role of fem-3 in the germ line of these species. Third, tra-2 encodes a transmembrane receptor that acts upstream of fem-3 in C. nigoni. Outside of the germ line, tra-2 mutations in all species cause a similar pattern of partial masculinization. However, heterozygosity for tra-2 does not alter germ cell fates in C. nigoni, as it can in sensitized backgrounds of 2 hermaphroditic species of Caenorhabditis. Finally, the epistatic relationships point to a simple, linear germline pathway in which tra-2 regulates fem-3 which regulates tra-1, unlike the more complex relationships seen in hermaphrodite germ cell development. Taking these results together, the regulation of sex determination is more robust and streamlined in the male/female species C. nigoni than in related species that make self-fertile hermaphrodites, a conclusion supported by studies of interspecies hybrids using sex determination mutations. Thus, we infer that the origin of self-fertility not only required mutations that activated the spermatogenesis program in XX germ lines, but prior to these there must have been mutations that decanalized the sex determination process, allowing for subsequent changes to germ cell fates. 
    more » « less
  5. ABSTRACT Sex‐specific trait expression represents a striking dimension of morphological variation within and across species. The mechanisms instructing sex‐specific organ development have been well studied in a small number of insect model systems, suggesting striking conservation in some parts of the somatic sex determination pathway while hinting at possible evolutionary lability in others. However, further resolution of this phenomenon necessitates additional taxon sampling, particularly in groups in which sexual dimorphisms have undergone significant elaboration and diversification. Here, we functionally investigate the somatic sex determination pathway in the gazelle dung beetleDigitonthophagus gazella, an emerging model system in the study of the development and evolution of sexual dimorphisms. We find that RNA interference (RNAi) targetingtransformer (tra)caused chromosomal females to develop morphological traits largely indistinguishable from those normally only observed in males, and thattraRNAiis sufficient to induce splicing of the normally male‐specific isoform ofdoublesexin chromosomal females, while leaving males unaffected. Further,intersexRNAiwas found to phenocopy previously described RNAi phenotypes ofdoublesexin female but not male beetles. These findings match predictions derived from models of the sex determination cascade as developed largely through studies inDrosophila melanogaster. In contrast, efforts to targettransformer2via RNAi resulted in high juvenile mortality but did not appear to affectdoublesexsplicing, whereas RNAi targetingSex‐lethaland two putative orthologs ofhermaphroditeyielded no obvious phenotypic modifications in either males or females, raising the possibility that the function of a subset of sex determination genes may be derived in select Diptera and thus nonrepresentative of their roles in other holometabolous orders. Our results help illuminate how the differential evolutionary lability of the somatic sex determination pathway has contributed to the extraordinary morphological diversification of sex‐specific trait expression found in nature. 
    more » « less