A Transient Hermaphroditic Stage in Early Male Gonadal Development in Little Yellow Croaker, Larimichthys polyactis
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...
Main Authors: | , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2021-01-01
|
Series: | Frontiers in Endocrinology |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/fendo.2020.542942/full |
id |
doaj-4209012569b843169ec0ad4c16d73e1e |
---|---|
record_format |
Article |
spelling |
doaj-4209012569b843169ec0ad4c16d73e1e2021-01-27T09:03:21ZengFrontiers Media S.A.Frontiers in Endocrinology1664-23922021-01-011110.3389/fendo.2020.542942542942A Transient Hermaphroditic Stage in Early Male Gonadal Development in Little Yellow Croaker, Larimichthys polyactisQing-Ping Xie0Qing-Ping Xie1Bing-Bing Li2Wei Zhan3Feng Liu4Peng Tan5Xu Wang6Xu Wang7Xu Wang8Bao Lou9Institute of Hydrobiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaMarine Fisheries Research Institute of Zhejiang Province, Zhoushan, ChinaSchool of Fishery, Zhejiang Ocean University, Zhoushan, ChinaInstitute of Hydrobiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaInstitute of Hydrobiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaMarine Fisheries Research Institute of Zhejiang Province, Zhoushan, ChinaDepartment of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL, United StatesAlabama Agricultural Experiment Station, Auburn, AL, United StatesThe HudsonAlpha Institute for Biotechnology, Huntsville, AL, United StatesInstitute of Hydrobiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaAnimal 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.https://www.frontiersin.org/articles/10.3389/fendo.2020.542942/fullhermaphroditesex differentiationhermaphroditismgonochorismintersex gonadal stage |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Qing-Ping Xie Qing-Ping Xie Bing-Bing Li Wei Zhan Feng Liu Peng Tan Xu Wang Xu Wang Xu Wang Bao Lou |
spellingShingle |
Qing-Ping Xie Qing-Ping Xie Bing-Bing Li Wei Zhan Feng Liu Peng Tan Xu Wang Xu Wang Xu Wang Bao Lou A Transient Hermaphroditic Stage in Early Male Gonadal Development in Little Yellow Croaker, Larimichthys polyactis Frontiers in Endocrinology hermaphrodite sex differentiation hermaphroditism gonochorism intersex gonadal stage |
author_facet |
Qing-Ping Xie Qing-Ping Xie Bing-Bing Li Wei Zhan Feng Liu Peng Tan Xu Wang Xu Wang Xu Wang Bao Lou |
author_sort |
Qing-Ping Xie |
title |
A Transient Hermaphroditic Stage in Early Male Gonadal Development in Little Yellow Croaker, Larimichthys polyactis |
title_short |
A Transient Hermaphroditic Stage in Early Male Gonadal Development in Little Yellow Croaker, Larimichthys polyactis |
title_full |
A Transient Hermaphroditic Stage in Early Male Gonadal Development in Little Yellow Croaker, Larimichthys polyactis |
title_fullStr |
A Transient Hermaphroditic Stage in Early Male Gonadal Development in Little Yellow Croaker, Larimichthys polyactis |
title_full_unstemmed |
A Transient Hermaphroditic Stage in Early Male Gonadal Development in Little Yellow Croaker, Larimichthys polyactis |
title_sort |
transient hermaphroditic stage in early male gonadal development in little yellow croaker, larimichthys polyactis |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Endocrinology |
issn |
1664-2392 |
publishDate |
2021-01-01 |
description |
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. |
topic |
hermaphrodite sex differentiation hermaphroditism gonochorism intersex gonadal stage |
url |
https://www.frontiersin.org/articles/10.3389/fendo.2020.542942/full |
work_keys_str_mv |
AT qingpingxie atransienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT qingpingxie atransienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT bingbingli atransienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT weizhan atransienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT fengliu atransienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT pengtan atransienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT xuwang atransienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT xuwang atransienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT xuwang atransienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT baolou atransienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT qingpingxie transienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT qingpingxie transienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT bingbingli transienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT weizhan transienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT fengliu transienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT pengtan transienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT xuwang transienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT xuwang transienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT xuwang transienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis AT baolou transienthermaphroditicstageinearlymalegonadaldevelopmentinlittleyellowcroakerlarimichthyspolyactis |
_version_ |
1724321707980750848 |