Evolutionary Dynamics and Functional Conservation of <i>amh</i> Signaling in Teleost Lineages

The anti-Müllerian hormone (<i>amh</i>) and its receptor, <i>amhr2</i>, along with the downstream bone morphogenetic protein receptors (<i>bmpr</i>s), have been recognized as the central regulators in teleost sex determination (SD) and differentiation. However, th...

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Main Authors: Lingqun Zhang, Qingke Zhang, Kai Hu, Wei Lu, Weigang Li, Fengchi Wang, Jie Cheng
Format: Article
Language:English
Published: MDPI AG 2025-07-01
Series:Fishes
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Online Access:https://www.mdpi.com/2410-3888/10/7/327
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author Lingqun Zhang
Qingke Zhang
Kai Hu
Wei Lu
Weigang Li
Fengchi Wang
Jie Cheng
author_facet Lingqun Zhang
Qingke Zhang
Kai Hu
Wei Lu
Weigang Li
Fengchi Wang
Jie Cheng
author_sort Lingqun Zhang
collection DOAJ
description The anti-Müllerian hormone (<i>amh</i>) and its receptor, <i>amhr2</i>, along with the downstream bone morphogenetic protein receptors (<i>bmpr</i>s), have been recognized as the central regulators in teleost sex determination (SD) and differentiation. However, their evolution and function in reproduction among diverse teleost lineages may represent species-specific patterns and still need more explanation. In this study, systematic investigations of <i>amh</i> signaling genes, including <i>amh</i>, <i>amhy</i> (Y-linked paralog of <i>amh</i>), <i>amhr2</i>, <i>bmpr1</i>, and <i>bmpr2</i>, were conducted among teleost species. The results revealed generally conserved gene copy number, phylogeny, structure, and synteny, among teleost <i>amh</i> signaling genes. Notably, significantly accelerated evolutionary rates (dN/dS) were found in teleost <i>amhy</i> compared to <i>amh</i>, and <i>amh</i> exhibited faster molecular evolution in <i>amhy</i>-SD teleosts than in non-<i>amhy</i>-SD teleosts, suggesting their enhanced evolutionary plasticity in teleosts. Expression profiling identified testis-biased expression of the most <i>amh</i> signaling genes in fish species with different SD genes and mechanisms, including <i>Lateolabrax maculatus</i> and <i>Dicentrarchus labrax</i> from Order Perciformes, <i>Cynoglossus semilaevis</i> and <i>Paralichthys olivaceus</i> from Order Pleuronectiformes, and <i>Salmo salar</i> and <i>Oncorhynchus mykiss</i> from Order Salmoniformes, with ovary-biased expression also found in Salmoniformes. A weighted gene co-expression network analysis further uncovered strong species-specific functional interactions between <i>amh</i> signaling components and genes of germ-cell development, the meiotic process, etc. Collectively, the integrated evidence from this study supports the hypothesis that <i>amh</i> signaling provides the key molecules governing sex differentiation in a species-specific manner in diverse teleost lineages, independent of its SD role, and interacts with functions of both testis and ovary development.
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spelling doaj-art-2d4ece9bcd194945b19c9ae6369618ce2025-08-20T02:45:38ZengMDPI AGFishes2410-38882025-07-0110732710.3390/fishes10070327Evolutionary Dynamics and Functional Conservation of <i>amh</i> Signaling in Teleost LineagesLingqun Zhang0Qingke Zhang1Kai Hu2Wei Lu3Weigang Li4Fengchi Wang5Jie Cheng6MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaThe anti-Müllerian hormone (<i>amh</i>) and its receptor, <i>amhr2</i>, along with the downstream bone morphogenetic protein receptors (<i>bmpr</i>s), have been recognized as the central regulators in teleost sex determination (SD) and differentiation. However, their evolution and function in reproduction among diverse teleost lineages may represent species-specific patterns and still need more explanation. In this study, systematic investigations of <i>amh</i> signaling genes, including <i>amh</i>, <i>amhy</i> (Y-linked paralog of <i>amh</i>), <i>amhr2</i>, <i>bmpr1</i>, and <i>bmpr2</i>, were conducted among teleost species. The results revealed generally conserved gene copy number, phylogeny, structure, and synteny, among teleost <i>amh</i> signaling genes. Notably, significantly accelerated evolutionary rates (dN/dS) were found in teleost <i>amhy</i> compared to <i>amh</i>, and <i>amh</i> exhibited faster molecular evolution in <i>amhy</i>-SD teleosts than in non-<i>amhy</i>-SD teleosts, suggesting their enhanced evolutionary plasticity in teleosts. Expression profiling identified testis-biased expression of the most <i>amh</i> signaling genes in fish species with different SD genes and mechanisms, including <i>Lateolabrax maculatus</i> and <i>Dicentrarchus labrax</i> from Order Perciformes, <i>Cynoglossus semilaevis</i> and <i>Paralichthys olivaceus</i> from Order Pleuronectiformes, and <i>Salmo salar</i> and <i>Oncorhynchus mykiss</i> from Order Salmoniformes, with ovary-biased expression also found in Salmoniformes. A weighted gene co-expression network analysis further uncovered strong species-specific functional interactions between <i>amh</i> signaling components and genes of germ-cell development, the meiotic process, etc. Collectively, the integrated evidence from this study supports the hypothesis that <i>amh</i> signaling provides the key molecules governing sex differentiation in a species-specific manner in diverse teleost lineages, independent of its SD role, and interacts with functions of both testis and ovary development.https://www.mdpi.com/2410-3888/10/7/327<i>amh</i> signalingmolecular evolutionco-expression networksex differentiationteleost
spellingShingle Lingqun Zhang
Qingke Zhang
Kai Hu
Wei Lu
Weigang Li
Fengchi Wang
Jie Cheng
Evolutionary Dynamics and Functional Conservation of <i>amh</i> Signaling in Teleost Lineages
Fishes
<i>amh</i> signaling
molecular evolution
co-expression network
sex differentiation
teleost
title Evolutionary Dynamics and Functional Conservation of <i>amh</i> Signaling in Teleost Lineages
title_full Evolutionary Dynamics and Functional Conservation of <i>amh</i> Signaling in Teleost Lineages
title_fullStr Evolutionary Dynamics and Functional Conservation of <i>amh</i> Signaling in Teleost Lineages
title_full_unstemmed Evolutionary Dynamics and Functional Conservation of <i>amh</i> Signaling in Teleost Lineages
title_short Evolutionary Dynamics and Functional Conservation of <i>amh</i> Signaling in Teleost Lineages
title_sort evolutionary dynamics and functional conservation of i amh i signaling in teleost lineages
topic <i>amh</i> signaling
molecular evolution
co-expression network
sex differentiation
teleost
url https://www.mdpi.com/2410-3888/10/7/327
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AT qingkezhang evolutionarydynamicsandfunctionalconservationofiamhisignalinginteleostlineages
AT kaihu evolutionarydynamicsandfunctionalconservationofiamhisignalinginteleostlineages
AT weilu evolutionarydynamicsandfunctionalconservationofiamhisignalinginteleostlineages
AT weigangli evolutionarydynamicsandfunctionalconservationofiamhisignalinginteleostlineages
AT fengchiwang evolutionarydynamicsandfunctionalconservationofiamhisignalinginteleostlineages
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