Regulatory Role of Retinoic Acid in Male Pregnancy of the Seahorse

Li, Chunyan; Li, Yongxin; Qin, Geng; Chen, Zelin; Qu, Meng; Zhang, Bo; Han, Xue; Wang, Xin; Qian, Pei‐Yuan; Lin, Qiang

doi:10.1016/j.xinn.2020.100052

Cited by 14 publications

(10 citation statements)

References 61 publications

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“…Male immune capabilities are higher than in female syngnathids but have been shown to come at a cost during pregnancy (Lin et al, 2016; Roth et al, 2011). Immune system states of pouch bearing syngnathids fluctuate owing to the shifting foeto‐paternal demands, and a consensus is growing that immune modulation is present and necessary (Keller & Roth, 2020; Li et al, 2020; Roth et al, 2020; Whittington et al, 2015). These observations are extended here in all pouched species, with many adaptive immune genes charged with tasks in antigen presentation and processing, showing a downregulation predominantly during early gestation (Table ).…”

Section: Discussionmentioning

confidence: 99%

Immunological tolerance in the evolution of male pregnancy

et al. 2022

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Pregnancy encompasses zygote implantation, embryonic retention, growth, and ends with the release of offspring at parturition. Viviparity has evolved independently more than 150 times across vertebrate species, with phylogenetic studies supporting the notion that gestation holds oviparous roots (Blackburn, 2015;Dudley et al., 2021). A culmination of morphological and physiological innovations that provide progeny with nutrient support, gas exchange and osmoregulation have evolved to shape this

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Section: Discussionmentioning

confidence: 99%

Immunological tolerance in the evolution of male pregnancy

et al. 2022

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“…They are considered to be “masters of camouflage” as they can deceive predators by changing their color pattern to resemble and blend with kelp and other seaweed. Like other syngnathids, seadragons have specialized morphological traits such as a tube-like toothless mouth, the absence of pelvic fins and scales, a bony armor covering the body, and “male pregnancy.” Males of all syngnathids incubate the fertilized eggs on a specialized incubation area, and in the modern lineages, even in enclosed brood pouches, making them prime examples for sex-role reversal ( 1 – 3 ). On the basis of the position of the brood pouch, syngnathids have been divided into tail-brooders (subfamily Syngnathinae represented by seahorses, some pipefishes and seadragons) and trunk-brooders (subfamily Nerophinae represented by Manado pipefish) ( 4 , 5 ).…”

Section: Introductionmentioning

confidence: 99%

Seadragon genome analysis provides insights into its phenotype and sex determination locus

Liu

Zhang

et al. 2021

Sci. Adv.

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The iconic phenotype of seadragons includes leaf-like appendages, a toothless tubular mouth, and male pregnancy involving incubation of fertilized eggs on an open “brood patch.” We de novo–sequenced male and female genomes of the common seadragon (Phyllopteryx taeniolatus) and its closely related species, the alligator pipefish (Syngnathoides biaculeatus). Transcription profiles from an evolutionary novelty, the leaf-like appendages, show that a set of genes typically involved in fin development have been co-opted as well as an enrichment of transcripts for potential tissue repair and immune defense genes. The zebrafish mutants for scpp5, which is lost in all syngnathids, were found to lack or have deformed pharyngeal teeth, supporting the hypothesis that the loss of scpp5 has contributed to the loss of teeth in syngnathids. A putative sex–determining locus encoding a male-specific amhr2y gene shared by common seadragon and alligator pipefish was identified.

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“…Viviparity has an independent origin and appears more than 150 times in vertebrates, while male pregnancy only emerges once in Syngnathidae fishes (4). Seahorses, the iconic species in the Syngnathid family with typical male pregnancy, have males with closed sophisticated brood pouch that act as the uterus during pregnancy, which provide protection, osmoregulation, gas exchange, and nutrition to the embryos (5,6). The brood pouch of male seahorse undergoes remodeling and even develop placenta during pregnancy (5,7).…”

Section: Introductionmentioning

confidence: 99%

Hepcidin Gene Co-Option Balancing Paternal Immune Protection and Male Pregnancy

et al. 2022

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Viviparity has originated independently more than 150 times in vertebrates, while the male pregnancy only emerged in Syngnathidae fishes, such as seahorses. The typical male pregnancy seahorses have closed sophisticated brood pouch that act as both uterus and placenta, representing an excellent model system for studying the evolutionary process of paternal immune protection. Phylogenetic analysis indicated that the hampII gene family has multiple tandem duplicated genes and shows independent lineage-specific expansion in seahorses, and they had the highest ratio of nonsynonymous substitutions to synonymous substitutions (dN/dS) in the seahorse phylogenetic branch. The expression levels of hampIIs in the brood pouch placenta were significantly higher during pregnancy than non-pregnancy. Both LPS stimulation test in vivo and cytotoxicity test in vitro proved the immunological protection function of hampIIs against pathogen infection in seahorse. Besides, seahorse hampII peptides exhibit weaker antibacterial function, but stronger agglutination and free endotoxin inhibition. We assumed that the modified immunological function seemed to be a trade-off between the resistance to microbial attack and offspring protection. In brief, this study suggests that the rapid co-option of hampIIs contributes to the evolutionary adaption to paternal immune care during male pregnancy.

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Regulatory Role of Retinoic Acid in Male Pregnancy of the Seahorse

Cited by 14 publications

References 61 publications

Immunological tolerance in the evolution of male pregnancy

Immunological tolerance in the evolution of male pregnancy

Seadragon genome analysis provides insights into its phenotype and sex determination locus

Hepcidin Gene Co-Option Balancing Paternal Immune Protection and Male Pregnancy

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