Immunogenetic losses co-occurred with seahorse male pregnancy and mutation in tlx1 accompanied functional asplenia

Nature Communications, Journal Year: 2022, Volume and Issue: 13(1)

Published: Dec. 9, 2022

In the highly derived syngnathid fishes (pipefishes, seadragons & seahorses), evolution of sex-role reversed brooding behavior culminated in seahorse lineage's male pregnancy, whose males feature a specialized brood pouch into which females deposit eggs during mating. Then, are intimately engulfed by placenta-like tissue that facilitates gas and nutrient exchange. As fathers immunologically tolerate allogenic embryos, it was suggested pregnancy co-evolved with specific immunological adaptations. Indeed, here we show amino-acid replacement tlx1 transcription factor is associated seahorses' asplenia (loss spleen, an organ central immune system), as confirmed CRISPR-Cas9 experiment using zebrafish. Comparative genomics across phylogeny revealed complexity system gene repertoire decreases parental care intensity increases. The synchronous immunogenetic alterations supports notion tolerance embryo.

Language: Английский

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Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta

Molecular Biology and Evolution, Journal Year: 2022, Volume and Issue: 39(4)

Published: April 1, 2022

Abstract The repeated evolution of the same traits in distantly related groups (convergent evolution) raises a key question evolutionary biology: do genes underpin convergent phenotypes? Here, we explore one such trait, viviparity (live birth), which, qualitative studies suggest, may indeed have evolved via genetic convergence. There are >150 independent origins live birth vertebrates, providing uniquely powerful system to test mechanisms underpinning convergence morphology, physiology, and/or gene recruitment during pregnancy. We compared transcriptomic data from eight vertebrates (lizards, mammals, sharks) that gestate embryos within uterus. Since many previous detected similarities use pregnancy, expected find significant overlap viviparous taxa. However, found no more uterine expression associated with than would expect by chance alone. Each lineage exhibits core set physiological functions. Yet, contrary prevailing assumptions about this none differentially expressed all lineages, or even amniote lineages. Therefore, across different been recruited support morphological and changes required for successful conclude redundancies function enabled through genomic “toolboxes”, which constrained ancestries each lineage.

Language: Английский

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Navigating sex and sex roles: deciphering sex-biased gene expression in a species with sex-role reversal ( Syngnathus typhle )

Royal Society Open Science, Journal Year: 2024, Volume and Issue: 11(4)

Published: April 1, 2024

Sexual dimorphism, the divergence in morphological traits between males and females of same species, is often accompanied by sex-biased gene expression. However, majority research has focused on species with conventional sex roles, where have highest energy burden both egg production parental care, neglecting diversity reproductive roles found nature. We investigated expression

Language: Английский

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Single-cell sequencing provides clues about the developmental genetic basis of evolutionary adaptations in syngnathid fishes

eLife, Journal Year: 2025, Volume and Issue: 13

Published: Feb. 3, 2025

Seahorses, pipefishes, and seadragons are fishes from the family Syngnathidae that have evolved extraordinary traits including male pregnancy, elongated snouts, loss of teeth, dermal bony armor. The developmental genetic cellular changes led to evolution these largely unknown. Recent syngnathid genome assemblies revealed suggestive gene content differences provided opportunity for detailed analyses. We created a single-cell RNA sequencing atlas Gulf pipefish embryos understand basis four traits: derived head shape, toothlessness, armor, pregnancy. completed marker analyses, built networks, examined spatial expression select genes. identified osteochondrogenic mesenchymal cells in elongating face express regulatory genes bmp4, sfrp1a , prdm16 . found no evidence tooth primordia cells, we observed re-deployment osteoblast networks developing Finally, epidermal expressed nutrient processing environmental sensing genes, potentially relevant brooding environment. evolutionary innovations composed recognizable cell types, suggesting features originate within existing networks. Future work addressing across multiple stages species is essential understanding how novelties fish evolved.

Language: Английский

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Brood pouch evolution in pipefish and seahorse based on histological observation

Placenta, Journal Year: 2022, Volume and Issue: 120, P. 88 - 96

Published: Feb. 23, 2022

Language: Английский

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Embryonic specializations for vertebrate placentation

Philosophical Transactions of the Royal Society B Biological Sciences, Journal Year: 2022, Volume and Issue: 377(1865)

Published: Oct. 17, 2022

The vertebrate placenta, a close association of fetal and parental tissue for physiological exchange, has evolved independently in sharks, teleost fishes, coelacanths, amphibians, squamate reptiles mammals. This transient organ forms during pregnancy is an important contributor to embryonic development both viviparous oviparous, brooding species. Placentae may be involved transport respiratory gases, wastes, immune molecules, hormones nutrients. Depending on the taxon, portion placenta comprised either extraembryonic membranes (yolk sac or chorioallantois) temporary tissues derived via hypertrophy pericardium, gill epithelium, gut, tails fins. These have been recruited convergently into placentae several lineages. Here, we highlight diversity common features placentation suggest future studies that will provide new knowledge about evolution pregnancy. article part theme issue ‘Extraembryonic tissues: exploring concepts, definitions functions across animal kingdom’.

Language: Английский

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Immunological tolerance in the evolution of male pregnancy

Molecular Ecology, Journal Year: 2021, Volume and Issue: 32(4), P. 819 - 840

Published: Dec. 24, 2021

The unique male pregnancy in pipefishes and seahorses ranges from basic attachment (pouch-less species: Nerophinae) of maternal eggs to specialized internal gestation pouched species (e.g. Syngnathus Hippocampus) with many transitions between. Due this diversity, offers a platform for assessing physiological molecular adaptations evolution. These insights will contribute answering long-standing questions why how evolved convergently so vertebrate systems. To understand the congruencies disparities evolution, we compared transcriptome-wide differentially expressed genes four syngnathid species, at stages (nonpregnant, early, late parturition). Across all forms, metabolic processes immune dynamics defined stages, especially shared expression features akin female pregnancy. observed downregulation adaptive early-stage its reversed upregulation during late/parturition most notably Hippocampus, combined directionless pouch-less suggests modulation be restricted that placenta-like We propose increased foeto-paternal intimacy syngnathids commands suppression early gestation, elevated response parturition coincides pouch opening reduced progeny reliance. Immune regulation supports recently described functional MHC II pathway loss as critical independent co-option similar pathways both highlights crucial evolutionary establishment

Language: Английский

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Development of gonad and brood pouch and expression profiles of cgα, fshβ and lhβ transcripts and plasma 17β-E2 and 11-KT during the first reproductive cycle of farmed big-belly seahorse (Hippocampus abdominalis)

Aquaculture, Journal Year: 2024, Volume and Issue: 589, P. 740986 - 740986

Published: April 23, 2024

Language: Английский

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Genome rearrangements, male pregnancy and immunological tolerance – the curious case of the syngnathid immune system

Frontiers in Marine Science, Journal Year: 2023, Volume and Issue: 10

Published: Jan. 26, 2023

The syngnathid fish group (seahorses, pipefishes and seadragons) is a fascinating lineage associated with an array of evolutionary peculiarities that include diverse morphologies their unique male pregnancy. These oddities also extend to immune systems, growing body research highlighting range intriguing immunological characteristics genomic rearrangements, which pose questions regarding history strategies. functional loss the major histocompatibility complex class II pathway (MHC II) in Syngnathus genus related components seahorse ( Hippocampus ) were two discoveries initially piqued interest. This sparked discussions concerning capabilities, possible facilitative roles advanced pregnancy evolution through means evoking tolerance, as well general re-evaluation how we interpret vertebrate plasticity. Experimental approaches have attempted clarify further impact repertoire on efficacy response, specificities pathways play during concept inheritance. first characterization cell typhle using scRNA-seq represents latest step understanding dynamics these enigmatic fish. report serves review for insights into group; encompassing history, populations, links pregnancy, sex specificity, addition future opportunities need investigation.

Language: Английский

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Single Cell RNA Sequencing Provides Clues for the Developmental Genetic Basis of Syngnathidae’s Evolutionary Adaptations

Published: June 5, 2024

Seahorses, pipefishes, and seadragons are fishes from the family Syngnathidae that have evolved extraordinary traits including male pregnancy, elongated snouts, loss of teeth, dermal bony armor. The developmental genetic cellular changes led to evolution these largely unknown. Recent syngnathid genomes revealed suggestive gene content differences provide opportunity for detailed analyses. We created a single cell RNA sequencing atlas Gulf pipefish embryos understand basis four traits: derived head shape, toothlessness, armor, pregnancy. completed marker analyses, built networks, examined spatial expression select genes. identified osteochondrogenic mesenchymal cells in elongating face express regulatory genes bmp4, sfrp1a , prdm16 . found no evidence tooth primordia cells, we observed re-deployment osteoblast networks developing armor.Finally, epidermal expressed nutrient processing environmental sensing genes, potentially relevant brooding environment. evolutionary innovations composed recognizable types, suggesting features originate within existing networks. Future work addressing across multiple stages species is essential understanding how their novelties evolved.

Language: Английский

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