Prolactin and the evolution of male pregnancy

Wilson, Anthony B.; Whittington, Camilla M.; Meyer, Axel; Scobell, Sunny K.; Gauthier, Marie-Emilie

doi:10.1016/j.ygcen.2023.114210

Cited by 4 publications

(5 citation statements)

References 55 publications

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“…This result provides evidence of the existence of nurse eggs, and these impaired embryos are likely to be broken-down nurse eggs (Ripley and Foran, 2006). As for the cause of embryo breakage, it may be related to the release of some substances (e.g., prolactin and growth hormone) by the male into the pouch after mating, which causes enzymatic breakdown of a small portion of embryos (Carcupino et al, 2002;Patron et al, 2008;Wilson et al, 2023). In addition, in Experiment 2, we also found that the deposition of sperm and eggs was not synchronous, but rather, the sperm lagged behind the eggs.…”

Section: Discussionmentioning

confidence: 97%

Brooding fathers actively consume viable embryos to take up nutrients in a monogamous syngnathid fish

Lin,

Liu,

et al. 2024

Front. Mar. Sci.

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Syngnathid fishes often experience a reduction in brood size and an increase in immunity during pregnancy. Researchers have studied the polygamous broad-nosed pipefish (Syngnathus typhle) and revealed that some eggs from low-quality females in the male’s brood pouch serve as nurse eggs that are absorbed by the father. It is unclear whether nurse eggs also exist in other syngnathid fishes, especially in monogamous syngnathid fishes. In monogamous syngnathid fishes, the male pouch only carries eggs from a single female. Thus, the question remains: do some eggs of monogamous syngnathid fishes also serve as nurse eggs? And if so, are these nurse eggs impaired eggs, or are they viable eggs that are consumed by the brooding father? In the present study, we used the monogamous lined seahorse (Hippocampus erectus) and asked whether nurse eggs exist in this species. We also explored whether nurse eggs potentially originate from viable versus inviable eggs. Using isotope labeling, we found that nutrients from embryos could be transferred to brooding fathers. Furthermore, we also found that brooding fathers with limited food had a higher isotope content and a smaller brood size compared to individuals with sufficient food. These results have demonstrated that nurse eggs exist in the lined seahorse, and also suggested that the brooding fathers actively consume viable embryos to absorb nutrients in response to low food availability. These findings help us better understand parent–embryo conflict, filial cannibalism, and male-only care in teleost fishes.

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Section: Discussionmentioning

confidence: 97%

Brooding fathers actively consume viable embryos to take up nutrients in a monogamous syngnathid fish

Lin,

Liu,

et al. 2024

Front. Mar. Sci.

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“…Previous studies postulate that PRL and PRLR are associated with growth in Scophthalmus maximus [117]. In Hippocampus abdominalis, the accumulation of PRL in the brood pouch reduces early embryonic mortality by regulating Na + /K + -ATPase and reducing Na + /K + concentration [118]. Additionally, PRL enhances lymphocyte proliferation and inhibits cortisol-induced proliferation and apoptosis in rainbow trout [119].…”

Section: Genes Associated With Growth Development and Reproductionmentioning

confidence: 90%

Whole-Genome Sequencing Analyses Reveal the Evolution Mechanisms of Typical Biological Features of Decapterus maruadsi

Deng,

Li,

Shuai

et al. 2024

Animals

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Decapterus maruadsi is a typical representative of small pelagic fish characterized by fast growth rate, small body size, and high fecundity. It is a high-quality marine commercial fish with high nutritional value. However, the underlying genetics and genomics research focused on D. maruadsi is not comprehensive. Herein, a high-quality chromosome-level genome of a male D. maruadsi was assembled. The assembled genome length was 716.13 Mb with contig N50 of 19.70 Mb. Notably, we successfully anchored 95.73% contig sequences into 23 chromosomes with a total length of 685.54 Mb and a scaffold N50 of 30.77 Mb. A total of 22,716 protein-coding genes, 274.90 Mb repeat sequences, and 10,060 ncRNAs were predicted, among which 22,037 (97%) genes were successfully functionally annotated. The comparative genome analysis identified 459 unique, 73 expanded, and 52 contracted gene families. Moreover, 2804 genes were identified as candidates for positive selection, of which some that were related to the growth and development of bone, muscle, cardioid, and ovaries, such as some members of the TGF-β superfamily, were likely involved in the evolution of typical biological features in D. maruadsi. The study provides an accurate and complete chromosome-level reference genome for further genetic conservation, genomic-assisted breeding, and adaptive evolution research for D. maruadsi.

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“…This contrasts with other teleost fishes, which express PRL1 also outside of the pituitary. PRLRa is expressed in the brood pouch and all other tissues and is specifically upregulated in the male brood pouch during the second half of pregnancy [33]. Immunostaining of brood pouch tissues showed that PRL1 protein and PRLRa are present in the pouch luminal epithelium.…”

Section: Prolactinmentioning

confidence: 97%

“…In mammals, the function of prolactin is extremely broad, from electrolyte homeostasis, metabolism, growth, brain function, and immunity to the regulation of gonadal cycling, mammary gland activity, uterine functions, embryo implantation, live birth (viviparity), and parental behavior [32]. Recently, Wilson et al [33] studied prolactin and its receptor expression in male pregnancy and analyzed how prolactin was evolutionarily co-opted to male pregnancy in Syngnathidae (big-belly seahorse Hippocampus abdominalis, greater pipefish Syngnathus acus, northern pipefish S. fuscus, and broad-nosed pipefish S. typhle). In contrast to many teleost fishes, which have multiple copies of PRL and PRLR, Syngnathidae have only a single copy (PRL1 and PRLRa) of each gene.…”

Section: Prolactinmentioning

confidence: 99%

“…Immunostaining of brood pouch tissues showed that PRL1 protein and PRLRa are present in the pouch luminal epithelium. Because the same epithelium also expressed the sodiumpotassium enzyme Na+/K+ ATPase, the authors concluded that pituitary-derived PRL1 and its receptor are involved in brood pouch osmoregulation during pregnancy [33]. Pre-vious transcriptome analysis of the seahorse brood pouch showed that Na+/K+-ATPase activity is high during the whole pregnancy [34].…”

Section: Prolactinmentioning

confidence: 99%

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Seahorse Male Pregnancy as a Model System to Study Pregnancy, Immune Adaptations, and Environmental Effects

Kloc

2023

IJMS

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Seahorses, together with sea dragons and pipefishes, belong to the Syngnathidae family of teleost fishes. Seahorses and other Syngnathidae species have a very peculiar feature: male pregnancy. Among different species, there is a gradation of paternal involvement in carrying for the offspring, from a simple attachment of the eggs to the skin surface, through various degrees of egg coverage by skin flaps, to the internal pregnancy within a brood pouch, which resembles mammalian uterus with the placenta. Because of the gradation of parental involvement and similarities to mammalian pregnancy, seahorses are a great model to study the evolution of pregnancy and the immunologic, metabolic, cellular, and molecular processes of pregnancy and embryo development. Seahorses are also very useful for studying the effects of pollutants and environmental changes on pregnancy, embryo development, and offspring fitness. We describe here the characteristics of seahorse male pregnancy, its regulatory mechanisms, the development of immune tolerance of the parent toward the allogeneic embryos, and the effects of environmental pollutants on pregnancy and embryo development.

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Prolactin and the evolution of male pregnancy

Cited by 4 publications

References 55 publications

Brooding fathers actively consume viable embryos to take up nutrients in a monogamous syngnathid fish

Brooding fathers actively consume viable embryos to take up nutrients in a monogamous syngnathid fish

Whole-Genome Sequencing Analyses Reveal the Evolution Mechanisms of Typical Biological Features of Decapterus maruadsi

Seahorse Male Pregnancy as a Model System to Study Pregnancy, Immune Adaptations, and Environmental Effects

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