Prolactin and the evolution of male pregnancy

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

doi:10.1016/j.ygcen.2023.114210

Prolactin and the evolution of male pregnancy

Gen Comp Endocrinol. 2023 Apr 1:334:114210. doi: 10.1016/j.ygcen.2023.114210. Epub 2023 Jan 13.

Authors

Anthony B Wilson¹, Camilla M Whittington², Axel Meyer³, Sunny K Scobell⁴, Marie-Emilie Gauthier⁵

Affiliations

¹ Department of Biology, Brooklyn College, 2900 Bedford Avenue, Brooklyn, NY 11210, United States; The Graduate Center, City University of New York, 365 Fifth Avenue, New York, NY 10016, United States; Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich 8057, Switzerland; Department of Biology, University of Konstanz, Universitätsstrasse 10, 78457, Germany. Electronic address: twilson@brooklyn.cuny.edu.
² Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich 8057, Switzerland; Sydney School of Veterinary Science, University of Sydney, Sydney 2006, Australia; School of Life and Environmental Sciences, University of Sydney, Sydney 2006, Australia.
³ Department of Biology, University of Konstanz, Universitätsstrasse 10, 78457, Germany.
⁴ Department of Biology, Brooklyn College, 2900 Bedford Avenue, Brooklyn, NY 11210, United States.
⁵ Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich 8057, Switzerland.

PMID: 36646326
DOI: 10.1016/j.ygcen.2023.114210

Abstract

Prolactin (PRL) is a multifunctional hormone of broad physiological importance, and is involved in many aspects of fish reproduction, including the regulation of live birth (viviparity) and both male and female parental care. Previous research suggests that PRL also plays an important reproductive role in syngnathid fishes (seahorses, pipefish and seadragons), a group with a highly derived reproductive strategy, male pregnancy - how the PRL axis has come to be co-opted for male pregnancy remains unclear. We investigated the molecular evolution and expression of the genes for prolactin and its receptor (PRLR) in an evolutionarily diverse sampling of syngnathid fishes to explore how the co-option of PRL for male pregnancy has impacted its evolution, and to clarify whether the PRL axis is also involved in regulating reproductive function in species with more rudimentary forms of male pregnancy. In contrast to the majority of teleost fishes, all syngnathid fishes tested carry single copies of PRL and PRLR that cluster genetically within the PRL1 and PRLRa lineages of teleosts, respectively. PRL1 gene expression in seahorses and pipefish is restricted to the pituitary, while PRLRa is expressed in all tissues, including the brood pouch of species with both rudimentary and complex brooding structures. Pituitary PRL1 expression remains stable throughout pregnancy, but PRLRa expression is specifically upregulated in the male brood pouch during pregnancy, consistent with the higher affinity of pouch tissues for PRL hormone during embryonic incubation. Finally, immunohistochemistry of brood pouch tissues reveals that both PRL1 protein and PRLRa and Na⁺/K⁺ ATPase-positive cells line the inner pouch epithelium, suggesting that pituitary-derived PRL1 may be involved in brood pouch osmoregulation during pregnancy. Our data provide a unique molecular perspective on the evolution and expression of prolactin and its receptor during male pregnancy, and provide the foundation for further manipulative experiments exploring the role of PRL in this unique form of reproduction.

Keywords: Pipefish; Reproduction; Seahorse; Syngnathid evolution; Teleost fish; Viviparity.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Female
Fishes / metabolism
Male
Prolactin* / genetics
Prolactin* / metabolism
Receptors, Prolactin / genetics
Reproduction / genetics
Smegmamorpha* / genetics

Substances

Prolactin
Receptors, Prolactin