The evolution of endocrine function; discovering the hormonal control of osmoregulation in basal vertebrates

The neuroendocrine system is the major mechanism through which changes in the environment are detected and transduced into a coordinated physiological response. Our current understanding of the hormonal control of osmoregulation in aquatic vertebrates comes almost entirely from work on advanced teleosts, in which prolactin (PRL) promotes osmoregulation in freshwater (FW) and growth hormone (GH) promotes osmoregulation in seawater (SW). Lamprey are basal vertebrates and sturgeon are basal bony fishes that share the same osmoregulatory strategy as teleosts and present a unique opportunity to examine the early evolution of the pituitary control of osmoregulation, which to date has been largely unexamined.

Simplified vertebrate lineage depicting the evolution of hormones associated with osmoregulation.

Osmoregulatory capacity, and prolactin and growth hormone control over osmoregulation in the vertebrate lineage. Image credit: Stephen McCormick

Our specific aims in this project are to 1) Determine the response of GH and GH receptor to salinity change in lamprey, 2) Determine the osmoregulatory actions of GH in lamprey, and 3) Determine the osmoregulatory roles of GH and PRL in sturgeon. We hypothesize that GH is a SW-acclimating hormone in sea lamprey and that distinct functions of FW acclimation by PRL, and SW-acclimation by GH, will be found in Atlantic sturgeon. By determining for the first time the osmoregulatory function of prolactin and growth hormone in the more basal extant vertebrates, this project will have profound implications for our understanding of endocrinology among all vertebrates including humans. We expect our results to provide evidence of the earliest function of prolactin and growth hormone that can contribute to the revision of physiology and endocrinology textbooks. The results will also have application to the aquaculture and conservation of endangered sturgeon populations and the management of invasive lamprey.

Publications

Shaughnessy CA, Myhre V, Hall DJ, McCormick SD, Dores RM. 2023. Hypothalamus-pituitary-interrenal (HPI) axis signaling in Atlantic sturgeon (Acipenser oxyrinchus) and sterlet (Acipenser ruthenus). Gen Comp Endo 339:114290.

Ferreira-Martins D, Walton E, Karlstrom RO, Sheridan MA, McCormick SD. 2023. The GH/IGF axis in the sea lamprey during metamorphosis and seawater acclimation. Mol Cell Endocrinol 571:111937.

Gong N, Ferreira-Martins D, Norstog JL, McCormick SD, Sheridan MA. Discovery of prolactin-like in lamprey: Role in osmoregulation and new insight into the evolution of the growth hormone/prolactin family. Proc. Natl. Acad. Sci. U.S.A. 119:e2212196119.

Shaughnessy CA, McCormick SD. 2021. 11-Deoxycortisol is a stress responsive and gluconeogenic hormone in a jawless vertebrate, the sea lamprey (Petromyzon marinus). J Exp Biol 224:jeb241943.

*Barany A, *Shaughnessy CA, McCormick SD. 2021. Corticosteroid control of Na+/K+-ATPase in the intestine of the sea lamprey (Petromyzon marinus). Gen Comp Endo 307:113756.

Gong N, Ferreira-Martins D, McCormick SD, Sheridan MA. 2020. Divergent genes encoding the putative receptors for growth hormone and prolactin in sea lamprey display distinct patterns of expression. Sci Rep 10:1674.

Shaughnessy CA, Barany A, McCormick SD. 2020. 11-Deoxycortisol controls hydromineral balance in the most basal osmoregulating vertebrate, sea lamprey (Petromyzon marinus). Sci Rep 10:12148.

Investigators:

Stephen McCormick, USGS Conte Anadromous Fish Research Center, Turners Falls, MA, USA and Departments of Biology and Environmental Conservation, University of Massachusetts, Amherst, MA, USA. mccormick@umext.umass.edu

Diogo Ferreira-Martins, Researcher, CIIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Portugal. dmartins@ciimar.up.pt

Ciaran Shaughnessy, Assistant Professor of Integrative Physiology, Department of Integrative Biology, Oklahoma State University, Stillwater, OK, USA. ciaran.shaughnessy@okstate.edu

Mark A. Sheridan, Professor, Department of Biological Sciences, Texas Tech University, Lubbock, TX, USA. mark.sheridan@ttu.edu

Ningping Gong, Researcher, Texas Tech University, Lubbock, TX, USA. ningping.gong@ttu.edu

Supported by the National Science Foundation