Accustomed to the heat: Temperature and thyroid hormone influences on oogenesis and gonadal steroidogenesis pathways vary among populations of Amargosa pupfish (Cyprinodon nevadensis amargosae)

Sean C Lema; Michelle I Chow; Andrew H Dittman; Darran May; Madeline J Housh

doi:10.1016/j.cbpa.2022.111280

Accustomed to the heat: Temperature and thyroid hormone influences on oogenesis and gonadal steroidogenesis pathways vary among populations of Amargosa pupfish (Cyprinodon nevadensis amargosae)

Comp Biochem Physiol A Mol Integr Physiol. 2022 Oct:272:111280. doi: 10.1016/j.cbpa.2022.111280. Epub 2022 Jul 25.

Authors

Sean C Lema¹, Michelle I Chow², Andrew H Dittman³, Darran May⁴, Madeline J Housh²

Affiliations

¹ Biological Sciences Department, Center for Coastal Marine Sciences, California Polytechnic State University, San Luis Obispo, CA, USA. Electronic address: slema@calpoly.edu.
² Biological Sciences Department, Center for Coastal Marine Sciences, California Polytechnic State University, San Luis Obispo, CA, USA.
³ Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA, Seattle, WA, USA.
⁴ Aquatic and Fishery Sciences, University of Washington, Seattle, WA, USA.

PMID: 35902003
DOI: 10.1016/j.cbpa.2022.111280

Abstract

Many fish experience diminished reproductive performance under atypically high or prolonged elevations of temperature. Such high temperature inhibition of reproduction comes about in part from altered stimulation of gametogenesis by the hypothalamic-pituitary-gonadal (HPG) endocrine axis. Elevated temperatures have also been shown to affect thyroid hormone (TH) signaling, and altered TH status under high temperatures may impact gametogenesis via crosstalk with HPG axis pathways. Here, we examined effects of temperature and 3'-triiodo-_L-thyronine (T₃) on pathways for gonadal steroidogenesis and gametogenesis in Amargosa pupfish (Cyprinodon nevadensis amargosae) from two allopatric populations: 1) the Amargosa River - a highly variable temperature habitat, and 2) Tecopa Bore - an invariably warm groundwater-fed marsh. These populations were previously shown to differ in TH signaling profiles both in the wild and under common laboratory conditions. Sexually-mature pupfish from each population were maintained at 24 °C or 34 °C for 88 days, after which a subset of fish was treated with T₃ for 18-24 h. In both populations, mRNA abundances for follicle-stimulating hormone receptor and luteinizing hormone receptor were higher in the ovary and testis at 24 °C compared to 34 °C. Females from Tecopa Bore - but not from the Amargosa River - also had greater ovarian transcript abundances for steroidogenic enzymes cytochrome P450 aromatase, 3β-hydroxysteroid dehydrogenase, and 17β-hydroxysteroid dehydrogenase at 24 °C compared to 34 °C, as well as higher liver mRNA levels of vitellogenins and choriogenins at cooler temperature. Transcript abundances for estrogen receptors esr1, esr2a, and esr2b were reduced at 34 °C in Amargosa River females, but not in Tecopa Bore females. T₃ augmented gonadal gene transcript levels for steroid acute regulatory protein (StAR) transporter in both sexes and populations. T₃ also downregulated liver estrogen receptor mRNAs in females from the warmer Tecopa Bore habitat only, suggesting T₃ modulation of liver E₂ sensitivity as a possible mechanism whereby temperature-induced changes in TH status may contribute to shifts in thermal sensitivity for oogenesis.

Keywords: Climate change; Estrogen receptor; Evolution; Fish; Reproduction; Temperature.

Publication types

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

MeSH terms

Animals
Female
Fishes / metabolism
Hot Temperature
Killifishes* / metabolism
Male
Oogenesis
RNA, Messenger / genetics
Temperature
Thyroid Hormones

Substances

RNA, Messenger
Thyroid Hormones