Fish reproduction in a warming world: vulnerable points in hormone regulation from sex determination to spawning.

Reproduction in fishes is sensitive to temperature. Elevated temperatures and anomalous 'heat waves' associated with climate change have the potential to impact fish reproductive performance and, in some cases, even induce sex reversals. Here we examine how thermal sensitivity in the hormone pathways regulating reproduction provides a framework for understanding impacts of warmer conditions on fish reproduction. Such effects will differ depending on evolved variation in temperature sensitivity of endocrine pathways regulating reproductive processes of sex determination/differentiation, gametogenesis and spawning, as well as how developmental timing of those processes varies with reproductive ecology. For fish populations unable to shift geographical range, persistence under future climates may require changes in temperature responsiveness of the hormone pathways regulating reproductive processes. How thermal sensitivity in those hormone pathways varies among populations and species, how those pathways generate temperature maxima for reproduction, and how rapidly reproductive thermal tolerances can change via adaptation or transgenerational plasticity will shape which fishes are most at risk for impaired reproduction under rising temperatures. This article is part of the theme issue 'Endocrine responses to environmental variation: conceptual approaches and recent developments'.

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

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, 3ß-hydroxysteroid dehydrogenase, and 17ß-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.