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.

Endocrine and metabolic impacts of warming aquatic habitats: differential responses between recently isolated populations of a eurythermal desert pupfish.

Temperatures of inland aquatic habitats are increasing with climate change, and understanding how fishes respond physiologically to thermal stress will be crucial for identifying species most susceptible to these changes. Desert fishes may be particularly vulnerable to rising temperatures because many species occupy only a fraction of their historical range and occur in habitats with already high temperatures. Here, we examined endocrine and metabolic responses to elevated temperature in Amargosa pupfish, Cyprinodon nevadensis amargosae. We studied C. n. amargosae from two habitats with distinct thermal conditions: the Amargosa River, which experiences diurnally and seasonally variable temperatures (0.2-40°C); and Tecopa Bore, a spring and marsh fed by hot groundwater (47.5°C) from an artesian borehole. These allopatric populations differ in morphology, and prior evidence suggests that temperature might contribute to these differences via altered thyroid hormone (TH) regulation of morphological development. Here, we document variation in hepatic iodothyronine deiodinase type 2 (dio2) and type 3 (dio3) and TH receptor ß (trß) gene transcript abundance between the Amargosa River and Tecopa Bore wild populations. Fish from these populations acclimated to 24 or 34°C retained differences in hepatic dio2, dio3 and trß mRNAs and also varied in transcripts encoding the TH membrane transporters monocarboxylate transporter 8 (mct8) and organic anion-transporting protein 1c1 (oatp1c1). Tecopa Bore pupfish also exhibited higher dio2 and trß mRNA levels in skeletal muscle relative to Amargosa River fish. Muscle citrate synthase activity was lower at 34°C for both populations, whereas lactate dehydrogenase activity and lactate dehydrogenase A-chain (ldhA) transcripts were both higher and 3,5,3'-triiodothryonine responsive in Tecopa Bore pupfish only. These findings reveal that local population variation and thermal experience interact to shape how pupfish respond to elevated temperatures, and point to the need to consider such interactions in management actions for desert fishes under a changing climate.