Reproduction under heat stress: inhibition of gonadal steroidogenesis and oogenesis in female pupfish at high temperature

Authors: Sean C. Lema, Samantha L. Bock, Michelle I. Chow, Darran May, Andrew H. Dittman

Year: 2016 (xlviii)

Abstract

The ability of desert fishes to cope with increasingly extreme temperatures may be critical to their continued persistence under a changing global climate. Moderate thermal conditions often stimulate reproduction in temperate fishes, but exposure to high temperatures can impair gametogenesis or, in extreme cases, trigger gonadal sex reversal. Cyprinodon pupfishes have the highest recorded thermal range for reproduction among teleost fishes. Even so, reproductive performance in some pupfishes has been observed to decline above approximately 32-34’C. Here, we examined how high water temperature (34-35’C) affected reproductive endocrinology in Cyprinodon pupfishes, with the hypothesis that exposure to high temperatures would alter hormone pathways in patterns indicative of impaired steroidogenesis and gametogenesis. In one experiment, adult C. variegatus pupfish were maintained at either 25’C or 35’C for 14-15 days. Both females and males at 35’C had a smaller gonadosomatic index (GSI) than same sex pupfish at 25’C. Females at 35’C showed lower relative levels of mRNAs encoding receptors for the gonadotropin hormones follicle-stimulating hormone (fshr) and luteinizing hormone (lhr) in gonadal tissues, as well as lower mRNA levels for cholesterol side chain cleavage enzyme (p450scc) and steroid acute regulatory protein (star), two proteins involved in the initial steps of cholesterol conversion to steroid hormones. Females at 35’C also had depressed ovarian gene transcript abundance for ovarian aromatase (cyp19a1a) ’ an enzyme that converts testosterone to estradiol. Similar to females, males exposed to 35’C exhibited lower relative levels of lhr and p450scc mRNAs in the testis than males at 25’C. In a second experiment, adult Amargosa pupfish, C. nevadensis amargosae, from two allopatric populations - Tecopa Bore and the Amargosa River - were acclimated in captivity to 24’C or 34’C for 88 days. Gene transcripts encoding receptors for the gonadotropin fshr and lhr receptors were again observed to be lower in the gonads of both sexes at 34’C compared to fish at 24’C. Tecopa Bore females exposed to 34’C also exhibited lower ovarian mRNA abundance for P450 aromatase, as well as depressed levels of mRNAs encoding vitellogenin yolk proteins and choriogenin egg envelope proteins in the liver. Combined, the results from these two experiments suggest that fe male C. n. amargosae exposed to stable temperature environments of 34-35’C may experience reduced gonadal estrogen synthesis and impaired oogenesis. Despite the phenomenal thermal range exhibited by these two Cyprinodon taxa, our findings imply that fish may experience impaired reproductive performance at 34-35’C, even though these temperatures are well within the range of thermal tolerance for these species.