Early warming stress on rainbow trout juveniles impairs male reproduction but contrastingly elicits intergenerational thermotolerance

Abstract

The exposure of adult fish to warm or high temperatures is known to impair reproduction, yet the long-term reproductive impacts for treatments at early life are not well clarified. This study aimed to evaluate the effects of warm temperature (WT) during juvenile stage on gonad maturation, gamete quality, and offspring thermotolerance in rainbow trout. While the comparison of basic reproductive parameters in WT females did not reveal any kind of impairment, many WT males showed an atrophied, undeveloped gonad, or a smaller testis with lower milt volume; sperm quality parameters in WT males and deformity rates in the respective progeny were also highly affected. However, despite of such negative effects, many of the remaining progeny presented better rates of survival and growth when exposed to the same conditions as those of parental fish (WT), suggesting that thermal stress in parr stage males elicited intergenerational thermotolerance after a single generation. The present results support that prolonged warming stress during early life stages can adversely affect key reproductive aspects, but contrastingly increase offspring performance at upper thermal ranges. These findings have implications on the capacity of fish to adapt and to cope with global warming.

Epigenetic Landscape of Heat Stress Intergenerational Inheritance in a Teleost Fish

“…In the tongue sole Cynoglossus semilaevis , thermally-induced sex reversed F1 pseudo-males have sex-reversed pseudo-male offspring although these F2 larvae are not exposed to thermal induction (Chen et al, 2014). In the rainbow trout Oncorhynchus mykiss , offspring thermotolerance (survival and growth) is improved when genitors also have experienced increased rearing temperature during gametogenesis (Butzge et al, 2021). These data argue in favor of an intergenerational epigenetic inheritance, and suggest that gametes can transmit environmental acclimation clues to the offspring.…”

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

“…Elevated temperature downregulation of steroidogenesis leads to lower circulating E 2 (similar to high temperature-induced masculinization; see §2a), which diminishes vitellogenin and choriogenin synthesis by the liver [55,56], impairs secondary/vitellogenic oocyte growth and chorion formation, and, ultimately, results in fewer or smaller eggs and lower egg viability [14]. Adult male fish have also been observed in some species to exhibit changes in HPG axis function at high temperatures [14,[56][57][58], although effects for males vary more across species than for females. Reductions in brain gnrh1 mRNA levels, pituitary Fsh β-subunit (fshb) and Lh β-subunit (lhb) mRNA levels, testicular gonadotropin receptor and steroidogenic enzyme expression, and circulating T and 11-KT have been reported in males of some fishes at elevated temperature [14,16,17,56,58].…”

“…Those changes in HPG axis signalling are likely responsible, in part, for the delayed sperm maturation, lower semen volumes, or reduced sperm motility observed in some fishes subjected to elevated temperature (e.g. [14,57]). Interestingly, male rainbow trout ( Oncorhynchus mykiss ) exposed to high temperature during the juvenile parr stage had lower sperm volumes and impaired sperm motility later in life, but also higher rates of survival and growth for offspring when their progeny were exposed to warmer conditions [57].…”

“…[14,57]). Interestingly, male rainbow trout ( Oncorhynchus mykiss ) exposed to high temperature during the juvenile parr stage had lower sperm volumes and impaired sperm motility later in life, but also higher rates of survival and growth for offspring when their progeny were exposed to warmer conditions [57]. Differences in DNA methylation were recently observed in spermatozoa from male rainbow trout experiencing 12 and 16°C during spermatogenesis [59], indicating chromatin remodelling of spermatozoa by temperature.…”

Does post-ejaculatory sperm experience prior to fertilization alter offspring performance beyond paternity in an external fertilizing fish?

“…However, there is increasing evidence of paternal effects, challenging the conventional notion that fathers solely contribute DNA through sperm (Crean et al, 2013; Crean & Bonduriansky, 2014; Evans et al, 2017; Ragsdale et al, 2022; Simmons et al, 2022). Changes in the father’s experience, such as modifications in diet, changes in hormonal profiles, or altered social interactions, can affect the content of their semen and influence offspring development (Butzge et al, 2021; see review Evans et al, 2019; Ragsdale et al, 2022; Simmons et al, 2022). But sperm also encounter various conditions post-release, especially in external fertilizers (Purchase et al, 2021).…”