Timing of reproduction modifies transgenerational effects of chronic exposure to stressors in an annual vertebrate

Abstract

Stressful environmental conditions can shape both an individual's phenotype and that of its offspring. However, little is known about transgenerational effects of chronic (as opposed to acute) stressors, nor whether these vary across the breeding lifespan of the parent. We exposed adult female (F0 generation) three-spined sticklebacks ( Gasterosteus aculeatus ) to chronic environmental stressors and compared their reproductive allocation with that of non-exposed controls across early, middle and late clutches produced within the single breeding season of this annual population. There was a seasonal trend (but no treatment difference) in F0 reproductive allocation, with increases in egg mass and fry size in late clutches. We then tested for transgenerational effects in the non-exposed F1 and F2 generations. Exposure of F0 females to stressors resulted in phenotypic change in their offspring and grandoffspring that were produced late in their breeding lifespan: F1 offspring produced from the late-season clutches of stressor-exposed F0 females had higher early life survival, and subsequently produced heavier eggs and F2 fry that were larger at hatching. Changed maternal allocation due to a combination of seasonal factors and environmental stressors can thus have a transgenerational effect by influencing the reproductive allocation of daughters, especially those born late in life.

Intergenerational plasticity to cycling high temperature and hypoxia affects offspring stress responsiveness and tolerance in zebrafish

“…Overall, with few exceptions (e.g. Stratholt et al, 1997 ), chronic maternal stress or elevated maternal plasma cortisol levels do not increase egg cortisol content in fishes ( Mileva et al, 2011 ; Sopinka et al, 2014 ; Jeffrey and Gilmour, 2016 ; Taylor et al, 2016 ; Lim and Bernier, 2022 ; Magierecka et al, 2022 ) implying that the ovary and embryo have a high capacity to buffer against maternal cortisol transfer in these animals. Nevertheless, although basal cortisol levels did not differ between larval treatments, the reduced hsd11b2 and hsd20b2 resting mRNA levels of the 5 dpf combined exposure larvae suggest potential carryover effects of the parental treatment on progeny cortisol catabolism.…”

“…In placental and egg-laying species, maternal stressors can increase the deposition of GCs into offspring ( Saino et al, 2005 ; Almasi et al, 2012 ; Sheriff and Love, 2013 ; Sopinka et al, 2017a ), and maternal GCs are known for their capacity to induce epigenetic modifications and shape offspring morphology, physiology and behavior ( McCormick, 1998 ; Kapoor and Matthews, 2005 ; Eriksen et al, 2011 ; Capelle et al, 2016 ; Sopinka et al, 2017b ; Best et al, 2017 ). In fish, however, it is unclear whether maternal stressors lead to an increase in offspring GC levels ( Stratholt et al, 1997 ; Sopinka et al, 2014 ; Taylor et al, 2016 ; Lim and Bernier, 2022 ; Magierecka et al, 2022 ) or whether exogenous GCs can improve offspring stressor tolerance ( Redfern et al, 2017 ; Warriner et al, 2020a , b ). In addition, fish eggs may buffer against maternally derived GCs using ATP-binding cassette efflux transporters ( Fischer et al, 2013 ; Paitz et al, 2016 ) and by converting GCs into inert forms using the catabolic enzymes 11β hydroxysteroid dehydrogenase type 2 (11β-HSD2) and 20β-HSD2 ( Alderman and Vijayan, 2012 ; Tokarz et al, 2012 ; Faught et al, 2016 ).…”

Elucidating the Effects of the Lipids Regulators Fibrates and Statins on the Health Status of Finfish Species: A Review

“…More chronic studies are needed to ascertain the effects of lipid-regulating agents at the population level in free-living fishes, including those that, such as salmonids, have experienced several rounds of genome duplication, gained a duplicated set of genes related to lipid regulation and management, and, thus, may be more resilient to pharmaceuticalderived metabolic alterations [132]. Seasonal trends in lipid allocation for vitellogenesis and gonadal maturation, coupled with transgenerational alterations due to chronic exposure to environmental stressors have been described in three-spined sticklebacks (Gasterosteus aculeatus) in an attempt to dissect the complexity of reproductive allocation of resources during the breeding season [133]. These, and other species with context-dependent lifecycles deserve more studies concerning the synergistic or antagonistic effects of lipid regulators, acting alone or coupled with other stressors, on normal and maladaptive physiology of fishes.…”

How important is hidden phenotypic plasticity arising from alternative but converging developmental trajectories, and what limits it?

“…There were no significant differences in the phenotype of offspring produced by stressed and control females early in the season. But by the time of the last clutches of the breeding season, the mothers exposed to stressors were producing offspring that were superficially similar to controls but had a higher survival rate (suggesting an altered trajectory), and in turn, these offspring produced larger eggs and fry (the grandoffspring of the exposed mothers) when they themselves came to breed ( Magierecka et al, 2022 ). The physiological mechanisms underlying these effects are not clear, not least because the environmental stressors, although causing changes in the mothers' behaviour, did not cause a measurable increase in their cortisol levels ( Magierecka et al, 2021 ).…”