Parental hypoxic exposure confers offspring hypoxia resistance in zebrafish (Danio rerio)

Abstract

SUMMARYParental influences are a potentially important component of transgenerational transfer of phenotype in vertebrates. This study examined how chronic hypoxic exposure on adult zebrafish (Danio rerio) affected the phenotype of their offspring. Separate adult populations were exposed to hypoxia (13.1kPa O 2 ) or normoxia (21.1kPa O 2 ) for periods ranging from 1 to 12weeks. Adults were then returned to normoxia and bred within experimental groups. Adult fecundity and egg characteristics (volume of egg, yolk and perivitelline fluid) were assessed. Subsequently, larval body length, time to loss of equilibrium in severe hypoxia (~4kPa O 2 ), and critical thermal minima (CT min ) and maxima (CT max ) were measured at 6, 9, 12, 15, 18, 21 and 60days post-fertilization (d.p.f.). Adult fecundity was depressed by hypoxic exposure. Egg component volumes were also depressed in adults exposed to 1-2weeks of hypoxia, but returned to control levels following longer hypoxic exposure. Adult hypoxic exposures of >1week resulted in longer body lengths in their larval offspring. Time to loss of equilibrium in severe hypoxia (i.e. hypoxic resistance) in control larvae decreased from 6 to 12d.p.f., remaining constant thereafter. Notably, hypoxic resistance from 6 to 18d.p.f. was ~15% lower in larvae whose parents were exposed to just 1week of chronic hypoxia, but resistance was significantly increased by ~24-30% in 6-18d.p.f. larvae from adults exposed to 2, 3 or 4weeks of hypoxia. CT min (~10-12°C) and CT max (~39.5°C) were unchanged by parental hypoxic exposure. This study demonstrates that parental hypoxic exposure in adult zebrafish has profound epigenetic effects on the morphological and physiological phenotype of their offspring.

Can acclimation of thermal tolerance, in adults and across generations, act as a buffer against climate change in tropical marine ectotherms?

“…Without being able to follow single parent crosses it is not possible to assess the heritability of thermal acclimation from the current study. Transgenerational plasticity is, however, increasingly being recognized as a mechanism providing mitigation for some of the negative impacts of climate change (Donelson and Munday, 2015;Zizzari and Ellers, 2014) including increasing CT max across generations (Ho and Burggren, 2012). Highlights  Adult acclimation of CT max was low; 0 to 0.06°C per 1°C increase in temperature  Transgenerational acclimation was up to 5 times greater than adult acclimation  Transgenerational acclimation may buffer climate change in tropical ectotherms…”

Epigenetics as a source of variation in comparative animal physiology – or – Lamarck is lookin' pretty good these days

“…(B) Transgenerational transfer of hypoxia tolerance, with decreased and increased tolerance evident in larvae whose parents were exposed to 1 week or 2-4 weeks, respectively, of hypoxia. After Ho and Burggren (Ho and Burggren, 2012).…”

“…For example, non-genetic inheritance of hypoxia tolerance has recently been demonstrated in the zebrafish, Danio rerio (Ho and Burggren, 2012). Adult zebrafish of both sexes were first raised in air-saturated water (normoxia, ~21kPa) at 27±0.5°C in standard 12h light/12h dark conditions, and fed daily with tropical fish flakes.…”

Physiological tradeoffs may underlie the evolution of hypoxia tolerance and exercise performance in sunfish (Centrarchidae)

“…Developmental plasticity can have a strong influence on adult physiology (West-Eberhard, 2003; Scott and Johnston, 2012; Schnurr et al, 2014), and developmental hypoxia in particular can have persistent effects on hypoxia tolerance, the gas-exchange organs, and the activities of metabolic enzymes in several tissues (Crocker et al, 2013;Blank and Burggren, 2014;Robertson et al, 2014). Exposure of parent zebrafish to hypoxia has also been shown to improve the hypoxia tolerance of their offspring (Ho and Burggren, 2012), suggesting that trans-generational effects could have also influenced some of our observations. Nevertheless, all of the fish we studied were caught from a single and relatively shallow lake to help minimize the variation in parental and developmental environment between species.…”