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Limited transgenerational effects of environmental temperatures on thermal performance of a cold-adapted salmonid

Chantelle M. Penney, Gary Burness, Joshua Robertson, Chris C. Wilson

Preprint posted on May 15, 2020 https://www.biorxiv.org/content/10.1101/2020.05.13.094318v1

Like mother, like daughter? Does transgenerational plasticity aid thermal acclimation in Lake Trout?

Selected by Charlotte Nelson

Lake trout (Salvelinus namaycush) are an example of one of many species which inhabit challenging aquatic environments, environments which are predicted to become even more hostile under current climate change projections. Range shifts, migrations, and relocations are already evident in many species, but for others this is simply impossible. For the lake trout, their habitat mainly consists of lakes whose winter ice coverage is decreasing, and surface temperatures is increasing, resulting in limited highly oxygenated refugia during the summer.

In organisms such as the lake trout for whom migration is impossible, adaptation to these changing conditions represents their only option for survival. Phenotypic, developmental and transgenerational plasticity (TGP) represent important components in the adaptation arsenal of any species. TGP describes the preconditioning of offspring for harsher environments based on the environmental experiences of the parents. Previously, TGP has only been demonstrated in eurythermal species, and it is unknown whether those adapted to stenothermal environments will have the standing genetic variation and so plasticity to adapt.

The aim of this study was to test the hypothesis that TGP occurs in cold-adapted, stenothermal ectotherms such as the lake trout, and that this may enable them to cope with a warming, more variable environment. Adult lake trout were acclimated to cool (optimal) or warm temperatures and a factorial mating design was employed to cross fish within and between temperatures. Resulting offspring were also acclimated to cool or warm temperatures that matched or mismatched the experiences of their parents. The authors predicted that if the lake trout can better cope with environmental warming due to TGP then the oxygen uptake (ṀO2) of offspring from warm acclimated parents would be higher compared to those from cool acclimated parents at all temperatures tested.

 

Does transgenerational plasticity play a role? 

Short answer: yes, but it’s complicated. Offspring from warm acclimated parents appear to tolerate warmer temperatures better than those from cool acclimated parents, but only when the offspring were also adapted to warm temperatures. There appears to be a complex set of interactions between parent and offspring environmental experiences which modulate the offspring’s thermal tolerance. Such interactions show a reduced cost of living (which potentially confers increased survival) when there is a matching of parent and offspring thermal experiences, but an increased cost and potentially decreased survival under mismatching conditions.

This study also demonstrates that the relative parental contribution to TGP is additive. The change in offspring ṀO2in response to the thermal challenge was not influenced by the sole effect of either parent’s acclimation temperature, but instead due to a complex interaction between maternal or paternal acclimation temperature with challenge temperature, and offspring acclimation temperature.

TGP appears to play an important role in adaptation, especially for those species which are unable to migrate away from unfavourable environments. However, many cold-adapted species have long generation times (lake trout require 6-12 years to reach maturity) and so may not be able to match the pace of climate changes. Consequently, TGP may provide an opportunity for species with limited within generation plasticity to buffer the challenges of climate change between generations, and therefore give them a chance to develop plasticity to changing thermal environments.

 

 

Outstanding questions

  1. If the lake trout are forced to spend more time in hypoxic areas of the lake as a result of high surface water temperatures, could this provide another avenue by which transgenerational plasticity may be important in the adaptation of this species to climate change?

 

  1. Do you think that thermal acclimation at a different life stage in the parents may be more important for TGP? For example, when the parents were developing fry or during gamete formation?

 

  1. How might the interaction of increased temperature and reduced oxygen availability contribute to the adaptive response seen in species such as the lake trout?

 

 

Additional references

Martin, N.V., Olver, C.H. (1980). The lake charr, Salvelinus namaycush. In: Balon EK, ed., Charrs: Salmonid Fishes of the Genus Salvelinus, First Edition. Springer, Netherlands, pp. 205–277.

Norin, T., Metcalfe, N.B. (2019). Ecological and evolutionary consequences of metabolic rate plasticity in response to environmental change. Philos. Trans. Royal Soc. B 374,20180180.

 

Tags: adaptation, lake trout, thermal tolerance, transgeneraional plasticity

Posted on: 31st May 2020 , updated on: 3rd June 2020

doi: https://doi.org/10.1242/prelights.21441

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  • Author's response

    Chantelle Penney shared

    1. It is entirely possible that the TGP we observe with elevated temperature will also occur with hypoxia in lake trout. We just focussed on the effects of temperature, but there is some published evidence to support TGP with hypoxia in other species of fish.
    2. This is a good question, and we think it highlights an area of research that deserves more research attention. The effect of the parental environment on the offspring’s phenotype can include the inheritance of epigenetic factors that regulate gene expression in the offspring, but patterns of epigenetic regulation are not ‘fixed’ like the sequence of a gene and we don’t really know how long an epigenetic pattern can persist within an individual’s lifetime. It may be environment and/or species specific. Climate change is expected to increase temperature and the number of extreme heat events during the summer. The summer is also when gametogenesis occurs in lake trout and we mimicked this scenario by acclimating adult trout to elevated temperatures during the summer, mirroring the timing for natural lake stratification. If the parents had also experienced warmer temperatures during their earlier life stages, and the epigenetic marks established during development persist into adulthood, then perhaps the TGP we observed in their offspring’s phenotype would have been stronger.
    3. It is difficult to predict how natural populations of lake trout will respond to the combined effect of increased temperature and reduced oxygen availability. Limited phenotypic plasticity and long generation times put the lake trout at an evolutionary disadvantage with rapid climate change, but TGP may buy some time for populations to respond. Different environmental stressors may even act on some of the same physiological pathways, so elevated temperature may induce the expression of physiological traits that are also suited to hypoxia – especially since these two events often naturally occur together. Theoretically, this principle could be extended to TGP where the transgenerational effect of warming and hypoxia occur in unison. It would be interesting to see if the transgenerational response to one environmental change (e.g. warming) facilitates the transgenerational response to another occurring simultaneously (e.g. hypoxia), sort of like a ‘co-operative’ or ‘synergistic’ TGP.

     

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