An interplay between plasticity and parental phenotype determines impacts of ocean acidification on a reef fish

Abstract

The impacts of ocean acidification will depend on the ability of marine organisms to tolerate, acclimate and eventually adapt to changes in ocean chemistry. Here, we use a unique transgenerational experiment to determine the molecular response of a coral reef fish to short-term, developmental and transgenerational exposure to elevated CO, and to test how these responses are influenced by variations in tolerance to elevated CO exhibited by the parents. Within-generation responses in gene expression to end-of-century predicted CO levels indicate that a self-amplifying cycle in GABAergic neurotransmission is triggered, explaining previously reported neurological and behavioural impairments. Furthermore, epigenetic regulator genes exhibited a within-generation specific response, but with some divergence due to parental phenotype. Importantly, we find that altered gene expression for the majority of within-generation responses returns to baseline levels following parental exposure to elevated CO conditions. Our results show that both parental variation in tolerance and cross-generation exposure to elevated CO are crucial factors in determining the response of reef fish to changing ocean chemistry.

Elevated CO2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon (Oncorhynchus kisutch)

“…We did not observe significant changes in gene expression of the GABA type A receptor, which has been hypothesized to play a role in CO 2 ‐linked disruption of neuronal and behavioral signaling in marine fish (Schunter et al, ). Interestingly, however, the expression of the GABA type B receptor subunit 2 ( gaba b2 ) was significantly elevated in the olfactory bulb following the high CO 2 exposure (Table , FDR <0.1).…”

Predatory strategies and behaviours in cephalopods are altered by elevated CO2

“…Similarly, Spady et al (2014) found no inhibition in the physical ability of pygmy squid to escape a predator, but instead changes in the types of escape responses utilized. This change in the decision-making process could be attributed to altered function of neurotransmitter receptors, such as GABA-A receptors, as suggested previously for molluscs (Moya et al, 2016;Watson et al, 2014) and fishes (Heuer & Grosell, 2014;Lai et al, 2015;Nilsson et al, 2012;Schunter et al, 2017). Changes to visual acuity (Chung, Marshall, Watson, Munday, & Nilsson, 2014), the function of the lateral line systems (see York & Bartol, 2014), or other alterations to sensory inputs, could also contribute to changes in predatory behaviour, either through impaired neurotransmitter function, or possibly other mechanisms (Briffa, de la Haye, & Munday, 2012).…”

“…GABA‐A receptors are important in this context as they appear to be responsible for the behavioural changes in other molluscs (Watson et al., ) and fishes (Hamilton, Holcombe, & Tresguerres, ; Heuer, Welch, Rummer, Munday, & Grosell, ; Lai, Jutfelt, & Nilsson, ; Nilsson et al., ) resulting from elevated CO 2 . Recent molecular analyses also demonstrate that substantial changes to GABA pathways are a feature of high CO 2 exposure in other invertebrates (Moya et al., ) and fish (Schunter et al., ), further supporting a role in behavioural changes. Cephalopods exhibit some of the most remarkable and flexible cryptic capabilities in the animal kingdom by mimicry of the surrounding environment (Hanlon & Messenger, ).…”

Predator‐induced maternal and paternal effects independently alter sexual selection

“…; Schunter et al. ). If parental effects also act on reproduction, the implications are extensive, as mating decisions can directly impact the generation and maintenance of species boundaries.…”

“…Much recent attention has focused on the potential for parental effects to facilitate rapid inter-and transgenerational responses to novel and changing environments, including predation (Burton and Metcalfe 2014;Kokko et al 2017). In these studies, however, emphasis has been on how parental effects that anticipate the parental environment enhance offspring survival (Storm and Lima 2010;Giesing et al 2011;Roche et al 2012;McGhee and Bell 2014;Stein and Bell 2014;Walsh et al 2015;Beaty et al 2016;Schunter et al 2018). If parental effects also act on reproduction, the implications are extensive, as mating decisions can directly impact the generation and maintenance of species boundaries.…”