Molecular basis of parental contributions to the behavioural tolerance of elevated pCO2 in a coral reef fish

Abstract

Knowledge of adaptive potential is crucial to predicting the impacts of ocean acidification (OA) on marine organisms. In the spiny damselfish, Acanthochromis polyacanthus, individual variation in behavioural tolerance to elevated pCO₂ has been observed and is associated with offspring gene expression patterns in the brain. However, the maternal and paternal contributions of this variation are unknown. To investigate parental influence of behavioural pCO₂ tolerance, we crossed pCO₂-tolerant fathers with pCO₂-sensitive mothers and vice versa, reared their offspring at control and elevated pCO₂ levels, and compared the juveniles' brain transcriptional programme. We identified a large influence of parental phenotype on expression patterns of offspring, irrespective of environmental conditions. Circadian rhythm genes, associated with a tolerant parental phenotype, were uniquely expressed in tolerant mother offspring, while tolerant fathers had a greater role in expression of genes associated with histone binding. Expression changes in genes associated with neural plasticity were identified in both offspring types: the maternal line had a greater effect on genes related to neuron growth while paternal influence impacted the expression of synaptic development genes. Our results confirm cellular mechanisms involved in responses to varying lengths of OA exposure, while highlighting the parental phenotype's influence on offspring molecular phenotype.

Keywords: climate change; genetic variance; ocean acidification; parental effects; phenotypic variation; transcriptome.

Figure 1.

Experimental design detailing the creation of breeding pairs, the holding conditions for parents and offspring, the testing conditions prior to euthanasia for the offspring and the names of the four different treatments as they are identified in the text. The blue colour refers to tolerant female, sensitive male parental pairs while green indicates tolerant male, sensitive female parental pairs.

Figure 2.

Principal coordinate analysis of variance stabilized read counts. Parental identity is indicated by shape and condition bycolour. Ellipses designate clusters by condition and are coloured to match. (Online version in colour.)

Figure 3.

Number of DEGs from pairwise comparisons between parental pairs within conditons and between conditions with parental pairs as a factor. Fish colour indicates parental identity while rectangle colour indicates labelled offspring treatment. (Online version in colour.)

Figure 4.

Principal component analysis of the top 5000 significant genes after running the LRT; (a) displays offspring from chronic treatments while (b) shows those from acute treatments. Condition is indicated by shape and parental identity by colour. Ellipses signify clusters due to parental identity and are coloured to match. (Online version in colour.)

Figure 5.

Graph of significantly enriched GO terms between all conditions compared to control, within parental pairs. Colour indicates the delta rank statistic from the GO-MWU enrichment while bubble size indicates FDR. GO terms associated with upregulated genes are considered positive while those related to downregulated genes are negative. (Online version in colour.)