Cross-generational plasticity in Atlantic silversides (Menidia menidia) under the combined effects of hypoxia and acidification.

Abstract

We investigated the potential for cross-generational plasticity to influence how offspring respond to hypoxia and ocean acidification (hereafter HypOA) in the coastal forage fish Atlantic silverside (Menidia menidia). Mature wild silversides were treated with a control (dissolved oxygen (DO):100% air saturation (a.s.) / pCO2: 650 µatm) or HypOA conditions (DO: 40% a.s. / pCO2: 2300 µatm) for 10 days prior to spawning. Their offspring were reared under both treatments in factorial experimental design. Parental environment had minimal effects on offspring phenotype: exposure to HypOA reduced survival and developmental rates regardless of parental treatment. However, RNAseq analysis revealed that direct offspring exposure to HypOA induced substantial transcriptional changes, with 1,606 differentially expressed transcripts (DETs) in larvae from control parents. These changes affected neural development, synaptic signaling, oxygen acquisition, and extracellular matrix organization. In contrast, larvae from HypOA-exposed parents exhibited a muted transcriptional response to HypOA, with only 4 DETs. Although we did not detect a statistically significant interaction between parental and offspring environments at the gene-wise level, a gene set test supported a consistent attenuation of expression changes in offspring from HypOA-treated parents. This pattern may be consistent with transcriptional frontloading, when stress-induced changes are retained and may modify future responses. However, because this effect did not improve offspring performance under HypOA, they are unlikely to represent an adaptive response. Instead, they may reflect non-adaptive carryover effects of parental exposure. Our findings highlight the potential for cross-generational effects to shape transcriptional plasticity, even in the absence of benefits to offspring.