Long non-coding RNAs mediate fish gene expression in response to ocean acidification.

The majority of the transcribed genome does not have coding potential but these non-coding transcripts play crucial roles in transcriptional and post-transcriptional regulation of protein-coding genes. Regulation of gene expression is important in shaping an organism's response to environmental changes, ultimately impacting their survival and persistence as population or species face global change. However, the roles of long non-coding RNAs (lncRNAs), when confronted with environmental changes, remain largely unclear. To explore the potential role of lncRNAs in fish exposed to ocean acidification (OA), we analyzed publicly available brain RNA-seq data from a coral reef fish Acanthochromis polyacanthus. We annotated the lncRNAs in its genome and examined the expression changes of intergenic lncRNAs (lincRNAs) between A. polyacanthus samples from a natural CO2 seep and a nearby control site. We identified 4728 lncRNAs, including 3272 lincRNAs in this species. Remarkably, 93.03% of these lincRNAs were species-specific. Among the 125 highly expressed lincRNAs and 403 differentially expressed lincRNAs in response to elevated CO2, we observed that lincRNAs were either neighboring or potentially trans-regulating differentially expressed coding genes associated with pH regulation, neural signal transduction, and ion transport, which are known to be important in the response to OA in fish. In summary, lncRNAs may facilitate fish acclimation and mediate the responses of fish to OA by modulating the expression of crucial coding genes, which offers insight into the regulatory mechanisms underlying fish responses to environmental changes.

Warming affects routine swimming activity and novel odour response in larval zebrafish.

Temperature is a primary factor affecting the physiology of ectothermic animals and global warming of water bodies may therefore impact aquatic life. Understanding the effects of near-future predicted temperature changes on the behaviour and underlying molecular mechanisms of aquatic animals is of particular importance, since behaviour mediates survival. In this study, we investigate the effects of developmental temperature on locomotory behaviour and olfactory learning in the zebrafish, Danio rerio. We exposed zebrafish from embryonic stage to either control (28 °C) or elevated temperature (30 °C) for seven days. Overall, warming reduced routine swimming activity and caused upregulation of metabolism and neuron development genes. When exposed to olfactory cues, namely catfish cue, a non-alarming but novel odour, and conspecifics alarming cue, warming differently affected the larvae response to the two cues. An increase in locomotory activity and a large transcriptional reprogramming was observed at elevated temperature in response to novel odour, with upregulation of cell signalling, neuron development and neuron functioning genes. As this response was coupled with the downregulation of genes involved in protein translation and ATP metabolism, novel odour recognition in future-predicted thermal conditions would require energetic trade-offs between expensive baseline processes and responsive functions. To evaluate their learning abilities at both temperatures, larvae were conditioned with a mixture of conspecifics alarm cue and catfish cue. Regardless of temperature, no behavioural nor gene expression changes were detected, reinforcing our findings that warming mainly affects zebrafish molecular response to novel odours. Overall, our results show that future thermal conditions will likely impact developing stages, causing trade-offs following novel olfactory detection in the environment.

Parents exposed to warming produce offspring lower in weight and condition.

The parental environment can alter offspring phenotypes via the transfer of non-genetic information. Parental effects may be viewed as an extension of (within-generation) phenotypic plasticity. Smaller size, poorer physical condition, and skewed sex ratios are common responses of organisms to global warming, yet whether parental effects alleviate, exacerbate, or have no impact on these responses has not been widely tested. Further, the relative non-genetic influence of mothers and fathers and ontogenetic timing of parental exposure to warming on offspring phenotypes is poorly understood. Here, we tested how maternal, paternal, and biparental exposure of a coral reef fish (Acanthochromis polyacanthus) to elevated temperature (+1.5°C) at different ontogenetic stages (development vs reproduction) influences offspring length, weight, condition, and sex. Fish were reared across two generations in present-day and projected ocean warming in a full factorial design. As expected, offspring of parents exposed to present-day control temperature that were reared in warmer water were shorter than their siblings reared in control temperature; however, within-generation plasticity allowed maintenance of weight, resulting in a higher body condition. Parental exposure to warming, irrespective of ontogenetic timing and sex, resulted in decreased weight and condition in all offspring rearing temperatures. By contrast, offspring sex ratios were not strongly influenced by their rearing temperature or that of their parents. Together, our results reveal that phenotypic plasticity may help coral reef fishes maintain performance in a warm ocean within a generation, but could exacerbate the negative effects of warming between generations, regardless of when mothers and fathers are exposed to warming. Alternatively, the multigenerational impact on offspring weight and condition may be a necessary cost to adapt metabolism to increasing temperatures. This research highlights the importance of examining phenotypic plasticity within and between generations across a range of traits to accurately predict how organisms will respond to climate change.

The time course of molecular acclimation to seawater in a euryhaline fish.

The Arabian pupfish, Aphanius dispar, is a euryhaline fish inhabiting both inland nearly-freshwater desert ponds and highly saline Red Sea coastal lagoons of the Arabian Peninsula. Desert ponds and coastal lagoons, located respectively upstream and at the mouths of dry riverbeds ("wadies"), have been found to potentially become connected during periods of intense rainfall, which could allow the fish to migrate between these different habitats. Flash floods would therefore flush Arabian pupfish out to sea, requiring a rapid acclimation to a greater than 40 ppt change in salinity. To investigate the molecular pathways of salinity acclimation during such events, a Red Sea coastal lagoon and a desert pond population were sampled, with the latter exposed to a rapid increase in water salinity. Changes in branchial gene expression were investigated via genome-wide transcriptome measurements over time from 6 h to 21 days. The two natural populations displayed basal differences in genes related to ion transport, osmoregulation and immune system functions. These mechanisms were also differentially regulated in seawater transferred fish, revealing their crucial role in long-term adaptation. Other processes were only transiently activated shortly after the salinity exposure, including cellular stress response mechanisms, such as molecular chaperone synthesis and apoptosis. Tissue remodelling processes were also identified as transient, but took place later in the timeline, suggesting their importance to long-term acclimation as they likely equip the fish with lasting adaptations to their new environment. The alterations in branchial functional pathways displayed by Arabian pupfish in response to salinity increases are diverse. These reveal a large toolkit of molecular processes important for adaptation to hyperosmolarity that allow for successful colonization to a wide variety of different habitats.

Sex- and time-specific parental effects of warming on reproduction and offspring quality in a coral reef fish.

Global warming can disrupt reproduction or lead to fewer and poorer quality offspring, owing to the thermally sensitive nature of reproductive physiology. However, phenotypic plasticity may enable some animals to adjust the thermal sensitivity of reproduction to maintain performance in warmer conditions. Whether elevated temperature affects reproduction may depend on the timing of exposure to warming and the sex of the parent exposed. We exposed male and female coral reef damselfish (Acanthochromis polyacanthus) during development, reproduction or both life stages to an elevated temperature (+1.5°C) consistent with projected ocean warming and measured reproductive output and newly hatched offspring performance relative to pairs reared in a present-day control temperature. We found female development in elevated temperature increased the probability of breeding, but reproduction ceased if warming continued to the reproductive stage, irrespective of the male's developmental experience. Females that developed in warmer conditions, but reproduced in control conditions, also produced larger eggs and hatchlings with greater yolk reserves. By contrast, male development or pairs reproducing in higher temperature produced fewer and poorer quality offspring. Such changes may be due to alterations in sex hormones or an endocrine stress response. In nature, this could mean female fish developing during a marine heatwave may have enhanced reproduction and produce higher quality offspring compared with females developing in a year of usual thermal conditions. However, male development during a heatwave would likely result in reduced reproductive output. Furthermore, the lack of reproduction from an average increase in temperature could lead to population decline. Our results demonstrate how the timing of exposure differentially influences females and males and how this translates to effects on reproduction and population sustainability in a warming world.