Transcriptomics and Fitness Data Reveal Adaptive Plasticity of Thermal Tolerance in Oysters Inhabiting Different Tidal Zones

Abstract

Fine-scale adaptive evolution is always constrained by strong gene flow at vertical level in marine organisms. Rapid environmental fluctuations and phenotypic plasticity through optimization of fitness-related traits in organisms play important roles in shaping intraspecific divergence. The coastal systems experience strong variations in multiple abiotic environmental factors, especially the temperature. We used a typical intertidal species, Pacific oyster (Crassostrea gigas), to investigate the interaction between plasticity and adaptive evolution. We collected intertidal and subtidal oysters from two ecological niches and carried out common garden experiments for one generation. We identified fine-scale vertical adaptive divergence between intertidal and subtidal F1 progeny at both sites, based on different hierarchical phenotypes, including morphological, physiological, and molecular traits. We further quantified the global plasticity to thermal stress through transcriptomic analysis. The intertidal oysters exhibited slow growth rate. However, they showed high survival and metabolic rates under heat stress, indicating vertically fine-scale phenotypic adaptive mechanisms and evolutionary trade-offs between growth and thermal tolerance. Transcriptomic analysis confirmed that the intertidal oysters have evolved high plasticity. The genes were classified into three types: evolutionarily divergent, concordantly plastic, and adaptive plastic genes. The evolved divergence between intertidal and subtidal oysters for these gene sets showed a significant positive correlation with plastic changes of subtidal populations in response to high temperature. Furthermore, the intertidal oysters exhibited delayed large-scale increase in expressional plasticity than that in subtidal counterparts. The same direction between plasticity and selection suggests that the oysters have evolved adaptive plasticity. This implies that adaptive plasticity facilitates the oyster to adapt to severe intertidal zones. The oysters exposed to strong environmental variability are thermal tolerant and have high adaptive potential to face the current global warming. Our findings will not only provide new insights into the significant role of plasticity in adaptive evolution that can be extended to other marine invertebrates, but also provide basic information for oyster resources conservation and reef reestablishment.

Evolutionary trade-offs between baseline and plastic gene expression in two congeneric oyster species

“…Other marine invertebrates, such as corals, show a similar pattern, where inshore warmadapted populations require a greater degree of plastic changes to be resistant to a thermally stressful environment [22]. Considering previous findings [3,6,7,23], we propose that oysters inhabiting thermally stressful environments may preferentially evolve high expression plasticity. However, a concern should be raised that this sublethal temperature may have led to cellular damage in the northern oysters, resulting in lower expression plasticity.…”

“…However, further studies are required to quantify relationships between hsp gene and HSP protein expression under these conditions. In addition to the molecular level, evolutionary trade-offs were also demonstrated at the organismal level: oysters inhabiting environments with greater thermal fluctuation evolve higher thermotolerance but slower growth than their counterparts inhabiting moderate environments [7], as well as oysters dwelling in intertidal or subtidal zones [6].…”

“…worldwide necessitates assessment of their adaptive potential [6,7]. Oysters have evolved a series of genetic and physiological adaptations that confer resilience against harsh environmental conditions, especially in heat shock protein (hsp) genes.…”

Thermotolerance Divergence Revealed by the Physiological and Molecular Responses in Two Oyster Subspecies of Crassostrea gigas in China

“…The pattern of increased followed by decreased aerobic metabolic activity over periods of thermal stress was indicated in oyster (Zhang et al, 2015; Li A. et al, 2017; Li A. et al, 2018; Li L. et al, 2018). In this study, there were clear differences in the ABT that were associated with the different metabolic capabilities of these two subspecies.…”

“…Understanding the role of temperature in establishing fine-scale patterns of thermal tolerance in closely related species can provide additional insights into the nature of adaptive variation in thermal tolerance (Sanford and Kelly, 2011). The relationship between distinctive zonation patterns and thermal tolerance has been indicated in intraspecific Pacific oyster (Li A. et al, 2018) as well as mussels ( Mytilus species) (Halpin et al, 2004), snails (Dong et al, 2017), and limpet species (Prusina et al, 2014). Moreover, latitudinal patterns of variation in intra- and interspecific comparisons of ectotherms, such as fishes (Fangue et al, 2006), crabs (Gaitan-Espitia et al, 2017), mussels (Tagliarolo and McQuaid, 2015), and oysters (Li A. et al, 2017; Li L. et al, 2018) have been documented.…”