Noncoding Variation and Transcriptional Plasticity Promote Thermal Adaptation in Oysters by Altering Energy Metabolism

Abstract

Genetic variation and phenotypic plasticity are both important to adaptive evolution. However, how they act together on particular traits remains poorly understood. Here, we integrated phenotypic, genomic, and transcriptomic data from two allopatric but closely related congeneric oyster species, Crassostrea angulata from southern/warm environments and Crassostrea gigas from northern/cold environments, to investigate the roles of genetic divergence and plasticity in thermal adaptation. Reciprocal transplantation experiments showed that both species had higher fitness in their native habitats than in non-native environments, indicating strong adaptive divergence. The southern species evolved higher transcriptional plasticity, and the plasticity was adaptive, suggesting that increased plasticity is important for thermal adaptation to warm climates. Genome-wide comparisons between the two species revealed that genes under selection tended to respond to environmental changes and showed higher sequence divergence in noncoding regions. All genes under selection and related to energy metabolism exhibited habitat-specific expression with genes involved in ATP production and lipid catabolism highly expressed in warm/southern habitats, and genes involved in ATP consumption and lipid synthesis were highly expressed in cold/northern habitats. The gene for acyl-CoA desaturase, a key enzyme for lipid synthesis, showed strong selective sweep in the upstream noncoding region and lower transcription in the southern species. These results were further supported by the lower free fatty acid (FFA) but higher ATP content in southern species and habitat, pointing to significance of ATP/FFA trade-off. Our findings provide evidence that noncoding variation and transcriptional plasticity play important roles in shaping energy metabolism for thermal adaptation in oysters.

Chromosome‐level genome and population genomic analysis provide insights into the evolution and environmental adaptation of Jinjiang oysterCrassostrea ariakensis

“…The northern and southern groups are morphologically differentiated to some extent (e.g., shell shape, Figure 3b, Table S12a), and their habitats are also characterized by different temperature and salinity. As critical factors, temperature and salinity make selective force driving adaptive divergence of marine invertebrates, especially oysters (Li et al, 2018, 2021; Li, Li, et al, 2020; Zhao et al, 2014). Data from satellite remote sensing show that northern and southern sampling sites display obviously different monthly‐average temperature and temperature range of sea surface during the period from June 2019 to June 2020 (Figure S7).…”

“…For example, the accumulation of hsp60 and hsp70 can promote the heat tolerance of Ruditapes philippinarum and Perna viridis (Aleng et al, 2015; Nie et al, 2017). In addition, healthy energy metabolism can help organisms adapt to changing environment more easily (Li et al, 2021). The pk and pepck are key genes involving in glycolysis/gluconeogenesis and pentose phosphate pathway, which provide energy for organisms.…”

“…The northern and southern groups are morphologically differentiated to some extent (e.g., shell shape, Figure 3b, Table S12a), and their habitats are also characterized by different temperature and salinity. As critical factors, temperature and salinity make selective force driving adaptive divergence of marine invertebrates, especially oysters (Li et al, 2018(Li et al, , 2021Zhao et al, 2014).…”

“…In addition, healthy energy metabolism can help organisms adapt to changing environment more easily (Li et al, 2021). The pk and pepck are key genes involving in glycolysis/gluconeogenesis and pentose phosphate pathway, which provide energy for organisms.…”

“…The pk and pepck are key genes involving in glycolysis/gluconeogenesis and pentose phosphate pathway, which provide energy for organisms. Recently, Li et al (2021) reported the important role of energy allocation mediated by non-coding region variation and gene expression plasticity in high temperature adaptation. Therefore, we suppose that these genes play important roles in the adaptation of the northern C. ariakensis to large temperature changes.…”