Embryonic thermal environments drive plasticity in gene expression

Abstract

When embryos experience different environments than their parents, plasticity can enable the development of alternate phenotypes that confer higher fitness in the new conditions. Temperature-induced plasticity could be especially critical for species that inhabit areas with considerable thermal variation. We studied transcriptional variation in embryos of mangrove rivulus (Kryptolebias marmoratus)—a self-fertilizing hermaphroditic, eurythermal fish that resides in notoriously spatiotemporally variable mangrove forests—exposed to different thermal regimes during development. To study transcriptional plasticity, we first improved the genome assembly to chromosome length scaffolds (N50 of 28.17 Megabases). Whole transcriptome sequencing revealed that both temperature and developmental timing modulated embryonic gene expression. We found few differences in gene expression between embryos incubated in cold and warm conditions and assessed before the temperature-sensitive period of development, indicating high resistance to stochastic changes in gene expression early in development. Replicate embryos exposed to cold temperatures and sampled after the temperature-sensitive period showed less variation in gene expression than those sampled before, suggesting canalization of the plastic response. DNA replication/repair, organelle, and gas transport pathways were upregulated while nervous system development, cell signaling, and cell adhesion were downregulated in cold-exposed compared to warm-exposed embryos sampled after the temperature-sensitive period. These plastic shifts in gene expression could have major implications for reorganizing the phenotype (e.g., apoptosis, mitosis) in response to environmental changes occurring within a generation.