Transcriptomic Responses of Two Ecologically Divergent Populations of Japanese Mantis Shrimp (Oratosquilla oratoria) under Thermal Stress

SIMPLE SUMMARY: Rising ocean temperature would change the seawater chemistry and affect the external and internal physiology of crustaceans due to their lack of certain efficient temperature regulators. In addition, the infraspecific populations of crustaceans might also have different response strategies to the rising of temperature. Therefore, we identified the transcriptomic variations to the same thermal stress between ecologically divergent populations of Oratosquilla oratoria. The aim of this study was to investigate the population-specific function genes and relevant pathways in response to thermal stress in O. oratoria. The results showed that gene-expressed variation was in a population-specific pattern, which indicated that the local environment could lead to the evolvement of changes in gene regulation, ultimately leading to adaptive divergences. Additionally, we found several genes with large pleiotropic effects in the Zhoushan population, which might indicate that the regulation mechanisms of the Zhoushan population were more efficient than those of the Qingdao population under same thermal stress. The results provided some novel insights into the local adaptive differences of the infraspecific populations of O. oratoria and other crustaceans. ABSTRACT: Crustaceans are generally considered more sensitive to ocean warming due to their lack of certain efficient regulators. However, the alterations in the physiology and behavior of crustaceans in response to thermal stress differ vastly even among the infraspecific populations of heterogeneous landscapes. Consequently, understanding the impact of temperature fluctuation on crustacean infraspecific populations might be essential for maintaining a sustainable persistence of populations at existing locations. In the present study, we chose the Japanese mantis shrimp (Oratosquilla oratoria) as the representative crustacean population, and conducted transcriptome analyses in two divergent O. oratoria populations (the Zhoushan and Qingdao populations) under same thermal stress (20–28 °C) to identify the population-specific expression response to thermal stress. The results showed significant differences in gene expressions, GO terms and metabolic pathways between the two populations. We hypothesized that intraspecific mutations in the same or different genes might lead to thermal adaptive divergences. Temperature increases from 20–28 °C produced significant enrichment in GO terms and altered the metabolic pathways in the Zhoushan population despite the lack of differentially expressed unigenes. Therefore, several functional genes with large pleiotropic effects may underlie the response to thermal stress in the Zhoushan population. Furthermore, the most significantly enriched biological processes of the Qingdao population were associated with the state or activity of cells and its significant enriched pathways with genetic information processing as well as immune and environmental information processing. In contrast, the differentially regulated unigenes of the Zhoushan population were primarily involved in the regulatory cellular and transcription processes and the most significant pathways found were metabolic and digestive. Consequently, the regulatory mechanisms of the Zhoushan population are probably more efficient than those of the Qingdao population under the same thermal stress.