Research Article: UVB Radiation Delays Tribolium castaneum Metamorphosis by Influencing Ecdysteroid Metabolism

Date Published: March 17, 2016

Publisher: Public Library of Science

Author(s): Wen Sang, Lin Yu, Li He, Wei-Hua Ma, Zhi-Hui Zhu, Fen Zhu, Xiao-Ping Wang, Chao-Liang Lei, Joshua B. Benoit.

http://doi.org/10.1371/journal.pone.0151831

Abstract

Ultraviolet B (UVB) radiation is an important environmental factor. It is generally known that UVB exhibits high genotoxicity due to causing DNA damage, potentially leading to skin carcinogenesis and aging in mammals. However, little is known about the effects of UVB on the development and metamorphosis of insects, which are the most abundant terrestrial animals. In the present study, we performed dose-response analyses of the effects UVB irradiation on Tribolium castaneum metamorphosis, assessed the function of the T. castaneum prothoracicotropic hormone gene (Trcptth), and analyzed ecdysteroid pathway gene expression profile and ecdysterone titers post-UVB irradiation. The results showed that UVB not only caused death of T. castaneum larvae, but also delayed larval-pupal metamorphosis and reduced the size and emergence rate of pupae. In addition, we verified the function of Trcptth, which is responsible for regulating metamorphosis. It was also found that the expression profiles of Trcptth as well as ecdysteroidogenesis and response genes were influenced by UVB radiation. Therefore, a disturbance pulse of ecdysteroid may be involved in delaying development under exposure to irradiation. To our knowledge, this is the first report indicating that UVB can influence the metamorphosis of insects. This study will contribute to a better understanding of the impact of UVB on signaling mechanisms in insect metamorphosis.

Partial Text

Solar ultraviolet radiation (UVR) is an important environmental factor in ecosystem and is classified into three categories: UVA (315–400 nm), UVB (280–315 nm), and UVC (200–280 nm) [1]. UVC is rarely reported to play a role in ecology due to its complete absorption by the ozone layer. Although UVA constitutes approximately 95% of solar UV radiation reaching the earth’s surface, it is regarded as a far less harmful environmental stressor because of its low DNA damaging ability. UVB constitutes only 5% of solar UV radiation, but it exhibits high genotoxicity due to the formation of cyclobutane pyrimidine dimers and (6–4) photoproducts through the excitation of nucleobases and oxygen-independent reactions, causing mutations. Thus, UVB has received more attention [2–4]. A considerable amount of research has mainly focused on detrimental effects on mammals, such as skin carcinogenesis and aging [5–7]. However, it is currently unclear how UVB radiation affects other important biological processes, such as development and metamorphosis, in other organisms. A few studies have referred to the effects of UVB on amphibians, such as Rana clamitans Latreille, Rana aurora Baird and Girard, and Rana pipiens Schreber, which include arrest and delay of the development and metamorphosis of larvae and reduction of larval mass [8–10]. However, little is known about the effects of UVB on the development and metamorphosis of insects, which are the most abundant group of terrestrial animals [11, 12].

UVB radiation can impact the larval-pupal metamorphosis and survival of T. castaneum. UVB-induced death of insects has been reported in previous studies, which is consistent with our results [11, 12]. In the present study, the development and metamorphosis of last-instar larvae of T. castaneum were prevented or delayed by UVB irradiation (Fig 1A). UVB-induced disruption of amphibian development was first detected in R. pipiens Schreber, whose embryos showed developmental delay after 3 days of UVB exposure from a quartz mercury-lamp. This study demonstrated that UVB could not only cause outright mortality, but could also have sublethal effects (impediments to development) [32]. Croteau summarized 12 studies on amphibian species showing that UVB radiation emitted from sunlight or an artificial source can induce various changes in amphibian development and metamorphosis, including delays and acceleration [33]. In the insect M. sexta L., UVB can only delay development of first-instar larvae and does not affect fifth-instar larvae [11]. T. castaneum is a pest of stored grain, and all stages of its life cycle develop within the food substrate. The low-UV environment of this beetle makes it highly sensitive to UV. Strategies for coping with UVB might have been lost in this species, resulting in obvious UVB-induced effects. Therefore, the observed variation in the influence on development and metamorphosis might be related to the species and developmental stages. UVB induced high mortality in larvae under increasing doses, but the larvae did not die immediately after irradiation (Fig 1B). Indeed, most of the insects survived for quite a long time post-irradiation, surviving for more than 16 days in some groups (data not shown). The UVB-induced damage to organisms is mainly related to DNA lesions. If these lesions overwhelm the DNA repair system, they lead to mutation. Although larvae still lived on post irradiation, mutations accumulate continuously with DNA replication and mitotic, ultimately resulting in abnormal gene expression and physiological disorders [2–4]. It is only when the accumulation of disorders reaches a level that exceeds the repair ability of insects that death will occur. Surviving insects were able to pupate and emerge after low-dose UVB exposure, but their pupal size was significantly reduced (Fig 1C and 1D). Animal body size is determined by the duration of the growth period and the amount of nutrition obtained during that period [34]. UVB delayed metamorphosis and increased the growth period, but the pupae became much smaller, indicating that the insects either reduced their nutrient intake or increased their nutrient consumption, which could be related to a decline in feeding activity or too great an energy input for repair activities. To our knowledge, this is the first report indicating that UVB can influence the metamorphosis of insects.

 

Source:

http://doi.org/10.1371/journal.pone.0151831