Abstract
Paranosema locustae is a gut parasite that has been applied widely in the control of grasshoppers in many parts of the world. Usually, P. locustae is transmitted horizontally via passive modes under natural conditions but in the current study, a positive transmission strategy of P. locustae was demonstrated. First, infection by P. locustae resulted in the cuticula of infected Locusta migratoria nymphs to become lighter in color: normally only a small proportion of locusts are pale with most either being partly or mostly black; but locusts infected with P. locustae became pale. And it was found that the change to pale occurred even among uninfected black and partly black nymphs reared with infected locusts. The eumelanin of the thorax and abdomen of infected individuals decreased significantly, as did the level of dopamine. In addition, there was a decrease in phenol oxidase activity and the expression of henna and pale, which are involved in the synthesis of cuticle melanin, decreased. What is the ecological significance of this increase in light-colored hosts caused by P. locustae? We discovered that light-colored locusts were more susceptible to the microsporidian pathogen than dark-colored individuals were, because of their weaker melanization. Phenol oxidase activity in pale locusts was lower than that of black locusts, but the serpin expression level of pale locusts was higher than that of black individuals. When examined for infection, it was found that initially uninfected nymphs had picked up P. locustae infections indicating that infections are readily passed from one pale locust to another. The infection rate of healthy locusts reared with light-colored locusts infected with P. locustae was 100% which was more than with black-colored ones. The increase in albinistic locusts clearly promoted the prevalence of P. locustae in the total population. In conclusion, these results elucidated a new strategy of positive self-transmission in P. locustae.Importance:Mother Nature always grants wisdom to her creatures and feeds them carefully. This wisdom is particularly apparent in the relationships between two interacting species. In this study, our team focused on the interaction between L. migratoria and P. locustae. In a previous study, it was found that L. migratoria isolate infected individuals, reducing avoiding the spread of P. locustae, in a previous study. The solitary, pale individuals infected by P. locustae were left behind as locust groups marched ahead, leading to a kind of behavioral immunity in the insects. Here, we reported that P. locustae promotes pigmentation loss in L. migratoria, causing a larger proportion of light-colored individuals, and these lighter individuals which possessed weaker immunity against pathogens. This strategy is advantageous to P. locustae, as it promotes its propagation and spread. These extraordinary abilities of L. migratoria and P. locustae have accumulated over millennia of years of interaction.
Highlights
Numerous entomopathogens transmitted in host populations follow the classical vertical and horizontal transmission modes (Bright and Bulgheresi, 2010; Watanabe et al, 2014; Fisher et al, 2017)
Several different phenotypes exist in laboratory populations of locusts
P. locustae infection resulted in a lighter cuticular color in Locusta migratoria: normally only a small proportion of gregarious locusts are pale with most either being partly or mostly black; but locusts infected with P. locustae became pale
Summary
Numerous entomopathogens (pathogenic fungi, pathogenic bacteria and insectivorous nematodes) transmitted in host populations follow the classical vertical and horizontal transmission modes (Bright and Bulgheresi, 2010; Watanabe et al, 2014; Fisher et al, 2017). Pathogens or spores are generally entrained by wind, water flow and host or even non-host organisms (Liu et al, 2016) This requirement means that environmental factors (humidity, environment temperature, and ultraviolet intensity, etc.), which are intermediaries in the transmission process, can influence the transmission efficiency of pathogens (Thomas et al, 1996; Kassa et al, 2004). Multiple studies have demonstrated that P. locustae circulates over greater distances and for longer periods in certain environmental conditions (Shi et al, 2009; Miao et al, 2012) Both horizontal and vertical transmission mechanisms exist in P. locustae (Henry and Oma, 1981; Raina et al, 1995; Lange, 1997), the evidence to date has not demonstrated a positive transmission strategy in P. locustae, but we provide evidence for such transmission here
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