Microsporidia-host interactions in beneficial lady beetles : factors that influence chronic disease

Abstract

Lady beetles produce species-specific defensive compounds (alkaloids) that are toxic to some predators and deters others with their foul taste. Some lady beetle alkaloids, such as harmonine from <em>Harmonia axyridis</em>, exhibit antimicrobial activity and may provide the beetle protection against pathogens. Convergine and hippodamine are the major and minor alkaloids produced by the convergent lady beetle, <em>Hippodamia convergens</em>. Adaline and adalinine are produced by the two-spotted lady beetle, <em>Adalia bipunctata</em>. Although the defensive chemistry of these lady beetles has received some attention, the role of their alkaloids with respect to pathogen virulence is poorly understood. Microsporidia, intracellular spore-forming parasites, have been reported in several coccinellid species, including <em>Tubulinosema hippodamiae</em> from <em>H. convergens</em> and <em>Vairimorpha (Nosema) adaliae</em> from <em>A. bipunctata</em>. These pathogens delay larval development but have no other observable effect on the host. However, previous studies were performed under optimal laboratory conditions and did not take into consideration challenges (stress factors) beetles would face in the natural environment. The objective of this study is to determine the relationship between alkaloids and microsporidiosis in <em>H. convergens</em> and <em>A. bipunctata</em>, and to examine the effects of different stress factors (limited food availability, rearing temperatures above optimal, and physical agitation) on the development of microsporidiosis and production of alkaloids in these beetles. During all three research trials, larval development was delayed for microsporidia-infected beetles when compared to uninfected beetles. In Chapter Two, limited food availability for microsporidia-infected <em>A. bipunctata</em> further delayed larval development compared to uninfected beetles, increased pathogen load and reduced adaline content. An irregular, unpredictable food supply acts as a stressor to further amplify the negative effects of microsporidiosis for <em>A. bipunctata</em>. No further development delays were observed for <em>H. convergens</em> when provided an irregular diet and no conclusions could be made regarding <em>H. convergens</em> alkaloid content. In Chapter Three, rearing <em>A. bipunctata</em> at temperatures above 25&deg;C shortened development, decreased pathogen load, and increased adaline content. Temperatures above 25&deg;C mitigate the microsporidian infection. In the final chapter, adaline content increased as <em>A. bipunctata</em> development progressed, uninfected adults produced more adaline than infected beetles when exposed to physical agitation on alternate days, and spore counts were highest when beetles were exposed to daily shaking. As with limited food availability, physical agitation further amplified the negative effects of microsporidiosis in<em> A. bipunctata</em> and had an influence on alkaloid production. Many plants produce antimicrobial secondary metabolites (phytoalexins) that can inhibit the germination and/or growth of bacteria and fungi. Alkaloids present in lady beetles may act as the animal equivalent of phytoalexins and play a larger role in the coccinellid immune system than previously thought. These findings provide some preliminary insight into the relationship between adaline, <em>V. adaliae</em> and <em>A.bipunctata</em>, including certain factors that influence this relationship. However, adalinine, hippodamine and convergine, alkaloids not examined in this study, may also influence infection and could be the focus of future studies.