Evolutionary ecology of microsporidia associated with the invasive ladybird Harmonia axyridis

Abstract

Invasive species are characterized by the rapid growth and spread of their populations after establishing a foothold in new habitats, and there are now many examples of such species negatively affecting biodiversity and the economy. It is unclear why some species can become successful invaders, whereas most (even if closely related) remain noninvasive. We previously proposed a hypothesis that parasites associated with invading species can promote their invasive success if they are harmless toward the invaders but harmful to their competitors and/or predators in the newly colonized habitat. Here we discuss whether microsporidia that have recently been discovered in the invasive ladybird Harmonia axyridis contribute to its invasive success. We show that all H. axyridis beetles sourced from diverse collection sites all over the world carry abundant microsporidia. This suggests that both native and invasive H. axyridis populations are associated with these tolerated parasites, which were likely to have existed in native populations before expansion rather than being acquired in newly colonized areas. We describe the pathogenesis of the microsporidia during different developmental stages of H. axyridis and we address the possibility that the predation of its infected eggs and larvae by competing native ladybird species may lead to their infection and ultimately to their decline. Finally, we discuss our initial hypothesis: microsporidia that are tolerated by an invasive vector insect can be active against susceptible native competitors and/or predator species.

Predators and parasitoids of the harlequin ladybird, Harmonia axyridis, in its native range and invaded areas

“…Further protection of the larvae is provided by spiny projections on their cuticle. Apart from these chemical and mechanical defenses, H. axyridis is also equipped with a biological weapon against some predators-symbiotic microsporidia, which are lethal to potential intraguild predators, C. septempunctata and A. bipunctata (Vilcinskas et al 2013(Vilcinskas et al , 2015Vogel et al 2017; but see Sloggett 2013;Solter et al 2013;Gegner et al 2015).…”

Der Asiatische Marienkäfer als Modell

“…Unsere Untersuchungen und publizierte Feldstudien weisen darauf hin, dass mit Eiern oder Larven aufgenommenes Harmonin von einheimischen Marienkäfern toleriert wird. [11].…”

“…Für die invasiven Marienkäfer ist es auf lange Sicht auch von Vorteil, wenn die Parasiten die Reproduktion der einheimischen Konkurrenten reduzieren. In der wissenschaftlichen Literatur gibt es zahlreiche Hinweise, dass Mikrosporidien die Fruchtbarkeit oder andere Parameter in den infizierten Wirten beeinträchtigen können [11].…”

“…In allen haben wir Mikrosporidien gefunden, was den Schluss nahelegt, dass sich die Assoziation zwischen H. axyridis und diesen Parasiten bereits in seinem ursprünglichen Verbreitungsgebiet ausgebildet hat [11]. Obwohl die Mikrosporidien in hohen Konzentrationen in der Hämolymphe von H. axyridis-Käfern vorkommen, wurden diese Parasiten offenbar bisher von Wissenschaftlern übersehen.…”

The infection of Harmonia axyridis by a parasitic nematode is mediated by entomopathogenic bacteria and triggers sex-specific host immune responses

“…Harmonine and AMPs display synergistic antimicrobial activity with c-type lysozymes 16 . The superior immune system of H. axyridis may also enable this host to carry the parasitic microsporidia described above, and to use them as biological weapons against competing ladybird species without suffering their effects directly 5 , 6 , 17 , 18 . We recently demonstrated that invasive and non-invasive populations of H. axyridis show distinct expression profiles of certain AMPs and confirmed the important protective role of one specific coleoptericin in the invasive populations, which suggests that rapidly-changing gene expression profiles in H. axyridis populations can promote pathogen resistance and thereby their invasive performance 19 .…”