Abstract
Insects are an important model for the study of innate immune systems, but remarkably little is known about the immune system of other arthropod groups despite their importance as disease vectors, pests, and components of biological diversity. Using comparative genomics, we have characterized the immune system of all the major groups of arthropods beyond insects for the first time—studying five chelicerates, a myriapod, and a crustacean. We found clear traces of an ancient origin of innate immunity, with some arthropods having Toll-like receptors and C3-complement factors that are more closely related in sequence or structure to vertebrates than other arthropods. Across the arthropods some components of the immune system, such as the Toll signaling pathway, are highly conserved. However, there is also remarkable diversity. The chelicerates apparently lack the Imd signaling pathway and beta-1,3 glucan binding proteins—a key class of pathogen recognition receptors. Many genes have large copy number variation across species, and this may sometimes be accompanied by changes in function. For example, we find that peptidoglycan recognition proteins have frequently lost their catalytic activity and switch between secreted and intracellular forms. We also find that there has been widespread and extensive duplication of the cellular immune receptor Dscam (Down syndrome cell adhesion molecule), which may be an alternative way to generate the high diversity produced by alternative splicing in insects. In the antiviral short interfering RNAi pathway Argonaute 2 evolves rapidly and is frequently duplicated, with a highly variable copy number. Our results provide a detailed analysis of the immune systems of several important groups of animals for the first time and lay the foundations for functional work on these groups.
Highlights
All animals must defend themselves against a battery of natural enemies, ranging from pathogens such as viruses, bacteria and fungi, to macroscopic parasites such as parasitic worms or insects
To investigate the evolution and origins of the arthropod innate immune system, we identified homologs of insect immunity genes in species that diverged early in the evolution of the arthropods
In our analysis we included the genomes of the insect Drosophila melanogaster, the crustacean Daphnia pulex, the myriapod Strigamia maritima and five species of chelicerate: Mesobuthus martensii (Chinese scorpion) (Cao et al 2013), Parasteatoda tepidariorum, Ixodes scapularis, Metaseiulus occidentalis, and Tetranychus urticae (Grbicet al. 2011)
Summary
All animals must defend themselves against a battery of natural enemies, ranging from pathogens such as viruses, bacteria and fungi, to macroscopic parasites such as parasitic worms or insects. All the major groups of animals possess an innate immune system, where immune receptors are genetically hard-coded and the response is typically relatively nonspecific with respect to individual pathogen strains or previous exposure (Hoffmann et al 1999; Kimbrell and Beutler 2001). In addition to an innate immune system, vertebrates possess an adaptive or acquired immune system, where receptor diversity is generated somatically and there is immunological memory (Hoffmann et al 1999; Kimbrell and Beutler 2001; Hoffmann and Reichhart 2002; Janeway and Medzhitov 2002; Smith et al 2011). Key components of the adaptive immune system are not found much beyond vertebrates (So€derha€ll 2011), some invertebrates have independently evolved both immune memory and mechanisms to generate receptor diversity somatically (Zhang et al 2004; Kurtz 2005)
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