Invertebrates versus Vertebrates Innate Immunity: In the Light of Evolution (‘Nothing in biology makes sense except in the light of evolution’ T. Dobzhansky, Amer Biol Teacher 1973;35:125–9)

Abstract

Invertebrates use a nonadaptive, innate immunity, the expression of germline encoded receptors, to identify the allogeneic and xenogeneic attributes. Vertebrates also have the capacity to express ontogenically related adaptive immunity which is a somatically selected gene rearrangement process. Several commonly accepted generalizations are utilized to explain the enigmatic lack of the adaptive immunity in invertebrates. All point to the primitive nature of the innate immunity and the primitive organization of the body plan and the life history patterns of invertebrates. Seven of the most common generalizations are reviewed and confuted by virtue of a biased literature presentation. Subsequently, three evolutionary puzzles are raised and the accepted paradigm that the vertebrate immunity is pathogenically directed is further challenged. This leads to an alternative idea suggesting that preserving the individuality against the threat of invading conspecific cells might have been the original function of the immune system. This ancient system has been co‐opted later on to serve as a defence mechanism against pathogens. The secondary role arose in the form of a multiplicity of newly developed phenomena, one of them being the vertebrate adaptive immunity. This proposal is supported by the fact that vertebrates still exhibit two distinct but common types of naturally occurring transplantation events (natural chimerism) and by a variety of recent studies, providing evidence for the crucial role of the vertebrate's innate immunity in signalling and triggering the acquired effector mechanisms.