Independent origins of parasitism in Animalia

Abstract

Nearly half of all animals may have a parasitic lifestyle, yet the number of transitions to parasitism and their potential for species diversification remain unresolved. Based on a comprehensive survey of the animal kingdom, we find that parasitism has independently evolved at least 223 times in just 15 phyla, with the majority of identified independent parasitic groups occurring in the Arthropoda, at or below the level of Family. Metazoan parasitology is dominated by the study of helminthes; however, only 20% of independently derived parasite taxa belong to those groups, with numerous transitions also seen in Mollusca, Rotifera, Annelida and Cnidaria. Parasitism is almost entirely absent from deuterostomes, and although worm-like morphology and host associations are widespread across Animalia, the dual symbiotic and trophic interactions required for parasitism may constrain its evolution from antecedent consumer strategies such as generalist predators and filter feeders. In general, parasitic groups do not differ from their free-living relatives in their potential for speciation. However, the 10 largest parasitic clades contain 90% of described parasitic species, or perhaps 40% of all animal species. Hence, a substantial fraction of animal diversity on the Earth arose following these few transitions to a parasitic trophic strategy.

Keywords: adaptive radiation; metazoan; parasite evolution; parasitism.

Figure 1.

Origins of parasitism across Animalia. Bar plot of the natural log transformed number of independent acquisitions of parasitism within Metazoa, Arthropoda and Insecta, arranged according to taxonomic affiliation [–21]. Bar shading denotes the per cent of the group that is parasitic and bar width is proportional to the log₁₀₀₀ transformed number of species per group. D, Deuterostomia; Pr, Protostomia; L, Lophotrochozoa; E, Ecdysozoa; Ch, Chelicerata; Cr, Crustacea; He, Hexapoda; Pa, Palaeoptera; Po, Polyneoptera; Co, Condylognatha; Ho, Holometabola.

Figure 2.

Plot of sister group pairs. Each point represents a single parasite/non-parasite pair with the number of free-living species as the x-coordinate and the number of parasite species as the y. The line represents a one-to-one relationship such that pairs with an equal number of free-living and parasite species are plotted on the line. (Online version in colour.)