Post-Miocene expansion, colonization, and host switching drove speciation among extant nematodes of the archaic genus Trichinella

Abstract

Parasitic nematodes of the genus Trichinella cause significant food-borne illness and occupy a unique evolutionary position at the base of the phylum Nematoda, unlike the free-living nematode Caenorhabditis elegans. Although the forthcoming genome sequence of Trichinella spiralis can provide invaluable comparative information about nematode biology, a basic framework for understanding the history of the genus Trichinella is needed to maximize its utility. We therefore developed the first robust and comprehensive analysis of the phylogeny and biogeographic history of Trichinella using the variation in three genes (nuclear small-subunit rDNA, and second internal transcribed spacer, mitochondrial large-subunit rDNA, and cytochrome oxidase I DNA) from all 11 recognized taxa. We conclude that (i) although Trichinellidae may have diverged from their closest extant relatives during the Paleozoic, all contemporary species of Trichinella diversified within the last 20 million years through geographic colonization and pervasive host switching among foraging guilds of obligate carnivores; (ii) mammalian carnivores disseminated encapsulated forms from Eurasia to Africa during the late Miocene and Pliocene, and to the Nearctic across the Bering Land Bridge during the Pliocene and Pleistocene, when crown species ultimately diversified; (iii) the greatest risk to human health is posed by those species retaining an ancestral capacity to parasitize a wide range of hosts; and (iv) early hominids may have first acquired Trichinella on the African savannah several million years before swine domestication as their diets shifted from herbivory to facultative carnivory.

Fig. 1.

Midpoint rooted minimum evolution trees reconstructed from all known encapsulated (red) and nonencapsulated (green) species and genotypes of Trichinella based on the variation in mitochondrial LSU and COI DNA (on the left) and SSU rDNA (on the right). Topological support is indicated by Bayesian posterior probabilities and by ML, minimum evolution (using ML distances), and parsimony bootstrap replicate analyses (B/ML/ME/P). Bootstrap support was reconstructed from 100-bp replicates.

Fig. 2.

Host associations and primary traits for the life history of Trichinella during diversification. Emphasized are shifts in patterns of transmission from omnivorous to carnivorous hosts, adaptations to changes in environmental temperatures, and retention of plesiomorphic traits among members of the nonencapsulated clade (green). Genotype abbreviations are consistent with Table 3.

Fig. 3.

Historical biogeography for species of the encapsulated clade of Trichinella. The cladogram for species of Trichinella has been mapped onto a global projection for range expansion. Subsequent to origins in Eurasia, Trichinella became distributed with its carnivorous hosts in Africa, broadly in the Palearctic, and later into the Nearctic. Emphasized is the role for independent events of biotic expansion and geographic colonization into Africa (Miocene/Pliocene/Pleistocene) and through Beringia into the Nearctic (Quaternary) as drivers for speciation. Genotype abbreviations are consistent with Table 3.