Submitted to: Proceedings of the National Academy of Sciences
Publication Type: Peer reviewed journal
Publication Acceptance Date: 3/27/2006
Publication Date: 5/9/2006
Citation: Zarlenga, D.S., Rosenthal, B.M., La Rosa, G., Pozio, E., Hoberg, E.P. 2006. Post-miocene expansion, colonization and host switching drove speciation among extant nematodes of the archaic genus trichinella. Proceedings of the National Academy of Sciences. 103:7354-7359. Interpretive Summary: Speciation within the genus Trichinella remains a controversial issue. The dearth of information on speciation within this genus in conjunction with the availability of genetic material from all currently recognized genotypes, has prompted an extensive multi-gene study of the phylogeny as well as an evaluation of the biogeography and biohistory of this genus. Herein, we propose a reclassification of the genus based upon new molecular and biochemical data. Or data revealed the following previously unknown facts and hypotheses: 1)contrary to current dogma, all contemporary species of Trichinella diversified within the last 20 million years; 2) early man may have first come in contact with Trichinella when their diets shifted from herbivory to carnivory on the African Savannah and before his domestication of pigs; and 3) expansion and speciation of Trichinella into North America likely occurred across the Bering Land Bridge which in turn acted as the driver for separation of Nearctic and Palearctic genotypes. These findings will assist researchers in determining whether certain populations of this species are more infectious to humans than others, and provide a sound basis for interpreting impending genome sequence data to better understand the relation of this parasite group to other nematodes as well as the broad group of nematodes to all metazoan.
Technical 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 Caenorhabditis elegans model. 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 variation in three genes (nuclear SSU rDNA and ITS2; mitochondrial LSU rDNA and COI DNA) from all eleven recognized taxa. We conclude that: 1) 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 increasingly carnivorous, foraging guilds; 2) mammalian carnivores disseminated encapsulated forms from Eurasia to Africa during the late Miocene and Pliocene and to the Nearctic across Bering Land Bridge during the Pliocene and Pleistocene, when crown species ultimately diversified; 3) the greatest risk to human health is posed by those species retaining an ancestral capacity to parasitize a wide range of hosts; and 4) early hominids may first have acquired trichinellosis as their diet shifted from herbivory to facultative carnivory on the African Savannah several million years prior to swine domestication.