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.biogeography ͉ mitochondrial DNA ͉ phylogeny ͉ ribosomal DNA E xceptional biological diversity among nematodes is exemplified by certain attributes of the parasite Trichinella spiralis. Organization of its mitochondrial genome more closely resembles that of coelomate metazoans than that of its presumed closest relatives, the secernentean nematodes (1). In addition, T. spiralis (Dorylaimia) shares a similar proportion (45%) of its ESTs with the nematode Caenorhabditis elegans (Rhabditina) as it does with the fruit fly Drosophila melanogaster (Arthropoda: Drosophilidae) (2). Thus, many ESTs common to T. spiralis and C. elegans are not necessarily specific to nematodes but may be conserved among diverse taxonomic groups of invertebrates. C. elegans is often thought of as a prototypical nematode because of its acceptance as a model for studying biological processes; however, genomic variation among nematodes is extensive and commensurate with their phylogenetic and ecological diversity. Therefore, the forthcoming genome sequence of T. spiralis will contribute substantially to our understanding of nematode biology and the origins of parasitism.In 1998, Blaxter et al. (3) used genetic data to delineate the phylum Nematoda into supertaxa consisting of five clades. Trichinella, a parasite of vertebrates, occupies a basal lineage (clade I) consisting of free-living Mononchida, ...

The Beringian Coevolution Project: holistic collections of mammals and associated parasites reveal novel perspectives on evolutionary and environmental change in the North

“…For example, assemblages of Trichinella nematodes that circulate through carnivory or scavenging by various mammals (e.g., carnivores, suids, and rodents) provide insights into colonization processes from Eurasia through the Nearctic and extending into the tropics (e.g., Pozio et al 2009;Korhonen et al 2016). The clade of "encapsulated" Trichinella initially diversified in central Eurasia with subsequent history dominated by sequential events of geographic and host colonization that account for the distribution of nine recognized species (Zarlenga et al 2006). A single species, T. patagoniensis, is endemic to southern South America among small felids that radiated near 8 MYBP (Johnson et al 2006).…”

Species-Specific Antibody Responses to the Recombinant 53-Kilodalton Excretory and Secretory Proteins in Mice Infected withTrichinellaspp

“…To date, two clades in the genus Trichinella have been identified: the encapsulated clade and the nonencapsulated clade (26). Muscle larvae in encapsulated species develop a thick collagen capsule, and the nonencapsulated species develop only a very thin collagen capsule (23).…”

“…Eight species (i.e., T. spiralis, T. britovi, T. nativa, T. murrelli, T. nelsoni, T. pseudospiralis, T. papuae, and T. zimbabwensis) and three genotypes (i.e., Trichinella T6, T8, and T9) have all been identified in the genus Trichinella, to date (26). Only five species in the genus Trichinella were observed for speciesspecific antibody responses to the 53-kDa recombinant proteins.…”

Parasitic nematodes—From genomes to control

“…Other than for the few successes in vaccinating against cestodes (Gauci et al, 2005;Lightowlers, 2004), development of recombinant antigens for control of veterinary parasites has been limited (Zarlenga, 2004). This may, in part, reflect the key roles that coevolution and adaptation have played in the hostparasite relationship (Zarlenga et al, 2006). Parasites often secrete or excrete products that regulate the local immune environment.…”