Ancient horizontal transfers of retrotransposons between birds and ancestors of human pathogenic nematodes.
Parasite host switches may trigger disease emergence, but prehistoric host ranges are often unknowable. Lymphatic filariasis and loiasis are major human diseases caused by the insect-borne filarial nematodes Brugia, Wuchereria and Loa. Here we show that the genomes of these nematodes and seven tropical bird lineages exclusively share a novel retrotransposon, AviRTE, resulting from horizontal transfer (HT). AviRTE subfamilies exhibit 83-99% nucleotide identity between genomes, and their phylogenetic distribution, paleobiogeography and invasion times suggest that HTs involved filarial nematodes. The HTs between bird and nematode genomes took place in two pantropical waves, >25-22 million years ago (Myr ago) involving the Brugia/Wuchereria lineage and >20-17 Myr ago involving the Loa lineage. Contrary to the expectation from the mammal-dominated host range of filarial nematodes, we hypothesize that these major human pathogens may have independently evolved from bird endoparasites that formerly infected the global breadth of avian biodiversity.
Department of Evolutionary Biology, Evolutionary Biology Centre (EBC), Uppsala University, SE-752 36 Uppsala, Sweden.
Alexander
A
Suh
Department of Biology and Museum of Southwestern Biology, University of New Mexico, Albuquerque, New Mexico 87131, USA.
Christopher C
CC
Witt
Department of Conservation Biology, Helmholtz Centre for Environmental Research (UFZ), D-04318 Leipzig, Germany.|Molecular Evolution and Systematics of Animals, Institute of Biology, University of Leipzig, D-04103 Leipzig, Germany.|Instituto Nacional de Pesquisas da Amazônia (INPA), AM 69067-375 Manaus, Brazil.
Juliana
J
Menger
Department of Biological Sciences, National University of Singapore, Singapore 117543, Singapore.
Keren R
KR
Sadanandan
Institute of Evolutionary Biology and Ecology, University of Bonn, D-53121 Bonn, Germany.
Lars
L
Podsiadlowski
Molecular Evolution and Systematics of Animals, Institute of Biology, University of Leipzig, D-04103 Leipzig, Germany.
Michael
M
Gerth
Molecular Evolution and Systematics of Animals, Institute of Biology, University of Leipzig, D-04103 Leipzig, Germany.|Max Planck Institute for Evolutionary Anthropology, D-04103 Leipzig, Germany.
Anne
A
Weigert
Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, Berkeley, California 94720, USA.
Jimmy A
JA
McGuire
National Center for Genome Resources, Santa Fe, New Mexico 87505, USA.
Joann
J
Mudge
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
Scott V
SV
Edwards
Department of Biological Sciences, National University of Singapore, Singapore 117543, Singapore.
Frank E
FE
Rheindt
D000818:Animals; D005075:Biological Evolution; D001715:Bird Diseases / Q000453:epidemiology / Q000266:history* / Q000469:parasitology / Q000635:transmission; D001717:Birds / Q000145:classification / Q000469:parasitology; D002009:Brugia / Q000145:classification / Q000235:genetics*; D004605:Elephantiasis, Filarial / Q000453:epidemiology / Q000266:history* / Q000469:parasitology / Q000635:transmission; D005368:Filariasis / Q000453:epidemiology / Q000266:history* / Q000469:parasitology / Q000635:transmission; D022761:Gene Transfer, Horizontal; D049690:History, Ancient; D006801:Humans; D008117:Loa / Q000145:classification / Q000235:genetics*; D008118:Loiasis / Q000453:epidemiology / Q000266:history* / Q000469:parasitology / Q000635:transmission; D010802:Phylogeny; D058974:Phylogeography; D018626:Retroelements; D014957:Wuchereria / Q000145:classification / Q000235:genetics*
D018626:Retroelements