Whipworms in humans and pigs: origins and demography

TY - JOUR

T1 - Whipworms in humans and pigs

T2 - origins and demography

AU - Hawash, Mohamed Bayoumi Fahmy

AU - Betson, Martha

AU - Al-Jubury, Azmi

AU - Ketzis, Jennifer

AU - LeeWillingham, Arve

AU - Bertelsen, Mads Frost

AU - Cooper, Philip J.

AU - Littlewood, D. Tim. J.

AU - Zhu, Xing-Quan

AU - Nejsum, Peter

PY - 2016/1/22

Y1 - 2016/1/22

N2 - BACKGROUND: Trichuris suis and T. trichiura are two different whipworm species that infect pigs and humans, respectively. T. suis is found in pigs worldwide while T. trichiura is responsible for nearly 460 million infections in people, mainly in areas of poor sanitation in tropical and subtropical areas. The evolutionary relationship and the historical factors responsible for this worldwide distribution are poorly understood. In this study, we aimed to reconstruct the demographic history of Trichuris in humans and pigs, the evolutionary origin of Trichuris in these hosts and factors responsible for parasite dispersal globally.METHODS: Parts of the mitochondrial nad1 and rrnL genes were sequenced followed by population genetic and phylogenetic analyses. Populations of Trichuris examined were recovered from humans (n = 31), pigs (n = 58) and non-human primates (n = 49) in different countries on different continents, namely Denmark, USA, Uganda, Ecuador, China and St. Kitts (Caribbean). Additional sequences available from GenBank were incorporated into the analyses.RESULTS: We found no differentiation between human-derived Trichuris in Uganda and the majority of the Trichuris samples from non-human primates suggesting a common African origin of the parasite, which then was transmitted to Asia and further to South America. On the other hand, there was no differentiation between pig-derived Trichuris from Europe and the New World suggesting dispersal relates to human activities by transporting pigs and their parasites through colonisation and trade. Evidence for recent pig transport from China to Ecuador and from Europe to Uganda was also observed from their parasites. In contrast, there was high genetic differentiation between the pig Trichuris in Denmark and China in concordance with the host genetics.CONCLUSIONS: We found evidence for an African origin of T. trichiura which were then transmitted with human ancestors to Asia and further to South America. A host shift to pigs may have occurred in Asia from where T. suis seems to have been transmitted globally by a combination of natural host dispersal and anthropogenic factors.

AB - BACKGROUND: Trichuris suis and T. trichiura are two different whipworm species that infect pigs and humans, respectively. T. suis is found in pigs worldwide while T. trichiura is responsible for nearly 460 million infections in people, mainly in areas of poor sanitation in tropical and subtropical areas. The evolutionary relationship and the historical factors responsible for this worldwide distribution are poorly understood. In this study, we aimed to reconstruct the demographic history of Trichuris in humans and pigs, the evolutionary origin of Trichuris in these hosts and factors responsible for parasite dispersal globally.METHODS: Parts of the mitochondrial nad1 and rrnL genes were sequenced followed by population genetic and phylogenetic analyses. Populations of Trichuris examined were recovered from humans (n = 31), pigs (n = 58) and non-human primates (n = 49) in different countries on different continents, namely Denmark, USA, Uganda, Ecuador, China and St. Kitts (Caribbean). Additional sequences available from GenBank were incorporated into the analyses.RESULTS: We found no differentiation between human-derived Trichuris in Uganda and the majority of the Trichuris samples from non-human primates suggesting a common African origin of the parasite, which then was transmitted to Asia and further to South America. On the other hand, there was no differentiation between pig-derived Trichuris from Europe and the New World suggesting dispersal relates to human activities by transporting pigs and their parasites through colonisation and trade. Evidence for recent pig transport from China to Ecuador and from Europe to Uganda was also observed from their parasites. In contrast, there was high genetic differentiation between the pig Trichuris in Denmark and China in concordance with the host genetics.CONCLUSIONS: We found evidence for an African origin of T. trichiura which were then transmitted with human ancestors to Asia and further to South America. A host shift to pigs may have occurred in Asia from where T. suis seems to have been transmitted globally by a combination of natural host dispersal and anthropogenic factors.

KW - Whipworms

KW - Trichuris

KW - Humans

KW - Pigs

KW - Demographic history

KW - Evolution

U2 - 10.1186/s13071-016-1325-8

DO - 10.1186/s13071-016-1325-8

M3 - Journal article

C2 - 26800683

SN - 1756-3305

VL - 9

JO - Parasites & Vectors

JF - Parasites & Vectors

M1 - 37

ER -