Paleobiogeographical origins of Fasciola hepatica and F. gigantica in light of new DNA sequence characteristics of F. nyanzae from hippopotamus

Abstract

Fascioliasis is a highly pathogenic disease affecting humans and livestock worldwide. It is caused by the liver flukesFasciola hepaticatransmitted byGalba/Fossarialymnaeid snails in Europe, Asia, Africa, the Americas and Oceania, andF. giganticatransmitted byRadixlymnaeids in Africa and Asia. An evident founder effect appears in genetic studies as the consequence of their spread by human-guided movements of domestic ruminants, equines and Old World camelids in the post-domestication period from the beginning of the Neolithic. Establishing the geographical origins of fasciolid expansion is multidisciplinary crucial for disease assessment. Sequencing of selected nuclear ribosomal and mitochondrial DNA markers ofF. nyanzaeinfecting hippopotamuses (Hippopotamus amphibius) in South Africa and their comparative analyses withF. hepaticaandF. gigantica, and the twoFascioloidesspecies,Fs. jacksonifrom Asian elephants andFs. magnafrom Holarctic cervids, allow to draw a tuned-up evolutionary scenario during the pre-domestication period. Close sequence similarities indicate a direct derivation ofF. hepaticaandF. giganticafromF. nyanzaeby speciation after host capture phenomena. Phylogenetic reconstruction, genetic distances and divergence estimates fully fit fossil knowledge, past interconnecting bridges between continents, present fasciolid infection in the wild fauna, and lymnaeid distribution. The paleobiogeographical analyses suggest an origin forF. giganticaby transfer from primitive hippopotamuses to grazing bovid ancestors of Reduncinae, Bovinae and Alcelaphinae, by keeping the same vectorRadix natalensisin warm lowlands of southeastern Africa in the mid-Miocene, around 13.5 mya. The origin ofF. hepaticashould have occurred after capture from primitive, less amphibiousHexaprotodonhippopotamuses to mid-sized ovicaprines as the wild bezoarCapra aegagrusand the wild mouflonOvis gmelini, and fromR. natalensistoGalba truncatulain cooler areas and mountainous foothills of Asian Near East in the latest Miocene to Early Pliocene, around 6.0 to 4.0 mya and perhaps shortly afterwards.