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Cryptic Intermediate Snail Host of the Liver Fluke Fasciola Hepatica in Africa

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Cryptic Intermediate Snail Host of the Liver Fluke Fasciola Hepatica in Africa View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by LSTM Online Archive Mahulu et al. Parasites Vectors (2019) 12:573 https://doi.org/10.1186/s13071-019-3825-9 Parasites & Vectors RESEARCH Open Access Cryptic intermediate snail host of the liver fuke Fasciola hepatica in Africa Anna Mahulu1, Catharina Clewing1, Björn Stelbrink1,2, Fred D. Chibwana1,3, Immaculate Tumwebaze1, J. Russell Stothard4 and Christian Albrecht1,5* Abstract Background: Snails such as Galba truncatula are hosts for trematode fukes causing fascioliasis, a zoonosis that is a major public health problem. Galba truncatula has recently been shown to be a cryptic species complex. African populations of Galba spp. are not yet studied using molecular assessments and is imperative to do so and reconstruct the centre of origin of Galba and to understand when and by what means it may have colonized the highlands of Africa and to what extent humans might have been involved in that process. Methods: Samples from all known sub-ranges throughout Africa and new samples from Europe and Asia were obtained. We used a combination of two mitochondrial (cox1 and 16S) and one nuclear (ITS2) markers and phyloge- netic, divergence time estimates and phylogeographical methods to determine the identity and biogeographical afnities. We also reconstructed the colonization history including the likely mode of dispersal and tested for the pres- ence of cryptic Galba species in Africa. Results: Galba truncatula is restricted to the Palaearctic region of the continent, namely Morocco. All sub-Saharan populations proved to be a distinct species according to the phylogenetic analyses and genetic distance. We propose to use the existing name Galba mweruensis (Connolly, 1929) for this species which is morphologically indistinguish- able from the other two species hitherto known to occur in northern Africa, i.e. G. truncatula and G. schirazensis. Sub-tropical Africa has been colonized only once in either the Pliocene and possibly Miocene. Diversifcation within G. mweruensis is dated to the Plio-Pleistocene and thus human-mediated dispersal can be ruled out for the initial coloni- zation of the isolated mountain ranges. There are potentially even more cryptic species in high altitude areas of Africa as outlined by the distinctness of the population found at the top of Mt. Elgon, Uganda. Conclusions: From a novel genetic inspection of available African material, a hitherto neglected distinct species, G. mweruensis, now appears a major host of F. hepatica throughout sub-Saharan Africa. A closer examination of trema- tode parasites hosted by this species is needed in order to understand transmission patterns in highlands throughout eastern and southern Africa. We encourage future studies to inspect other high altitudes areas in Africa in light of parasites of either veterinary or medical importance. Keywords: Fascioliasis, Medical malacology, Cryptic species, Galba truncatula, Lymnaeidae, Dispersal, Islands-in-the- sky Background economic damage. Indeed, fascioliasis, a very debilitat- Parasitic disease caused by the liver fukes of the genus ing snail-borne disease, is widespread across the globe; Fasciola afects hundreds of millions of people and live- however, in the subtropical/cooler regions it is caused stock worldwide. Collectively, they cause considerable by Fasciola hepatica [1] whereas in the tropical/warmer regions is caused by Fasciola gigantica [2]. *Correspondence: [email protected] To complete the life-cycle, the two species of liver 1 Department of Animal Ecology and Systematics, Justus Liebig University fuke are tied to a variety of intermediate freshwater Giessen, Giessen, Germany Full list of author information is available at the end of the article pulmonate snail hosts of the family Lymnaeidae [3]. © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Mahulu et al. Parasites Vectors (2019) 12:573 Page 2 of 11 Until relatively recently, the taxonomy of snails was Despite the variety of applicable molecular diagnostic consolidated to a single genus Lymnaea with remark- markers, there is a signifcant gap of knowledge about able morphological diversity; however, with application snails referred to as G. truncatula on the African conti- of molecular phylogenetics a multi-generic nomencla- nent. Here, the Galba truncatula-like snails have a dis- ture has become favoured with Galba and Radix now junct distribution with four largely isolated sub-ranges: in used in preference [4]. In Africa, for example, Galba the mountainous parts of the Maghreb states in northern truncatula (also known as Lymnaea truncatula) is Africa [18], the highlands of Ethiopia [19], some highland involved in the transmission of F. hepatica while Radix areas in East Africa such as Mt. Elgon [20], Usambara Mt. natalensis is involved in the transmission of F. gigantica [21], the Kitulo Plateau [22], the highlands of Lesotho with any epidemiological cross-over considered to be [23], and temperate coastal, i.e. cooler, regions of South rare [4]. As an intermediate host of F. hepatica, the liver Africa [24]. fuke largely responsible for human disease, G. trunca- When compared to the other native lymnaeid spe- tula is characterized by its amphibious lifestyle, adap- cies in Africa, such as Radix natalensis the main host tation to cooler habitats, and its ability to withstand of Fasciola gigantica, the distribution pattern of what drought events and other harsh environmental condi- is considered G. truncatula is particularly striking tions in unstable waterbodies [5]. It has been found in (Fig. 1) being confined to allopatry in higher altitudes high altitudes in South America, where it can reach up [20]. The discontinuous range of G. truncatula has to 4100 m [6] and it is thus among the few gastropods been hypothesized to be the result of passive disper- reaching extreme habitats on high elevations [7]. sal by migratory birds, being more likely perhaps than Te taxonomy of lymnaeid gastropods continues to be an alternative of much longer historical associations debated [4, 8], but recent molecular phylogenetic stud- with geological vicariance of uplifted African high ies improved the understanding of the evolution of this highlands [25]. Given scattered subfossil records in major freshwater gastropod family [3, 9–11]. Te species the Sahara, the Near East and Namibia [21], this could G. truncatula has been treated as belonging to Lymnaea represent a range of ancestral or relic habitats isolated and Fossaria in North America and is thus a prime exam- for eons. Another possibility would be a human- or ple of taxonomic confusion in lymnaeid systematics. livestock-mediated introduction, given the well-recog- Galba truncatula as the type-species of the genus is con- nized anthropophily of the species [26]. In fact, histor- ceived to be mainly a Holarctic species [12], with a wide ical records in the eastern part of the DR Congo have distribution range throughout North America and Eura- been attributed to human introductions [13]. Records sia, where it reaches as far as India [13]. Te scattered of the Nile Delta in Egypt recently turned out to repre- occurrences in South America have been interpreted as sent populations of Lymnaea schirazensis [27] and thus recent introductions [14]. However, the real extent of the raise questions as to a potential camouflaged invasion distribution of G. truncatula on a global scale is poten- in other parts of the continent. The only populations tially masked by the occurrence of cryptic species that of Galba spp. that were identified by molecular DNA are morphologically indistinguishable from G. trunca- to be G. truncatula inhabited Mt. Elgon [20] and the tula. Among these species are Lymnaea cubensis [15] and Kitulo Plateau in southern Tanzania [22]. Both studies, Lymnaea schirazensis, two species that have been previ- however, used short fragments of the highly conserva- ously confused with G. truncatula prior to the introduc- tive nuclear ribosomal 18S gene. Whereas, this genetic tion of molecular methods of characterisation. Such a marker is sufficient to delimit Galba spp. from Radix confusing situation has important implications to para- natalensis, it is not suitable for intra-generic stud- site transmission and epidemiology because the cryptic ies. Given this situation, it remains currently unclear species may difer in their competence for transmission whether the high-altitude African populations of of F. hepatica. Galba spp. indeed represent Galba truncatula. More- Given the importance of these species for veterinary over, it is unknown how these populations are related and human parasitology, a number of attempts have been to populations in Europe, Asia and the Americas. Due made to identify species based on molecular markers. As to the complete absence of molecular assessments (but a result, a relatively rich record of sequences of several see [22]) it is, to date, impossible to reconstruct the mitochondrial and nuclear molecular markers is available centre of origin of Galba spp. and to understand when for comparative analyses of material studied recently [3]. and by what means Galba spp. may have colonized On the population level, SNPs [16] and microsatellites Africa and to what extent humans might have been have been published [17]. A recent study proposed an involved in that process. easy and inexpensive PCR-based approach to distinguish To shed new light on the phylogeography of Galba among three cryptic Galba species [15]. spp. populations, and its impact on snail-borne Mahulu et al.
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