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A phylogeny for the pomatiopsidae (Gastropoda: Rissooidea): a resource for taxonomic, parasitological and biodiversity studies.

Liu L, Huo GN, He HB, Zhou B, Attwood SW - BMC Evol. Biol. (2014)

Bottom Line: Consequently, the aim of the study was to collect DNA-sequence data for as many pomatiopsid taxa as possible, as a first step in providing a resource for identification of epidemiologically significant species (by non-malacologists), for use in resolving taxonomic confusion and for testing phylogeographical hypotheses.The molecular dates and phylogenetic estimates in this study are consistent with an Australasian origin for the Pomatiopsidae and an East to West radiation via Oligocene Borneo-Philippines island hopping to Japan and then China (Triculinae arising mid-Miocene in Southeast China), and less so with a triculine origin in Tibet.The lack of monophyly in the medically important genera and indications of taxonomic inaccuracies, call for further work to identify epidemiologically significant taxa (e.g., Halewisia may be potential hosts for Schistosoma mekongi) and highlight the need for surveys to determine the true biodiversity of the Triculinae.

View Article: PubMed Central - HTML - PubMed

Affiliation: State Key Laboratory of Biotherapy, West China Hospital, West China Medical School, Sichuan University, 1 KeYuan 4 Lu, Chengdu, Sichuan 610041, People's Republic of China. swahuaxi@yahoo.com.

ABSTRACT

Background: The Pomatiopsidae are reported from northern India into southern China and Southeast Asia, with two sub-families, the Pomatiopsinae (which include freshwater, amphibious, terrestrial and marine species) and the freshwater Triculinae. Both include species acting as intermediate host for species of the blood-fluke Schistosoma which cause a public health problem in East Asia. Also, with around 120 species, triculine biodiversity exceeds that of any other endemic freshwater molluscan fauna. Nevertheless, the origins of the Pomatiopsidae, the factors driving such a diverse radiation and aspects of their co-evolution with Schistosoma are not fully understood. Many taxonomic questions remain; there are problems identifying medically relevant species. The predicted range is mostly unsurveyed and the true biodiversity of the family is underestimated. Consequently, the aim of the study was to collect DNA-sequence data for as many pomatiopsid taxa as possible, as a first step in providing a resource for identification of epidemiologically significant species (by non-malacologists), for use in resolving taxonomic confusion and for testing phylogeographical hypotheses.

Results: The evolutionary radiation of the Triculinae was shown to have been rapid and mostly post late Miocene. Molecular dating indicated that the radiation of these snails was driven first by the uplift of the Himalaya and onset of a monsoon system, and then by late-Pliocene global warming. The status of Erhaia as Anmicolidae is supported. The genera Tricula and Neotricula are shown to be non-monophyletic and the tribe Jullieniini may be polyphyletic (based on convergent characters). Triculinae from northern Vietnam could be derived from Gammatricula of Fujian/Yunnan, China.

Conclusions: The molecular dates and phylogenetic estimates in this study are consistent with an Australasian origin for the Pomatiopsidae and an East to West radiation via Oligocene Borneo-Philippines island hopping to Japan and then China (Triculinae arising mid-Miocene in Southeast China), and less so with a triculine origin in Tibet. The lack of monophyly in the medically important genera and indications of taxonomic inaccuracies, call for further work to identify epidemiologically significant taxa (e.g., Halewisia may be potential hosts for Schistosoma mekongi) and highlight the need for surveys to determine the true biodiversity of the Triculinae.

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Summary of alternative phylogeographies for the Pomatiopsidae. Semi-schematic showing alternative hypotheses for the origins and evolutionary radiation of the Pomatiopsidae. A. Tibet hypothesis: The ancestor of the Pomatiopsidae arises in Gondwana and is rafted on the Indian Craton after the break up of the super continent. These taxa are then introduced to China via Tibet after the collision between India (or earlier Cimmerian blocks) and Asia (150–120 Ma). The Pomatiopsinae and Triculinae then diverge in the Yangtze and Mekong river systems as these cut their way southwards to the sea [10]. B. Hunan (East to West) hypothesis, as proposed by Attwood (2009) [9]: Proto-Pomatiopsinae diverge in Australasia, with marine forms developing and colonizing South Africa and South America. Precursors of Oncomelania colonize northwards along island chains created by low sea levels and by tectonic movements (rafting). After reaching Japan, Proto-Oncomelania gives rise to the Japanese Pomtiopsinae and Oncomelania hupensis; the latter colonizes China and back-tracks (grey stippled arrow) to recolonize the Philippines and Sulawesi (replacing antecedent forms). The Triculinae arise in Southwest China and diverge in uplifting mountain areas. Dates are from the present analyses. Approximate distributions of major formations of calcareous rocks are shown as shaded areas. Coastlines are rough approximations for 15–10 Ma, drawing from the palaeogeographical literature [31-39].
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Figure 2: Summary of alternative phylogeographies for the Pomatiopsidae. Semi-schematic showing alternative hypotheses for the origins and evolutionary radiation of the Pomatiopsidae. A. Tibet hypothesis: The ancestor of the Pomatiopsidae arises in Gondwana and is rafted on the Indian Craton after the break up of the super continent. These taxa are then introduced to China via Tibet after the collision between India (or earlier Cimmerian blocks) and Asia (150–120 Ma). The Pomatiopsinae and Triculinae then diverge in the Yangtze and Mekong river systems as these cut their way southwards to the sea [10]. B. Hunan (East to West) hypothesis, as proposed by Attwood (2009) [9]: Proto-Pomatiopsinae diverge in Australasia, with marine forms developing and colonizing South Africa and South America. Precursors of Oncomelania colonize northwards along island chains created by low sea levels and by tectonic movements (rafting). After reaching Japan, Proto-Oncomelania gives rise to the Japanese Pomtiopsinae and Oncomelania hupensis; the latter colonizes China and back-tracks (grey stippled arrow) to recolonize the Philippines and Sulawesi (replacing antecedent forms). The Triculinae arise in Southwest China and diverge in uplifting mountain areas. Dates are from the present analyses. Approximate distributions of major formations of calcareous rocks are shown as shaded areas. Coastlines are rough approximations for 15–10 Ma, drawing from the palaeogeographical literature [31-39].

Mentions: Differing hypotheses have been put forward to explain the origins, radiation and current biodiversity and deployment of the Pomatiopsidae (Figure 2). Davis [10] proposed a Gondwanan origin for the Pomatiopsidae, with rafting to mainland Asia (via the Indian Craton after the break up of Gondwana) and colonization of Southeast Asia and China (Tibet/Yunnan) via the northern India-Myanmar, Brahmaputra-Irrawaddy river corridor during the mid to late Miocene. The drivingforce behind the radiation of the Triculinae was attributed to the opening up of new habitats along the extending courses of the main rivers of Asia, following their inception at the collision of India and Asia, and the uplift of the Tibetan Plateau. The origin of the Triculinae was located in the highlands of Tibet and Yunnan and dated at around 18 Ma (megaannum or million years). The Gondwana-Indian origin would predict Pomatiopsidae in India and Myanmar/Bangladesh; however, no pomatiopsids have been verified in that region. Species cited from the region, such as Tricula horae, T. martini, T. taylori (Myanmar), and even the type species of the genus itself, Tricula montana (India) are known only from poorly described, single collections, made decades ago, the identification of which has long been controversial [40]. Indeed many of these taxa more resemble Oncomelania than Tricula, but it is the distribution of the Triculinae which is key because triculine snails show much poorer dispersal capabilities. Recent reports of Tricula from Nepal (e.g., Tricula godawariensis Nesemann & Sharma 2007) [41] are simlarly data deficient, with descriptions of new taxa based on shell characters only – as noted by Davis [42], one cannot distinguish these taxa on the basis of shell and radula characters alone. Under this hypothesis the Pomatiopsinae diverge in the Yangtze river drainage and the Triculinae into the Mekong river drainage; this major separation dated mid-Miocene (18 Ma). Oncomelania was assumed to have colonized Japan and the Philippines from China, with the radiation into several species of terrestrial Pomatiopsinae in Japan being driven by Miocene tectonic upheaval [10]. The lack of divergence among the other Pomatiopsinae (e.g., Tomichia with limited geographical or habitat range and few species having evolved over 80 Ma; see Figure 1) is explained by environmental stability [43]. Nevertheless, such a lack of radiation in southern continentally distributed pomatiopsines over 80 Ma compared with the extensive radiation of the Japanese taxa over 23–5 Ma is not easy to accept, and also the lack of radiation on the tectonically active Philippines (only one sub species of O. hupensis is found there) requires explanation. The phylogeny, dispersal tracts and time markers associated with this hypotheses are summarized in Table 1 and Figures 2 and 3A.


A phylogeny for the pomatiopsidae (Gastropoda: Rissooidea): a resource for taxonomic, parasitological and biodiversity studies.

Liu L, Huo GN, He HB, Zhou B, Attwood SW - BMC Evol. Biol. (2014)

Summary of alternative phylogeographies for the Pomatiopsidae. Semi-schematic showing alternative hypotheses for the origins and evolutionary radiation of the Pomatiopsidae. A. Tibet hypothesis: The ancestor of the Pomatiopsidae arises in Gondwana and is rafted on the Indian Craton after the break up of the super continent. These taxa are then introduced to China via Tibet after the collision between India (or earlier Cimmerian blocks) and Asia (150–120 Ma). The Pomatiopsinae and Triculinae then diverge in the Yangtze and Mekong river systems as these cut their way southwards to the sea [10]. B. Hunan (East to West) hypothesis, as proposed by Attwood (2009) [9]: Proto-Pomatiopsinae diverge in Australasia, with marine forms developing and colonizing South Africa and South America. Precursors of Oncomelania colonize northwards along island chains created by low sea levels and by tectonic movements (rafting). After reaching Japan, Proto-Oncomelania gives rise to the Japanese Pomtiopsinae and Oncomelania hupensis; the latter colonizes China and back-tracks (grey stippled arrow) to recolonize the Philippines and Sulawesi (replacing antecedent forms). The Triculinae arise in Southwest China and diverge in uplifting mountain areas. Dates are from the present analyses. Approximate distributions of major formations of calcareous rocks are shown as shaded areas. Coastlines are rough approximations for 15–10 Ma, drawing from the palaeogeographical literature [31-39].
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4016560&req=5

Figure 2: Summary of alternative phylogeographies for the Pomatiopsidae. Semi-schematic showing alternative hypotheses for the origins and evolutionary radiation of the Pomatiopsidae. A. Tibet hypothesis: The ancestor of the Pomatiopsidae arises in Gondwana and is rafted on the Indian Craton after the break up of the super continent. These taxa are then introduced to China via Tibet after the collision between India (or earlier Cimmerian blocks) and Asia (150–120 Ma). The Pomatiopsinae and Triculinae then diverge in the Yangtze and Mekong river systems as these cut their way southwards to the sea [10]. B. Hunan (East to West) hypothesis, as proposed by Attwood (2009) [9]: Proto-Pomatiopsinae diverge in Australasia, with marine forms developing and colonizing South Africa and South America. Precursors of Oncomelania colonize northwards along island chains created by low sea levels and by tectonic movements (rafting). After reaching Japan, Proto-Oncomelania gives rise to the Japanese Pomtiopsinae and Oncomelania hupensis; the latter colonizes China and back-tracks (grey stippled arrow) to recolonize the Philippines and Sulawesi (replacing antecedent forms). The Triculinae arise in Southwest China and diverge in uplifting mountain areas. Dates are from the present analyses. Approximate distributions of major formations of calcareous rocks are shown as shaded areas. Coastlines are rough approximations for 15–10 Ma, drawing from the palaeogeographical literature [31-39].
Mentions: Differing hypotheses have been put forward to explain the origins, radiation and current biodiversity and deployment of the Pomatiopsidae (Figure 2). Davis [10] proposed a Gondwanan origin for the Pomatiopsidae, with rafting to mainland Asia (via the Indian Craton after the break up of Gondwana) and colonization of Southeast Asia and China (Tibet/Yunnan) via the northern India-Myanmar, Brahmaputra-Irrawaddy river corridor during the mid to late Miocene. The drivingforce behind the radiation of the Triculinae was attributed to the opening up of new habitats along the extending courses of the main rivers of Asia, following their inception at the collision of India and Asia, and the uplift of the Tibetan Plateau. The origin of the Triculinae was located in the highlands of Tibet and Yunnan and dated at around 18 Ma (megaannum or million years). The Gondwana-Indian origin would predict Pomatiopsidae in India and Myanmar/Bangladesh; however, no pomatiopsids have been verified in that region. Species cited from the region, such as Tricula horae, T. martini, T. taylori (Myanmar), and even the type species of the genus itself, Tricula montana (India) are known only from poorly described, single collections, made decades ago, the identification of which has long been controversial [40]. Indeed many of these taxa more resemble Oncomelania than Tricula, but it is the distribution of the Triculinae which is key because triculine snails show much poorer dispersal capabilities. Recent reports of Tricula from Nepal (e.g., Tricula godawariensis Nesemann & Sharma 2007) [41] are simlarly data deficient, with descriptions of new taxa based on shell characters only – as noted by Davis [42], one cannot distinguish these taxa on the basis of shell and radula characters alone. Under this hypothesis the Pomatiopsinae diverge in the Yangtze river drainage and the Triculinae into the Mekong river drainage; this major separation dated mid-Miocene (18 Ma). Oncomelania was assumed to have colonized Japan and the Philippines from China, with the radiation into several species of terrestrial Pomatiopsinae in Japan being driven by Miocene tectonic upheaval [10]. The lack of divergence among the other Pomatiopsinae (e.g., Tomichia with limited geographical or habitat range and few species having evolved over 80 Ma; see Figure 1) is explained by environmental stability [43]. Nevertheless, such a lack of radiation in southern continentally distributed pomatiopsines over 80 Ma compared with the extensive radiation of the Japanese taxa over 23–5 Ma is not easy to accept, and also the lack of radiation on the tectonically active Philippines (only one sub species of O. hupensis is found there) requires explanation. The phylogeny, dispersal tracts and time markers associated with this hypotheses are summarized in Table 1 and Figures 2 and 3A.

Bottom Line: Consequently, the aim of the study was to collect DNA-sequence data for as many pomatiopsid taxa as possible, as a first step in providing a resource for identification of epidemiologically significant species (by non-malacologists), for use in resolving taxonomic confusion and for testing phylogeographical hypotheses.The molecular dates and phylogenetic estimates in this study are consistent with an Australasian origin for the Pomatiopsidae and an East to West radiation via Oligocene Borneo-Philippines island hopping to Japan and then China (Triculinae arising mid-Miocene in Southeast China), and less so with a triculine origin in Tibet.The lack of monophyly in the medically important genera and indications of taxonomic inaccuracies, call for further work to identify epidemiologically significant taxa (e.g., Halewisia may be potential hosts for Schistosoma mekongi) and highlight the need for surveys to determine the true biodiversity of the Triculinae.

View Article: PubMed Central - HTML - PubMed

Affiliation: State Key Laboratory of Biotherapy, West China Hospital, West China Medical School, Sichuan University, 1 KeYuan 4 Lu, Chengdu, Sichuan 610041, People's Republic of China. swahuaxi@yahoo.com.

ABSTRACT

Background: The Pomatiopsidae are reported from northern India into southern China and Southeast Asia, with two sub-families, the Pomatiopsinae (which include freshwater, amphibious, terrestrial and marine species) and the freshwater Triculinae. Both include species acting as intermediate host for species of the blood-fluke Schistosoma which cause a public health problem in East Asia. Also, with around 120 species, triculine biodiversity exceeds that of any other endemic freshwater molluscan fauna. Nevertheless, the origins of the Pomatiopsidae, the factors driving such a diverse radiation and aspects of their co-evolution with Schistosoma are not fully understood. Many taxonomic questions remain; there are problems identifying medically relevant species. The predicted range is mostly unsurveyed and the true biodiversity of the family is underestimated. Consequently, the aim of the study was to collect DNA-sequence data for as many pomatiopsid taxa as possible, as a first step in providing a resource for identification of epidemiologically significant species (by non-malacologists), for use in resolving taxonomic confusion and for testing phylogeographical hypotheses.

Results: The evolutionary radiation of the Triculinae was shown to have been rapid and mostly post late Miocene. Molecular dating indicated that the radiation of these snails was driven first by the uplift of the Himalaya and onset of a monsoon system, and then by late-Pliocene global warming. The status of Erhaia as Anmicolidae is supported. The genera Tricula and Neotricula are shown to be non-monophyletic and the tribe Jullieniini may be polyphyletic (based on convergent characters). Triculinae from northern Vietnam could be derived from Gammatricula of Fujian/Yunnan, China.

Conclusions: The molecular dates and phylogenetic estimates in this study are consistent with an Australasian origin for the Pomatiopsidae and an East to West radiation via Oligocene Borneo-Philippines island hopping to Japan and then China (Triculinae arising mid-Miocene in Southeast China), and less so with a triculine origin in Tibet. The lack of monophyly in the medically important genera and indications of taxonomic inaccuracies, call for further work to identify epidemiologically significant taxa (e.g., Halewisia may be potential hosts for Schistosoma mekongi) and highlight the need for surveys to determine the true biodiversity of the Triculinae.

Show MeSH
Related in: MedlinePlus