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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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The radiation of Pachydrobiini into Sundaland. Semi-schematic depicting a possible late Miocene dispersal route for Robertsiella-Guoia clade Pachydrobiini diverging in Hunan to enter Sundaland via now extinct river systems draining the, now submarine, Sunda shelf. This model allows for the observed independent and heterochronous colonization of Sundaland by Neotricula and Robertsiella. Present day coastlines are shown by thick broken lines, the modern Mul and Mekong rivers are indicated as thin grey lines and the Miocene extended Mekong-Ping river is shown by a dotted black line. The extent of the Miocene coastline beyond that of the present is indicated in light grey. Geological features and coastlines approximate.
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Figure 7: The radiation of Pachydrobiini into Sundaland. Semi-schematic depicting a possible late Miocene dispersal route for Robertsiella-Guoia clade Pachydrobiini diverging in Hunan to enter Sundaland via now extinct river systems draining the, now submarine, Sunda shelf. This model allows for the observed independent and heterochronous colonization of Sundaland by Neotricula and Robertsiella. Present day coastlines are shown by thick broken lines, the modern Mul and Mekong rivers are indicated as thin grey lines and the Miocene extended Mekong-Ping river is shown by a dotted black line. The extent of the Miocene coastline beyond that of the present is indicated in light grey. Geological features and coastlines approximate.

Mentions: The phylogeny in Figure 6 then shows a series of Plio-Pleistocene divergences among minor taxonomic groups. The divergence of Delavaya of Dianchi lake (Yunnan) from the spring-dwelling Tricula of Yunnan is estimated to have occurred around 4 Ma; this appears to correspond with the creation of Dianchi lake in the Pliocene, some time prior to 3.4 Ma [100]. Table 4 (Malaya) shows that Robertisiella diverged from Neotricula aperta and other Mekong river Pachydrobiini around an estimated 3.5 Ma. Table 1 links this divergence to events isolating the Pahang river system of West Malaysia from the extended Mekong river due to river course changes and rising sea levels which flooded the Sunda shelf (2.6-0.8 Ma), the Pliocene Mekong river flowed directly from southern Laos, across Cambodia (via the Tonle Sap of today) to Kampot and then into Pahang drainage of Malaysia (Figure 7) [59,60]. More recent evidence suggests a particularly warm and generally humid global climate between 3.56 and 3.4 Ma [101]; this would certainly have flooded the Sunda shelf and isolated Malaysian Robertsiella from the Mekong river pachydrobiinine radiation. The divergence of Robertsiella from Neotricula appears to predate that of Schistosoma mekongi from S. malayensis, which was dated at around 1.3 Ma [60], although the polarity of Schistosoma does appear to match that of their intermediate hosts (i.e., Robertsiella appears to have arisen first – Davis proposed that this genus arose as part of the Hunan pachydrobiinine radiation [8]). The divergence of Robertsiella could also be associated with the accelerated uplift of the eastern edge of the Qinghai-Tibet Plateau at 3.4 Ma [56], affecting Sichuan, Yunnan and Sundaland along the eastern margin of the Sibamasu block. The greater affinity of Robertsiella with taxa of North Sundaland and Yunnan (N. burchi and Jinghongia) supports earlier studies that suggested a direct tract of dispersal of Robertsiella from Hunan to the proto-Mekong river of Cambodia, across the exposed Sunda shelf off the modern coast of Vietnam [53] (Figure 7); thus explaining why Robertsiella is not derived from the lower Mekong Pachydrobiini clade and suggesting that Neotricula aperta arrived in Cambodia via a slightly different drainage system.


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)

The radiation of Pachydrobiini into Sundaland. Semi-schematic depicting a possible late Miocene dispersal route for Robertsiella-Guoia clade Pachydrobiini diverging in Hunan to enter Sundaland via now extinct river systems draining the, now submarine, Sunda shelf. This model allows for the observed independent and heterochronous colonization of Sundaland by Neotricula and Robertsiella. Present day coastlines are shown by thick broken lines, the modern Mul and Mekong rivers are indicated as thin grey lines and the Miocene extended Mekong-Ping river is shown by a dotted black line. The extent of the Miocene coastline beyond that of the present is indicated in light grey. Geological features and coastlines approximate.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: The radiation of Pachydrobiini into Sundaland. Semi-schematic depicting a possible late Miocene dispersal route for Robertsiella-Guoia clade Pachydrobiini diverging in Hunan to enter Sundaland via now extinct river systems draining the, now submarine, Sunda shelf. This model allows for the observed independent and heterochronous colonization of Sundaland by Neotricula and Robertsiella. Present day coastlines are shown by thick broken lines, the modern Mul and Mekong rivers are indicated as thin grey lines and the Miocene extended Mekong-Ping river is shown by a dotted black line. The extent of the Miocene coastline beyond that of the present is indicated in light grey. Geological features and coastlines approximate.
Mentions: The phylogeny in Figure 6 then shows a series of Plio-Pleistocene divergences among minor taxonomic groups. The divergence of Delavaya of Dianchi lake (Yunnan) from the spring-dwelling Tricula of Yunnan is estimated to have occurred around 4 Ma; this appears to correspond with the creation of Dianchi lake in the Pliocene, some time prior to 3.4 Ma [100]. Table 4 (Malaya) shows that Robertisiella diverged from Neotricula aperta and other Mekong river Pachydrobiini around an estimated 3.5 Ma. Table 1 links this divergence to events isolating the Pahang river system of West Malaysia from the extended Mekong river due to river course changes and rising sea levels which flooded the Sunda shelf (2.6-0.8 Ma), the Pliocene Mekong river flowed directly from southern Laos, across Cambodia (via the Tonle Sap of today) to Kampot and then into Pahang drainage of Malaysia (Figure 7) [59,60]. More recent evidence suggests a particularly warm and generally humid global climate between 3.56 and 3.4 Ma [101]; this would certainly have flooded the Sunda shelf and isolated Malaysian Robertsiella from the Mekong river pachydrobiinine radiation. The divergence of Robertsiella from Neotricula appears to predate that of Schistosoma mekongi from S. malayensis, which was dated at around 1.3 Ma [60], although the polarity of Schistosoma does appear to match that of their intermediate hosts (i.e., Robertsiella appears to have arisen first – Davis proposed that this genus arose as part of the Hunan pachydrobiinine radiation [8]). The divergence of Robertsiella could also be associated with the accelerated uplift of the eastern edge of the Qinghai-Tibet Plateau at 3.4 Ma [56], affecting Sichuan, Yunnan and Sundaland along the eastern margin of the Sibamasu block. The greater affinity of Robertsiella with taxa of North Sundaland and Yunnan (N. burchi and Jinghongia) supports earlier studies that suggested a direct tract of dispersal of Robertsiella from Hunan to the proto-Mekong river of Cambodia, across the exposed Sunda shelf off the modern coast of Vietnam [53] (Figure 7); thus explaining why Robertsiella is not derived from the lower Mekong Pachydrobiini clade and suggesting that Neotricula aperta arrived in Cambodia via a slightly different drainage system.

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