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Recurrent camouflaged invasions and dispersal of an Asian freshwater gastropod in tropical Africa.

Van Bocxlaer B, Clewing C, Mongindo Etimosundja JP, Kankonda A, Wembo Ndeo O, Albrecht C - BMC Evol. Biol. (2015)

Bottom Line: Assessing ecological and evolutionary consequences of invasions simultaneously may therefore be the most effective approach to study taxa with complex invasion histories.Finally, the results of geographic modeling indicate that cryptic M. tuberculata invasions occurred primarily in densely populated areas.We draw suggestions for more effective conservation strategies from our integrated approach.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32 (IFZ), D-35392, Giessen, Germany. bert.vanbocxlaer@ugent.be.

ABSTRACT

Background: Non-indigenous taxa currently represent a large fraction of the species and biomass of freshwater ecosystems. The accumulation of invasive taxa in combination with other stressors in these ecosystems may alter the habitats to which native taxa are adapted, which could elicit evolutionary changes in native populations and their ecological interactions. Assessing ecological and evolutionary consequences of invasions simultaneously may therefore be the most effective approach to study taxa with complex invasion histories. Here we apply such an integrated approach to the cerithioid gastropod Melanoides tuberculata, a model system in invasion biology.

Results: Molecular phylogenetics and ancestral range reconstructions allowed us to identify several independent Asian invasions in Lakes Malawi and Tanganyika, the Congo River, Nigeria and Cameroon. Some invasive M. tuberculata populations display much variation in shell morphology, and overlap in morphospace with M. tuberculata populations native to Africa. Experiments confirmed great ecophenotyic plasticity in some invasive populations, which, in combination with the overlap in disparity with native populations, masks invaders and their dispersal through Africa. Finally, the results of geographic modeling indicate that cryptic M. tuberculata invasions occurred primarily in densely populated areas.

Conclusions: We reveal the continental nature of invasions of Asian M. tuberculata to Africa. Several of the affected ecosystems have high endemicity in Cerithioidea: Lake Tanganyika has an unparalleled diversity in freshwater cerithioids (>10 endemic genera) and the Congo Basin and Lake Malawi are home to the two largest endemic species clusters of Melanoides in Africa (~12 and ~8 species, respectively). Cerithioids perform ecologically important functions in the benthic ecosystems of African freshwaters, but invaders and ecosystem change pose risks to their native diversity. We draw suggestions for more effective conservation strategies from our integrated approach.

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Maximum credibility phylogeny ofMelanoidesbased on mitochondrial COI and 16S data. Bayesian posterior probabilities are given above the nodes (values <0.50 not indicated). Color coding indicates geographical range, with representation of the maximum likelihood reconstructions of ancestral geographic origin at selected nodes; black codes for terminal taxa indicate an African origin; blue ones originate from other continents. Three-letter morph codes are indicated for Melanoides tuberculata. The scale bar represents substitutions per site according to the applied model of sequence evolution. Clades specifically discussed in the text are labeled at their basal nodes with encircled numbers (which also facilitate comparison to Figure 3). Gradient rectangles indicate the invasions here discussed. *indicates sequences obtained from GenBank. The inset map of tropical Africa indicates that invasions (arrows) occurred in areas with high human population density; Lakes Malawi, Tanganyika and Victoria are labelled. Population data were obtained from NASA’s Socioeconomic Data and Applications Center (http://sedac.ciesin.columbia.edu; copyright ownership by the Center for International Earth Science Information Network [CIESIN]; accessed 28 March 2014).
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Fig2: Maximum credibility phylogeny ofMelanoidesbased on mitochondrial COI and 16S data. Bayesian posterior probabilities are given above the nodes (values <0.50 not indicated). Color coding indicates geographical range, with representation of the maximum likelihood reconstructions of ancestral geographic origin at selected nodes; black codes for terminal taxa indicate an African origin; blue ones originate from other continents. Three-letter morph codes are indicated for Melanoides tuberculata. The scale bar represents substitutions per site according to the applied model of sequence evolution. Clades specifically discussed in the text are labeled at their basal nodes with encircled numbers (which also facilitate comparison to Figure 3). Gradient rectangles indicate the invasions here discussed. *indicates sequences obtained from GenBank. The inset map of tropical Africa indicates that invasions (arrows) occurred in areas with high human population density; Lakes Malawi, Tanganyika and Victoria are labelled. Population data were obtained from NASA’s Socioeconomic Data and Applications Center (http://sedac.ciesin.columbia.edu; copyright ownership by the Center for International Earth Science Information Network [CIESIN]; accessed 28 March 2014).

Mentions: Phylogenetic analyses of the concatenated COI + 16S dataset (Figure 2) resulted in overall highly similar topologies to those in single fragment phylogenies (Figure 3), despite substantial differences in the sampling for both genes (Table 1). Analyses of BF revealed that the fit of uncorrelated lognormal relaxed clock models to our datasets was consistently better than that of strict clock approaches, and hence uniform rates of sequence evolution along the phylogeny were rejected. Ancestral range reconstructions in R and using Lagrange resulted in almost identical results; the first method was used for visualization; results of the second method are displayed in Additional file 2: Table S2.Figure 2


Recurrent camouflaged invasions and dispersal of an Asian freshwater gastropod in tropical Africa.

Van Bocxlaer B, Clewing C, Mongindo Etimosundja JP, Kankonda A, Wembo Ndeo O, Albrecht C - BMC Evol. Biol. (2015)

Maximum credibility phylogeny ofMelanoidesbased on mitochondrial COI and 16S data. Bayesian posterior probabilities are given above the nodes (values <0.50 not indicated). Color coding indicates geographical range, with representation of the maximum likelihood reconstructions of ancestral geographic origin at selected nodes; black codes for terminal taxa indicate an African origin; blue ones originate from other continents. Three-letter morph codes are indicated for Melanoides tuberculata. The scale bar represents substitutions per site according to the applied model of sequence evolution. Clades specifically discussed in the text are labeled at their basal nodes with encircled numbers (which also facilitate comparison to Figure 3). Gradient rectangles indicate the invasions here discussed. *indicates sequences obtained from GenBank. The inset map of tropical Africa indicates that invasions (arrows) occurred in areas with high human population density; Lakes Malawi, Tanganyika and Victoria are labelled. Population data were obtained from NASA’s Socioeconomic Data and Applications Center (http://sedac.ciesin.columbia.edu; copyright ownership by the Center for International Earth Science Information Network [CIESIN]; accessed 28 March 2014).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4373078&req=5

Fig2: Maximum credibility phylogeny ofMelanoidesbased on mitochondrial COI and 16S data. Bayesian posterior probabilities are given above the nodes (values <0.50 not indicated). Color coding indicates geographical range, with representation of the maximum likelihood reconstructions of ancestral geographic origin at selected nodes; black codes for terminal taxa indicate an African origin; blue ones originate from other continents. Three-letter morph codes are indicated for Melanoides tuberculata. The scale bar represents substitutions per site according to the applied model of sequence evolution. Clades specifically discussed in the text are labeled at their basal nodes with encircled numbers (which also facilitate comparison to Figure 3). Gradient rectangles indicate the invasions here discussed. *indicates sequences obtained from GenBank. The inset map of tropical Africa indicates that invasions (arrows) occurred in areas with high human population density; Lakes Malawi, Tanganyika and Victoria are labelled. Population data were obtained from NASA’s Socioeconomic Data and Applications Center (http://sedac.ciesin.columbia.edu; copyright ownership by the Center for International Earth Science Information Network [CIESIN]; accessed 28 March 2014).
Mentions: Phylogenetic analyses of the concatenated COI + 16S dataset (Figure 2) resulted in overall highly similar topologies to those in single fragment phylogenies (Figure 3), despite substantial differences in the sampling for both genes (Table 1). Analyses of BF revealed that the fit of uncorrelated lognormal relaxed clock models to our datasets was consistently better than that of strict clock approaches, and hence uniform rates of sequence evolution along the phylogeny were rejected. Ancestral range reconstructions in R and using Lagrange resulted in almost identical results; the first method was used for visualization; results of the second method are displayed in Additional file 2: Table S2.Figure 2

Bottom Line: Assessing ecological and evolutionary consequences of invasions simultaneously may therefore be the most effective approach to study taxa with complex invasion histories.Finally, the results of geographic modeling indicate that cryptic M. tuberculata invasions occurred primarily in densely populated areas.We draw suggestions for more effective conservation strategies from our integrated approach.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32 (IFZ), D-35392, Giessen, Germany. bert.vanbocxlaer@ugent.be.

ABSTRACT

Background: Non-indigenous taxa currently represent a large fraction of the species and biomass of freshwater ecosystems. The accumulation of invasive taxa in combination with other stressors in these ecosystems may alter the habitats to which native taxa are adapted, which could elicit evolutionary changes in native populations and their ecological interactions. Assessing ecological and evolutionary consequences of invasions simultaneously may therefore be the most effective approach to study taxa with complex invasion histories. Here we apply such an integrated approach to the cerithioid gastropod Melanoides tuberculata, a model system in invasion biology.

Results: Molecular phylogenetics and ancestral range reconstructions allowed us to identify several independent Asian invasions in Lakes Malawi and Tanganyika, the Congo River, Nigeria and Cameroon. Some invasive M. tuberculata populations display much variation in shell morphology, and overlap in morphospace with M. tuberculata populations native to Africa. Experiments confirmed great ecophenotyic plasticity in some invasive populations, which, in combination with the overlap in disparity with native populations, masks invaders and their dispersal through Africa. Finally, the results of geographic modeling indicate that cryptic M. tuberculata invasions occurred primarily in densely populated areas.

Conclusions: We reveal the continental nature of invasions of Asian M. tuberculata to Africa. Several of the affected ecosystems have high endemicity in Cerithioidea: Lake Tanganyika has an unparalleled diversity in freshwater cerithioids (>10 endemic genera) and the Congo Basin and Lake Malawi are home to the two largest endemic species clusters of Melanoides in Africa (~12 and ~8 species, respectively). Cerithioids perform ecologically important functions in the benthic ecosystems of African freshwaters, but invaders and ecosystem change pose risks to their native diversity. We draw suggestions for more effective conservation strategies from our integrated approach.

Show MeSH