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Multiple invasions into freshwater by pufferfishes (teleostei: tetraodontidae): a mitogenomic perspective.

Yamanoue Y, Miya M, Doi H, Mabuchi K, Sakai H, Nishida M - PLoS ONE (2011)

Bottom Line: The resulting phylogenies reveal that the family is composed of four major lineages and that freshwater species from the different continents are independently nested in two of the four lineages.Relaxed molecular-clock Bayesian divergence time estimation suggests that the timing of these invasions differs between continents, occurring at 0-10 million years ago (MA) in South America, 17-38 MA in Central Africa, and 48-78 MA in Southeast Asia.These timings are congruent with geological events that could facilitate adaptation to freshwater habitats in each continent.

View Article: PubMed Central - PubMed

Affiliation: Atmosphere and Ocean Research Institute, University of Tokyo, Kashiwa, Chiba, Japan. yamanouey@yahoo.co.jp

ABSTRACT
Pufferfishes of the Family Tetraodontidae are the most speciose group in the Order Tetraodontiformes and mainly inhabit coastal waters along continents. Although no members of other tetraodontiform families have fully discarded their marine lives, approximately 30 tetraodontid species spend their entire lives in freshwaters in disjunct tropical regions of South America, Central Africa, and Southeast Asia. To investigate the interrelationships of tetraodontid pufferfishes and thereby elucidate the evolutionary origins of their freshwater habitats, we performed phylogenetic analysis based on whole mitochondrial genome sequences from 50 tetraodontid species and closely related species (including 31 newly determined sequences). The resulting phylogenies reveal that the family is composed of four major lineages and that freshwater species from the different continents are independently nested in two of the four lineages. A monophyletic origin of the use of freshwater habitats was statistically rejected, and ancestral habitat reconstruction on the resulting tree demonstrates that tetraodontids independently entered freshwater habitats in different continents at least three times. Relaxed molecular-clock Bayesian divergence time estimation suggests that the timing of these invasions differs between continents, occurring at 0-10 million years ago (MA) in South America, 17-38 MA in Central Africa, and 48-78 MA in Southeast Asia. These timings are congruent with geological events that could facilitate adaptation to freshwater habitats in each continent.

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Distribution patterns of marine (shaded) and freshwater (colored) species in Tetraodontidae.Freshwater genera in South America, Central Africa, and Southeast Asia are shown with numbers of species in parentheses. Freshwater regions where only diadromous species occur are not indicated here. Distribution data follow Berra [11], Ebert [18], and Froese and Pauly [12].
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pone-0017410-g001: Distribution patterns of marine (shaded) and freshwater (colored) species in Tetraodontidae.Freshwater genera in South America, Central Africa, and Southeast Asia are shown with numbers of species in parentheses. Freshwater regions where only diadromous species occur are not indicated here. Distribution data follow Berra [11], Ebert [18], and Froese and Pauly [12].

Mentions: The Tetraodontidae, known as pufferfishes, are highly derived euteleosts. Composed of 189 species placed in 19 genera [12], Tetraodontidae is the most speciose family within the Order Tetraodontiformes. Fishes of this family have notably the smallest genomes among vertebrates, approximately 400 Mb or 1/8 the size of the human genome [13]. Considering these features, two pufferfishes, Takifugu rubripes and Tetraodon nigroviridis, were proposed as model systems for the evolution of vertebrate genomes [14], [15]. Most species occur in inshore and estuarine waters, but approximately 30 tetraodontid species spend their entire life cycles in freshwater in disjunct tropical regions of South America, Central Africa, and Southeast Asia [16], [17], [18] (Figure 1). It should be noted that no fishes in the other tetraodontiform families have discarded their marine lives [9].


Multiple invasions into freshwater by pufferfishes (teleostei: tetraodontidae): a mitogenomic perspective.

Yamanoue Y, Miya M, Doi H, Mabuchi K, Sakai H, Nishida M - PLoS ONE (2011)

Distribution patterns of marine (shaded) and freshwater (colored) species in Tetraodontidae.Freshwater genera in South America, Central Africa, and Southeast Asia are shown with numbers of species in parentheses. Freshwater regions where only diadromous species occur are not indicated here. Distribution data follow Berra [11], Ebert [18], and Froese and Pauly [12].
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3045446&req=5

pone-0017410-g001: Distribution patterns of marine (shaded) and freshwater (colored) species in Tetraodontidae.Freshwater genera in South America, Central Africa, and Southeast Asia are shown with numbers of species in parentheses. Freshwater regions where only diadromous species occur are not indicated here. Distribution data follow Berra [11], Ebert [18], and Froese and Pauly [12].
Mentions: The Tetraodontidae, known as pufferfishes, are highly derived euteleosts. Composed of 189 species placed in 19 genera [12], Tetraodontidae is the most speciose family within the Order Tetraodontiformes. Fishes of this family have notably the smallest genomes among vertebrates, approximately 400 Mb or 1/8 the size of the human genome [13]. Considering these features, two pufferfishes, Takifugu rubripes and Tetraodon nigroviridis, were proposed as model systems for the evolution of vertebrate genomes [14], [15]. Most species occur in inshore and estuarine waters, but approximately 30 tetraodontid species spend their entire life cycles in freshwater in disjunct tropical regions of South America, Central Africa, and Southeast Asia [16], [17], [18] (Figure 1). It should be noted that no fishes in the other tetraodontiform families have discarded their marine lives [9].

Bottom Line: The resulting phylogenies reveal that the family is composed of four major lineages and that freshwater species from the different continents are independently nested in two of the four lineages.Relaxed molecular-clock Bayesian divergence time estimation suggests that the timing of these invasions differs between continents, occurring at 0-10 million years ago (MA) in South America, 17-38 MA in Central Africa, and 48-78 MA in Southeast Asia.These timings are congruent with geological events that could facilitate adaptation to freshwater habitats in each continent.

View Article: PubMed Central - PubMed

Affiliation: Atmosphere and Ocean Research Institute, University of Tokyo, Kashiwa, Chiba, Japan. yamanouey@yahoo.co.jp

ABSTRACT
Pufferfishes of the Family Tetraodontidae are the most speciose group in the Order Tetraodontiformes and mainly inhabit coastal waters along continents. Although no members of other tetraodontiform families have fully discarded their marine lives, approximately 30 tetraodontid species spend their entire lives in freshwaters in disjunct tropical regions of South America, Central Africa, and Southeast Asia. To investigate the interrelationships of tetraodontid pufferfishes and thereby elucidate the evolutionary origins of their freshwater habitats, we performed phylogenetic analysis based on whole mitochondrial genome sequences from 50 tetraodontid species and closely related species (including 31 newly determined sequences). The resulting phylogenies reveal that the family is composed of four major lineages and that freshwater species from the different continents are independently nested in two of the four lineages. A monophyletic origin of the use of freshwater habitats was statistically rejected, and ancestral habitat reconstruction on the resulting tree demonstrates that tetraodontids independently entered freshwater habitats in different continents at least three times. Relaxed molecular-clock Bayesian divergence time estimation suggests that the timing of these invasions differs between continents, occurring at 0-10 million years ago (MA) in South America, 17-38 MA in Central Africa, and 48-78 MA in Southeast Asia. These timings are congruent with geological events that could facilitate adaptation to freshwater habitats in each continent.

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