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The strange case of East African annual fishes: aridification correlates with diversification for a savannah aquatic group?

Dorn A, Musilová Z, Platzer M, Reichwald K, Cellerino A - BMC Evol. Biol. (2014)

Bottom Line: The mechanism of Nothobranchius diversification was allopatric and driven by geographic isolation.Although confidence intervals for the estimated ages of the four Nothobranchius clades are quite large, this scenario is compatible with the biology of extant Nothobranchius that are critically dependent on savannah habitats.Therefore, Nothobranchius diversification might have been shaped by the same paleoclimatic events that shaped African ungulate evolution.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Annual Nothobranchius fishes are distributed in East and Southern Africa and inhabit ephemeral pools filled during the monsoon season. Nothobranchius show extreme life-history adaptations: embryos survive by entering diapause and they are the vertebrates with the fastest maturation and the shortest lifespan. The distribution of Nothobranchius overlaps with the East Africa Rift System. The geological and paleoclimatic history of this region is known in detail: in particular, aridification of East Africa and expansion of grassland habitats started 8 Mya and three humid periods between 3 and 1 Mya are superimposed on the longer-term aridification. These climatic oscillations are thought to have shaped evolution of savannah African mammals. We reconstructed the phylogeny of Nothobranchius and dated the different stages of diversification in relation to these paleoclimatic events.

Results: We sequenced one mitochondrial locus and five nuclear loci in 63 specimens and obtained a robust phylogeny. Nothobranchius can be divided in four geographically separated clades whose boundaries largely correspond to the East Africa Rift system. Statistical analysis of dispersal and vicariance identifies a Nilo-Sudan origin with southwards dispersion and confirmed that these four clades are the result of vicariance events In the absence of fossil Nothobranchius, molecular clock was calibrated using more distant outgroups (secondary calibration). This method estimates the age of the Nothobranchius genus to be 8.3 (6.0 - 10.7) My and the separation of the four clades 4.8 (2.7-7.0) Mya. Diversification within the clades was estimated to have started ~3 Mya and most species pairs were estimated to have an age of 0.5-1 My.

Conclusions: The mechanism of Nothobranchius diversification was allopatric and driven by geographic isolation. We propose a scenario where diversification of Nothobranchius started in rough coincidence with aridification of East Africa, establishment of grassland habitats and the appearance of the typical African bovid fauna of the savannah. Although confidence intervals for the estimated ages of the four Nothobranchius clades are quite large, this scenario is compatible with the biology of extant Nothobranchius that are critically dependent on savannah habitats. Therefore, Nothobranchius diversification might have been shaped by the same paleoclimatic events that shaped African ungulate evolution.

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Related in: MedlinePlus

Calibrated phylogenetic tree. Molecular clock tree reconstructed by BEAST analysis. The tree was calibrated by the secondary calibration of 8.32 (5.92 – 10.75) Mya for the genus Nothobranchius. Time axis shows the age in mya. The table embedded within the image reports the age estimates of individual nodes in the molecular-clock tree, where vicariance or dispersal occured. Results from the analysis in BEAST software using one individual per species.
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Fig3: Calibrated phylogenetic tree. Molecular clock tree reconstructed by BEAST analysis. The tree was calibrated by the secondary calibration of 8.32 (5.92 – 10.75) Mya for the genus Nothobranchius. Time axis shows the age in mya. The table embedded within the image reports the age estimates of individual nodes in the molecular-clock tree, where vicariance or dispersal occured. Results from the analysis in BEAST software using one individual per species.

Mentions: The final step of diversification was the divergence of several pairs of closely related sister species (N. rachovii and N. pienaari, N. furzeri and N. kadleci, N. oestergaardi and N. kafuensis, N. ugandensis and N. sp. “Lake Victoria”, N. hassoni and N. sp. “Lubumbashi”, N. kirki and N. wattersi, N. melanospilus and N. lucius, N. ruudwildekampi and N. albimarginatus) that occurred between ~ 0.5 and ~ 1 Mya. (Figure 3). We specifically tested for deviation from constant rate of cladogenesis by analysing lineage through time using TreePar [34] but could not detect deviations from a constant cladogenesis rate (Additional file 4: Table S3).Figure 3


The strange case of East African annual fishes: aridification correlates with diversification for a savannah aquatic group?

Dorn A, Musilová Z, Platzer M, Reichwald K, Cellerino A - BMC Evol. Biol. (2014)

Calibrated phylogenetic tree. Molecular clock tree reconstructed by BEAST analysis. The tree was calibrated by the secondary calibration of 8.32 (5.92 – 10.75) Mya for the genus Nothobranchius. Time axis shows the age in mya. The table embedded within the image reports the age estimates of individual nodes in the molecular-clock tree, where vicariance or dispersal occured. Results from the analysis in BEAST software using one individual per species.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4209228&req=5

Fig3: Calibrated phylogenetic tree. Molecular clock tree reconstructed by BEAST analysis. The tree was calibrated by the secondary calibration of 8.32 (5.92 – 10.75) Mya for the genus Nothobranchius. Time axis shows the age in mya. The table embedded within the image reports the age estimates of individual nodes in the molecular-clock tree, where vicariance or dispersal occured. Results from the analysis in BEAST software using one individual per species.
Mentions: The final step of diversification was the divergence of several pairs of closely related sister species (N. rachovii and N. pienaari, N. furzeri and N. kadleci, N. oestergaardi and N. kafuensis, N. ugandensis and N. sp. “Lake Victoria”, N. hassoni and N. sp. “Lubumbashi”, N. kirki and N. wattersi, N. melanospilus and N. lucius, N. ruudwildekampi and N. albimarginatus) that occurred between ~ 0.5 and ~ 1 Mya. (Figure 3). We specifically tested for deviation from constant rate of cladogenesis by analysing lineage through time using TreePar [34] but could not detect deviations from a constant cladogenesis rate (Additional file 4: Table S3).Figure 3

Bottom Line: The mechanism of Nothobranchius diversification was allopatric and driven by geographic isolation.Although confidence intervals for the estimated ages of the four Nothobranchius clades are quite large, this scenario is compatible with the biology of extant Nothobranchius that are critically dependent on savannah habitats.Therefore, Nothobranchius diversification might have been shaped by the same paleoclimatic events that shaped African ungulate evolution.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Annual Nothobranchius fishes are distributed in East and Southern Africa and inhabit ephemeral pools filled during the monsoon season. Nothobranchius show extreme life-history adaptations: embryos survive by entering diapause and they are the vertebrates with the fastest maturation and the shortest lifespan. The distribution of Nothobranchius overlaps with the East Africa Rift System. The geological and paleoclimatic history of this region is known in detail: in particular, aridification of East Africa and expansion of grassland habitats started 8 Mya and three humid periods between 3 and 1 Mya are superimposed on the longer-term aridification. These climatic oscillations are thought to have shaped evolution of savannah African mammals. We reconstructed the phylogeny of Nothobranchius and dated the different stages of diversification in relation to these paleoclimatic events.

Results: We sequenced one mitochondrial locus and five nuclear loci in 63 specimens and obtained a robust phylogeny. Nothobranchius can be divided in four geographically separated clades whose boundaries largely correspond to the East Africa Rift system. Statistical analysis of dispersal and vicariance identifies a Nilo-Sudan origin with southwards dispersion and confirmed that these four clades are the result of vicariance events In the absence of fossil Nothobranchius, molecular clock was calibrated using more distant outgroups (secondary calibration). This method estimates the age of the Nothobranchius genus to be 8.3 (6.0 - 10.7) My and the separation of the four clades 4.8 (2.7-7.0) Mya. Diversification within the clades was estimated to have started ~3 Mya and most species pairs were estimated to have an age of 0.5-1 My.

Conclusions: The mechanism of Nothobranchius diversification was allopatric and driven by geographic isolation. We propose a scenario where diversification of Nothobranchius started in rough coincidence with aridification of East Africa, establishment of grassland habitats and the appearance of the typical African bovid fauna of the savannah. Although confidence intervals for the estimated ages of the four Nothobranchius clades are quite large, this scenario is compatible with the biology of extant Nothobranchius that are critically dependent on savannah habitats. Therefore, Nothobranchius diversification might have been shaped by the same paleoclimatic events that shaped African ungulate evolution.

Show MeSH
Related in: MedlinePlus