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Strong population genetic structuring in an annual fish, Nothobranchius furzeri, suggests multiple savannah refugia in southern Mozambique.

Bartáková V, Reichard M, Janko K, Polačik M, Blažek R, Reichwald K, Cellerino A, Bryja J - BMC Evol. Biol. (2013)

Bottom Line: Genetic markers consistently demonstrated strong population structuring and suggested two main genetic groups associated with river basins.Analysis of historical demography revealed that the expansion of both groups is ongoing, supported by frequent founder effects in marginal parts of the range and evidence of secondary contact between Chefu and Limpopo populations.We demonstrated: (1) ancient (pre-Pleistocene) divergence between the two main N. furzeri lineages, their recent secondary contact and lack of reproductive isolation; (2) important genetic structuring attributed to the fragmented nature of their environment and isolation-by-distance, suggesting that dispersal is limited, occurs over short distances and is not directly associated with river routes; (3) an apparent role of the River Limpopo as a barrier to dispersal and gene flow.

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Affiliation: Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Květná 8, Brno 603 65, Czech Republic. bryja@brno.cas.cz.

ABSTRACT

Background: Intraspecific genetic variation of African fauna has been significantly affected by pronounced climatic fluctuations in Plio-Pleistocene, but, with the exception of large mammals, very limited empirical data on diversity of natural populations are available for savanna-dwelling animals. Nothobranchius furzeri is an annual fish from south-eastern Africa, inhabiting discrete temporary savannah pools outside main river alluvia. Their dispersal is limited and population processes affecting its genetic structure are likely a combination of those affecting terrestrial and aquatic taxa. N. furzeri is a model taxon in ageing research and several populations of known geographical origin are used in laboratory studies. Here, we analysed the genetic structure, diversity, historical demography and temporal patterns of divergence in natural populations of N. furzeri across its entire distribution range.

Results: Genetic structure and historical demography of N. furzeri were analysed using a combination of mitochondrial (partial cytochrome b sequences, 687 bp) and nuclear (13 microsatellites) markers in 693 fish from 36 populations. Genetic markers consistently demonstrated strong population structuring and suggested two main genetic groups associated with river basins. The split was dated to the Pliocene (>2 Mya). The northern group inhabits savannah pools across the basin of the intermittent river Chefu in south-western Mozambique and eastern Zimbabwe. The southern group (from southernmost Mozambique) is subdivided, with the River Limpopo forming a barrier (maximum divergence time 1 Mya). A strong habitat fragmentation (isolated temporary pools) is reflected in significant genetic structuring even between adjacent pools, with a major influence of genetic drift and significant isolation-by-distance. Analysis of historical demography revealed that the expansion of both groups is ongoing, supported by frequent founder effects in marginal parts of the range and evidence of secondary contact between Chefu and Limpopo populations.

Conclusions: We demonstrated: (1) ancient (pre-Pleistocene) divergence between the two main N. furzeri lineages, their recent secondary contact and lack of reproductive isolation; (2) important genetic structuring attributed to the fragmented nature of their environment and isolation-by-distance, suggesting that dispersal is limited, occurs over short distances and is not directly associated with river routes; (3) an apparent role of the River Limpopo as a barrier to dispersal and gene flow.

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Mismatch distribution and Bayesian skyline plots for the three mtDNA clades. (a) Mismatch distribution between mtDNA haplotypes from three major mtDNA clades. Dashed lines connect observed values and solid lines show the expected distribution under a demographic expansion model. (b) Bayesian skyline plots for the three main clades, showing changes in effective population size (Nem; on a log10 scale) over time (in years). The thick solid line depicts the median estimate, while dotted lines represent the 95% highest posterior density intervals.
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Figure 4: Mismatch distribution and Bayesian skyline plots for the three mtDNA clades. (a) Mismatch distribution between mtDNA haplotypes from three major mtDNA clades. Dashed lines connect observed values and solid lines show the expected distribution under a demographic expansion model. (b) Bayesian skyline plots for the three main clades, showing changes in effective population size (Nem; on a log10 scale) over time (in years). The thick solid line depicts the median estimate, while dotted lines represent the 95% highest posterior density intervals.

Mentions: Comparison of mtDNA variation among the three main genetic groups and the results of neutrality tests are shown in Table 4. All populations significantly fitted the model of sudden growth according to SSD analysis in ARLEQUIN and showed a unimodal pattern (Figure 4a). Bayesian skyline plots indicated moderate (LimpN, LimpS) to intensive (Chefu) population growth in all three genetic groups (Figure 4b). This finding is consistent with neutrality tests that showed a non-significant signal for population growth in the LimpS and LimpN clades (where only the R2 values were significant), while all tests indicated highly significant deviations from neutrality in the Chefu clade (Table 4). The τ values from DnaSP suggested more recent population expansions compared to estimates by ARLEQUIN, which conforms to a previously reported tendency of the moment method to underestimate the true values [49]. Nonetheless the DnaSP estimates were always included within the 90% CI of ARLEQUIN (Table 4). ARLEQUIN analysis was congruent with the BSP analysis and indicated a more recent population expansion in the Chefu group (mean estimates 70–118 kya according to the method used) compared to two Limpopo groups (112–255 kya) (Table 4). This timing is comparable to that suggested by the BSP analysis (Figure 4b).


Strong population genetic structuring in an annual fish, Nothobranchius furzeri, suggests multiple savannah refugia in southern Mozambique.

Bartáková V, Reichard M, Janko K, Polačik M, Blažek R, Reichwald K, Cellerino A, Bryja J - BMC Evol. Biol. (2013)

Mismatch distribution and Bayesian skyline plots for the three mtDNA clades. (a) Mismatch distribution between mtDNA haplotypes from three major mtDNA clades. Dashed lines connect observed values and solid lines show the expected distribution under a demographic expansion model. (b) Bayesian skyline plots for the three main clades, showing changes in effective population size (Nem; on a log10 scale) over time (in years). The thick solid line depicts the median estimate, while dotted lines represent the 95% highest posterior density intervals.
© Copyright Policy - open-access
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4231482&req=5

Figure 4: Mismatch distribution and Bayesian skyline plots for the three mtDNA clades. (a) Mismatch distribution between mtDNA haplotypes from three major mtDNA clades. Dashed lines connect observed values and solid lines show the expected distribution under a demographic expansion model. (b) Bayesian skyline plots for the three main clades, showing changes in effective population size (Nem; on a log10 scale) over time (in years). The thick solid line depicts the median estimate, while dotted lines represent the 95% highest posterior density intervals.
Mentions: Comparison of mtDNA variation among the three main genetic groups and the results of neutrality tests are shown in Table 4. All populations significantly fitted the model of sudden growth according to SSD analysis in ARLEQUIN and showed a unimodal pattern (Figure 4a). Bayesian skyline plots indicated moderate (LimpN, LimpS) to intensive (Chefu) population growth in all three genetic groups (Figure 4b). This finding is consistent with neutrality tests that showed a non-significant signal for population growth in the LimpS and LimpN clades (where only the R2 values were significant), while all tests indicated highly significant deviations from neutrality in the Chefu clade (Table 4). The τ values from DnaSP suggested more recent population expansions compared to estimates by ARLEQUIN, which conforms to a previously reported tendency of the moment method to underestimate the true values [49]. Nonetheless the DnaSP estimates were always included within the 90% CI of ARLEQUIN (Table 4). ARLEQUIN analysis was congruent with the BSP analysis and indicated a more recent population expansion in the Chefu group (mean estimates 70–118 kya according to the method used) compared to two Limpopo groups (112–255 kya) (Table 4). This timing is comparable to that suggested by the BSP analysis (Figure 4b).

Bottom Line: Genetic markers consistently demonstrated strong population structuring and suggested two main genetic groups associated with river basins.Analysis of historical demography revealed that the expansion of both groups is ongoing, supported by frequent founder effects in marginal parts of the range and evidence of secondary contact between Chefu and Limpopo populations.We demonstrated: (1) ancient (pre-Pleistocene) divergence between the two main N. furzeri lineages, their recent secondary contact and lack of reproductive isolation; (2) important genetic structuring attributed to the fragmented nature of their environment and isolation-by-distance, suggesting that dispersal is limited, occurs over short distances and is not directly associated with river routes; (3) an apparent role of the River Limpopo as a barrier to dispersal and gene flow.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Květná 8, Brno 603 65, Czech Republic. bryja@brno.cas.cz.

ABSTRACT

Background: Intraspecific genetic variation of African fauna has been significantly affected by pronounced climatic fluctuations in Plio-Pleistocene, but, with the exception of large mammals, very limited empirical data on diversity of natural populations are available for savanna-dwelling animals. Nothobranchius furzeri is an annual fish from south-eastern Africa, inhabiting discrete temporary savannah pools outside main river alluvia. Their dispersal is limited and population processes affecting its genetic structure are likely a combination of those affecting terrestrial and aquatic taxa. N. furzeri is a model taxon in ageing research and several populations of known geographical origin are used in laboratory studies. Here, we analysed the genetic structure, diversity, historical demography and temporal patterns of divergence in natural populations of N. furzeri across its entire distribution range.

Results: Genetic structure and historical demography of N. furzeri were analysed using a combination of mitochondrial (partial cytochrome b sequences, 687 bp) and nuclear (13 microsatellites) markers in 693 fish from 36 populations. Genetic markers consistently demonstrated strong population structuring and suggested two main genetic groups associated with river basins. The split was dated to the Pliocene (>2 Mya). The northern group inhabits savannah pools across the basin of the intermittent river Chefu in south-western Mozambique and eastern Zimbabwe. The southern group (from southernmost Mozambique) is subdivided, with the River Limpopo forming a barrier (maximum divergence time 1 Mya). A strong habitat fragmentation (isolated temporary pools) is reflected in significant genetic structuring even between adjacent pools, with a major influence of genetic drift and significant isolation-by-distance. Analysis of historical demography revealed that the expansion of both groups is ongoing, supported by frequent founder effects in marginal parts of the range and evidence of secondary contact between Chefu and Limpopo populations.

Conclusions: We demonstrated: (1) ancient (pre-Pleistocene) divergence between the two main N. furzeri lineages, their recent secondary contact and lack of reproductive isolation; (2) important genetic structuring attributed to the fragmented nature of their environment and isolation-by-distance, suggesting that dispersal is limited, occurs over short distances and is not directly associated with river routes; (3) an apparent role of the River Limpopo as a barrier to dispersal and gene flow.

Show MeSH
Related in: MedlinePlus