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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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Genetic variation of nuclear microsatellites assessed using STRUCTURE. Pie chart colours represent the proportional membership of individuals to microsatellite-based clusters inferred from the model for K = 7 (this model is well supported by Evanno et al. approach and provides detailed substructuring; see also Additional file 3). The dashed red line indicates the border between the Chefu and Limpopo haplogroups. The diameter of the pie charts is related to allelic richness (except the captive population GRZ, which is not scaled). Asterisks indicate populations with probable inbreeding (deficit of heterozygotes at four loci; Pop323 and Pop124); the red arrow indicates a population showing a significant bottleneck (Pop13); green arrow indicates secondary contact of two mtDNA lineages (Pop406).
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Figure 2: Genetic variation of nuclear microsatellites assessed using STRUCTURE. Pie chart colours represent the proportional membership of individuals to microsatellite-based clusters inferred from the model for K = 7 (this model is well supported by Evanno et al. approach and provides detailed substructuring; see also Additional file 3). The dashed red line indicates the border between the Chefu and Limpopo haplogroups. The diameter of the pie charts is related to allelic richness (except the captive population GRZ, which is not scaled). Asterisks indicate populations with probable inbreeding (deficit of heterozygotes at four loci; Pop323 and Pop124); the red arrow indicates a population showing a significant bottleneck (Pop13); green arrow indicates secondary contact of two mtDNA lineages (Pop406).

Mentions: Most populations (25 out of 30) showed deviance from HWE, when calculated over all loci. In most cases deviations from HWE were caused by alleles present at an increased frequency at some loci and populations. The mean frequency of alleles for 21 locus-population tests significant after FDR correction (from 13 × 30 = 390 locus-population pairs) was 13.1 ± 5.45% (N = 21), while for the whole dataset the mean frequency of alleles was only 2.43 ± 4.14% (N = 390). In most populations, the HW disequilibrium was caused by just one or two loci. The only exceptions were peripheral populations Pop124 and Pop323, which showed a deficit of heterozygotes at four loci, suggesting an increased level of inbreeding (Figure 2).


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)

Genetic variation of nuclear microsatellites assessed using STRUCTURE. Pie chart colours represent the proportional membership of individuals to microsatellite-based clusters inferred from the model for K = 7 (this model is well supported by Evanno et al. approach and provides detailed substructuring; see also Additional file 3). The dashed red line indicates the border between the Chefu and Limpopo haplogroups. The diameter of the pie charts is related to allelic richness (except the captive population GRZ, which is not scaled). Asterisks indicate populations with probable inbreeding (deficit of heterozygotes at four loci; Pop323 and Pop124); the red arrow indicates a population showing a significant bottleneck (Pop13); green arrow indicates secondary contact of two mtDNA lineages (Pop406).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4231482&req=5

Figure 2: Genetic variation of nuclear microsatellites assessed using STRUCTURE. Pie chart colours represent the proportional membership of individuals to microsatellite-based clusters inferred from the model for K = 7 (this model is well supported by Evanno et al. approach and provides detailed substructuring; see also Additional file 3). The dashed red line indicates the border between the Chefu and Limpopo haplogroups. The diameter of the pie charts is related to allelic richness (except the captive population GRZ, which is not scaled). Asterisks indicate populations with probable inbreeding (deficit of heterozygotes at four loci; Pop323 and Pop124); the red arrow indicates a population showing a significant bottleneck (Pop13); green arrow indicates secondary contact of two mtDNA lineages (Pop406).
Mentions: Most populations (25 out of 30) showed deviance from HWE, when calculated over all loci. In most cases deviations from HWE were caused by alleles present at an increased frequency at some loci and populations. The mean frequency of alleles for 21 locus-population tests significant after FDR correction (from 13 × 30 = 390 locus-population pairs) was 13.1 ± 5.45% (N = 21), while for the whole dataset the mean frequency of alleles was only 2.43 ± 4.14% (N = 390). In most populations, the HW disequilibrium was caused by just one or two loci. The only exceptions were peripheral populations Pop124 and Pop323, which showed a deficit of heterozygotes at four loci, suggesting an increased level of inbreeding (Figure 2).

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