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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.

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.

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Map showing the distribution of 36 sample sites. Different symbols indicate the distribution of three main mtDNA haplogroups (called Chefu, LimpN, and LimpS). Numbers of localities correspond to Table 1. Haplotypes from the two haplogroups (Chefu and LimpN) were found in Pop406 (marked by the green arrow). Note that LimpS includes the localities from both the Limpopo and Incomati basins. Black arrow shows the position of the locality at Gona Re Zhou National Park in Zimbabwe (GRZ) that was excluded from some analyses because the individuals originated from a captive population. The inset figures show the position of the study area within Africa and Mozambique.
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Figure 1: Map showing the distribution of 36 sample sites. Different symbols indicate the distribution of three main mtDNA haplogroups (called Chefu, LimpN, and LimpS). Numbers of localities correspond to Table 1. Haplotypes from the two haplogroups (Chefu and LimpN) were found in Pop406 (marked by the green arrow). Note that LimpS includes the localities from both the Limpopo and Incomati basins. Black arrow shows the position of the locality at Gona Re Zhou National Park in Zimbabwe (GRZ) that was excluded from some analyses because the individuals originated from a captive population. The inset figures show the position of the study area within Africa and Mozambique.

Mentions: Fish were collected during 8 field trips between 2008 and 2012, visiting 336 individual savannah pools across southern and central Mozambique, with the aim of sampling pools across the entire savannah habitat in that region. From a total of 163 pools populated by Nothobranchius spp., 73 pools were inhabited by N. furzeri, all of them south of the River Save (Figure 1). Fish were collected using dip and Seine nets. Species identification took place in the field, and at most sites a small fin clip from the caudal fin was taken and stored in 96% ethanol. Only adult fish, clearly identified to species, were sampled. Each population sample consisted of fish collected the same day. Different populations (within and across geographical regions), however, were collected across study years (Table 1). There was no major flood between 2008 and 2012 that would cause a dispersal of fish or eggs across populations. A subsample of captured fish was stored in 5% formaldehyde or 80% ethanol for further reference and phenotype analyses while most fish were released back into the pool. Two GRZ (type locality) specimens were obtained from the breeding stock in Leibniz Institute for Age Research, Jena, Germany. For genetic analysis, N. furzeri populations from 36 pools (= localities) were selected which cover the entire known species range (Table 1, Figure 1). Adjacent savannah pools were generally omitted, except for two regions where analyses focussed on small-scale structuring. All fieldwork complied with legal regulations of Mozambique (collection permit 154/II/2009/DARPPE and sample export permit 049MP00518-A/09 of the Mozambican Ministry of Fisheries).


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)

Map showing the distribution of 36 sample sites. Different symbols indicate the distribution of three main mtDNA haplogroups (called Chefu, LimpN, and LimpS). Numbers of localities correspond to Table 1. Haplotypes from the two haplogroups (Chefu and LimpN) were found in Pop406 (marked by the green arrow). Note that LimpS includes the localities from both the Limpopo and Incomati basins. Black arrow shows the position of the locality at Gona Re Zhou National Park in Zimbabwe (GRZ) that was excluded from some analyses because the individuals originated from a captive population. The inset figures show the position of the study area within Africa and Mozambique.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Map showing the distribution of 36 sample sites. Different symbols indicate the distribution of three main mtDNA haplogroups (called Chefu, LimpN, and LimpS). Numbers of localities correspond to Table 1. Haplotypes from the two haplogroups (Chefu and LimpN) were found in Pop406 (marked by the green arrow). Note that LimpS includes the localities from both the Limpopo and Incomati basins. Black arrow shows the position of the locality at Gona Re Zhou National Park in Zimbabwe (GRZ) that was excluded from some analyses because the individuals originated from a captive population. The inset figures show the position of the study area within Africa and Mozambique.
Mentions: Fish were collected during 8 field trips between 2008 and 2012, visiting 336 individual savannah pools across southern and central Mozambique, with the aim of sampling pools across the entire savannah habitat in that region. From a total of 163 pools populated by Nothobranchius spp., 73 pools were inhabited by N. furzeri, all of them south of the River Save (Figure 1). Fish were collected using dip and Seine nets. Species identification took place in the field, and at most sites a small fin clip from the caudal fin was taken and stored in 96% ethanol. Only adult fish, clearly identified to species, were sampled. Each population sample consisted of fish collected the same day. Different populations (within and across geographical regions), however, were collected across study years (Table 1). There was no major flood between 2008 and 2012 that would cause a dispersal of fish or eggs across populations. A subsample of captured fish was stored in 5% formaldehyde or 80% ethanol for further reference and phenotype analyses while most fish were released back into the pool. Two GRZ (type locality) specimens were obtained from the breeding stock in Leibniz Institute for Age Research, Jena, Germany. For genetic analysis, N. furzeri populations from 36 pools (= localities) were selected which cover the entire known species range (Table 1, Figure 1). Adjacent savannah pools were generally omitted, except for two regions where analyses focussed on small-scale structuring. All fieldwork complied with legal regulations of Mozambique (collection permit 154/II/2009/DARPPE and sample export permit 049MP00518-A/09 of the Mozambican Ministry of Fisheries).

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