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

Abstract

BackgroundIntraspecific 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.ResultsGenetic 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.ConclusionsWe 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.

The African turquoise killifish: A research organism to study vertebrate aging and diapause

“…The turquoise killifish strain that is most frequently used is the GRZ strain, an inbred line that originates from a sample collected in 1970 in the Gona‐Re‐Zhou National Park of Zimbabwe (Parle, 1970). Since then, several additional samples have been collected in Mozambique and Zimbabwe, and wild strains or strains derived from these samples (e.g., the MZM0403 and 0410 strains which were collected in 2004) have also been broadly used for a variety of studies (Bartakova et al., 2013; Baumgart et al., 2016; Blazek et al., 2017; Kirschner et al., 2012; Reichard, Polacik & Sedlacek, 2009; Reichwald et al., 2015; Terzibasi et al., 2008; Valenzano et al., 2009, 2015). In particular, these strains were used to identify the genetic architecture underlying phenotypic differences in these strains, such as color (Valenzano et al., 2009) and survival under specific laboratory environments (Baumgart et al., 2016; Blazek et al., 2017; Reichwald et al., 2015; Valenzano et al., 2015).…”

“…The turquoise killifish naturally live in ephemeral ponds in Mozambique and Zimbabwe where water is only present during the brief rainy season. The rainy season is followed by a prolonged dry season, during which the ponds entirely dry up (Bartakova et al., 2013; Furzer, 1969; Jubb, 1969, 1971; Reichard et al., 2009). This extreme habitat challenges the inhabiting species not only to propagate fast within the short rainy season, but also to survive through the following long dry season.…”

Female fecundity traits in wild populations of African annual fish: the role of the aridity gradient

“…2; Bartáková et al. 2013, 2015). In total, we analyzed 141  N. furzeri females belonging to Chefu and 66 to Limpopo mitochondrial lineage.…”

“…Aridity index approximated the expected lifespan along the climatic gradient, and genetic structure controlled for independent evolution of traits and their trade‐offs within mitochondrial lineages (Bartáková et al. 2013, 2015; Valenzano et al. 2015).…”

“…Nothobranchius populations are highly genetically structured (Bartáková et al. 2013, 2015), allowing potential evolution of different life‐history optima. Hence, populations across the aridity gradient differ in their life expectancy and interpopulation lifespan differences were recorded in captivity (Terzibasi et al.…”