Separated by sand, fused by dropping water: habitat barriers and fluctuating water levels steer the evolution of rock-dwelling cichlid populations in Lake Tanganyika

Abstract

The conditions of phenotypic and genetic population differentiation allow inferences about the evolution, preservation and loss of biological diversity. In Lake Tanganyika, water level fluctuations are assumed to have had a major impact on the evolution of stenotopic littoral species, though this hypothesis has not been specifically examined so far. The present study investigates whether subtly differentiated colour patterns of adjacent Tropheus moorii populations are maintained in isolation or in the face of continuous gene flow, and whether the presumed influence of water level fluctuations on lacustrine cichlids can be demonstrated in the small-scale population structure of the strictly stenotopic, littoral Tropheus. Distinct population differentiation was found even across short geographic distances and minor habitat barriers. Population splitting chronology and demographic histories comply with our expectation of old and rather stable populations on steeper sloping shore, and more recently established populations in a shallower region. Moreover, population expansions seem to coincide with lake level rises in the wake of Late Pleistocene megadroughts ~100 KYA. The imprint of hydrologic events on current population structure in the absence of ongoing gene flow suggests that phenotypic differentiation among proximate Tropheus populations evolves and persists in genetic isolation. Sporadic gene flow is effected by lake level fluctuations following climate changes and controlled by the persistence of habitat barriers during lake level changes. Since similar demographic patterns were previously reported for Lake Malawi cichlids, our data furthermore strengthen the hypothesis that major climatic events synchronized facets of cichlid evolution across the East African Great Lakes.

The puzzling phylogeography of the haplochromine cichlid fish Astatotilapia burtoni

“…More general, discordance between nuclear and mtDNA phylogenetic inferences is known from many freshwater fish taxa and attributed to their high propensity to hybridize (see Wallis et al., 2017). In particular, in stenotopic, littoral cichlids from Lake Tanganyika—such as Eretmodus cyanosticus , Tropheus moorii and Variabilichromis moorii —such mtDNA/ncDNA discordance patterns due to introgression/hybridization have been linked to lake‐level fluctuations leading to past contact zones between otherwise isolated populations and large‐scale migration events (Koblmüller et al., 2011; Nevado, Mautner, Sturmbauer, & Verheyen, 2013; Sefc, Baric, Salzburger, & Sturmbauer, 2007; Sturmbauer et al., 2001). In the genus Tropheus , for example, populations from opposite shorelines in the central and southern basin of Lake Tanganyika have been shown to share identical mtDNA haplotypes (Sturmbauer, Koblmuller, Sefc, & Duftner, 2005; Sturmbauer et al., 2001).…”

“…The observed distribution of the main mtDNA haplotype lineages was interpreted to reflect past lake‐level oscillations (Theis et al., 2014). Such fluctuations in the lake level, caused by variation in hydrology through time (Cohen, Lezzar, Tiercelin, & Soreghan, 1997; McGlue et al., 2010; Scholz et al., 2007), have previously been documented to affect population dynamics in rock‐dwelling, littoral cichlid species from lakes Tanganyika (Baric, Salzburger, & Sturmbauer, 2003; Koblmüller et al., 2011; Sturmbauer, Baric, Salzburger, Rüber, & Verheyen, 2001) and Malawi (Genner, Knight, Haesler, & Turner, 2010). In a follow‐up study based on single nucleotide polymorphisms (SNPs) derived from genomic DNA (via restriction site‐associated DNA sequencing; RADseq), we confirmed a deep divergence in A. burtoni populations in the South of Lake Tanganyika, in this case, however, between the Lufubu River and all remaining populations including the fish sampled at the estuary of the Lufubu River (Egger et al., 2017).…”

A separate lowstand lake at the northern edge of Lake Tanganyika? Evidence from phylogeographic patterns in the cichlid genus Tropheus

“…For all 152 new samples, the most variable part of the mitochondrial control region was amplified and sequenced following Koblmüller et al (2011) and Duftner et al (2005), respectively. The primers used for PCR amplification and chain termination sequencing were L-Pro-F (Meyer et al, 1994) and TDK-D (Lee et al, 1995).…”

“…A series of previous studies on the evolution and colonization history of this genus set out to reconstruct the origin and spread of this highly specialized rockdwelling species-complex (Sturmbauer & Meyer, 1992;Sturmbauer et al, 1997;Rüber et al, 1999;Baric et al, 2003;Sturmbauer et al, 2005;Egger et al, 2007;Sefc et al, 2007Koblmüller et al, 2011;Nevado et al, 2013). These studies suggested mitochondrial introgression, sometimes on a small scale between presently allopatric populations, sometimes on a large-scale producing true hybrid populations, at various time points in the evolutionary history of the genus Tropheus.…”

“…Most of these events of population displacement were triggered by lake level fluctuations, which extended to a few hundred meters below present level (Lezzar et al, 1996;Cohen et al, 1997;Scholz et al, 2003;McGlue et al, 2008). While the effect is widely seen in population genetic studies on various Lake Tanganyika cichlid species (Verheyen et al, 1996;Rüber et al, 1999Rüber et al, , 2001Duftner et al, 2006;Koblmüller et al, 2007Koblmüller et al, , 2009Koblmüller et al, , 2011Sefc et al, 2007;Nevado et al, 2013;Van Steenberge et al, 2015), studies specifically testing for the impact of Pleistocene water level fluctuations are scarce (Koblmüller et al, 2011;Winkelmann et al, 2016).…”