Past lake shore dynamics explain present pattern of unidirectional introgression across a habitat barrier

Abstract

Introgression patterns between divergent lineages are often characterized by asymmetry in the direction and among-marker variation in the extent of gene flow, and therefore inform on the mechanisms involved in differentiation and speciation. In the present study, we test the hypothesis that unidirectional introgression between two phenotypically and genetically distinct lineages of the littoral, rockdwelling cichlid fish Tropheus moorii across a wide sandy bay is linked to observed differences in mate preferences between the two lineages. This hypothesis predicts bi-directional nuclear gene flow and was rejected by congruent patterns of introgression in mtDNA, AFLP and microsatellite markers, with admixture confined to the populations west of the bay. This pattern can be explained on the basis of habitat changes in the course of lake level fluctuations, which first facilitated the development of a symmetric admixture zone including the area corresponding to the present sand bay and then shaped asymmetry by causing local extinctions and cessation of gene flow when this area became once more inhabitable. This conforms with previous assumptions that habitat dynamics are a primary determinant of populationlevel evolution in Tropheus. In this respect, Tropheus may be representative of species whose preferred habitat is subject to frequent re-structuring.

Phylogeny and phylogeography of Altolamprologus: ancient introgression and recent divergence in a rock-dwelling Lake Tanganyika cichlid genus

“…The stenotopic rock-dwelling genus Tropheus from Lake Tanganyika is one example in which both population genetic and lake-wide phylogeographic studies have been conducted. In this fish, strong small-scale population differentiation contrasts with evidence for ancient introgression among phylogenetically old lineages Sefc et al, 2007;Egger et al, 2007;Koblmüller et al, 2011;Sefc et al, 2016). A similar picture-deep intraspecific divergences and past introgression among geographically distant populations-emerged in a phylogeographic study of another rock-dwelling cichlid of Lake Tanganyika, the Neolamprologus brichardi/pulcher complex (Duftner et al, 2007).…”

“…Simultaneous expansions have also been inferred in other rock-dwelling cichlids from Lake Tanganyika (Koblmüller et al, 2011;Nevado et al, 2013;Winkelmann et al, 2016;Sefc et al, 2016) and Lake Malawi (Genner & Turner, 2015;Husemann et al, 2015), suggesting synchronization by an external trigger, such as habitat expansion during a lake level rise after a major drought period. Throughout their history, both Lake Tanganyika and Lake Malawi experienced numerous severe lake level fluctuations with drops of several hundred metres below the current level, which drastically altered the distribution and extent of littoral habitat types (e.g.…”

“…In rock-dwelling cichlids, dispersal is often restricted by habitat barriers such as sandy beaches (Rico & Turner, 2002;Sefc et al, 2007Sefc et al, , 2016Koblmüller et al, 2011) and fish remain confined within their native rock patch. Because populations are isolated from each other, different genetic lineages can persist and diverge within species.…”

“…Smaller fluctuations in the more recent past, especially the lake level drop of *260 m during the last glacial maximum (*20 KYA), also had a profound impact on the current genetic structure of rock-dwelling cichlid species Scholz et al, 2007;McGlue et al, 2008). We have previously noted difficulties in aligning molecular datings of population divergence and growth with the geological datings of lake level fluctuations (Koblmüller et al, 2011;Sefc et al, 2016); in particular, the age of recent demographic events may be overestimated due to the potential time dependency of the molecular clock (Ho et al, 2007) in combination with comparatively ancient calibration points ) and large confidence intervals around substitution rates inferred from recent events (Genner et al, 2010b). In this light, although the reconstructed dates do not match exactly, divergence between A. compressiceps and A. calvus and the first wave of population expansion in A. compressiceps may be connected with lake level fluctuations during the megadroughts, and the more recent population size expansions in A. compressiceps and A. calvus may be associated with fluctuations during the last glacial maximum.…”

“…In the two East African lakes Malawi and Tanganyika, stenotopic cichlid species inhabiting the discontinuous rocky littoral consistently show remarkable genetic population differentiation, even across very short geographic distances (e.g. van Oppen et al, 1997;Markert et al, 1999;Rico & Turner, 2002;Pereyra et al, 2004;Duftner et al, 2006;Koblmüller et al, 2011;Sefc et al, 2007;Wagner & McCune, 2009;Nevado et al, 2013;Van Steenberge et al, 2015;Sefc et al, 2016). Differentiation is lower and only occurs on a larger geographic scale in less specialized species and species that inhabit the intermediate habitat, i.e.…”