Establishment and expansion of Lake Malawi rock fish populations after a dramatic Late Pleistocene lake level rise

Abstract

Major environmental events that fragment populations among multiple island habitats have potential to drive large-scale episodes of speciation and adaptive radiation. A recent palaeolimnological study of sediment cores indicated that Lake Malawi underwent major climate-driven desiccation events 75,000-135,000 years ago that lowered the water level to at least 580 m below the present state and severely reduced surface area. After this period, lake levels rose and stabilized, creating multiple discontinuous littoral rocky habitats. Here, we present evidence supporting the hypothesis that establishment and expansion of isolated philopatric rock cichlid populations occurred after this rise and stabilization of lake level. We studied the Pseudotropheus (Maylandia) species complex, a group with both allopatric and sympatric populations that differ in male nuptial colour traits and tend to mate assortatively. Using coalescent analyses based on mitochondrial DNA, we found evidence that populations throughout the lake started to expand and accumulate genetic diversity after the lake level rise. Moreover, most haplotypes were geographically restricted, and the greatest genetic similarities were typically among sympatric or neighbouring populations. This is indicative of limited dispersal and establishment of assortative mating among populations following the lake level rise. Together, this evidence is compatible with a single large-scale environmental event being central to evolution of spatial patterns of genetic and species diversity in P. (Maylandia) and perhaps other Lake Malawi rock cichlids. Equivalent climate-driven pulses of habitat formation and fragmentation may similarly have contributed to observed rapid and punctuated cladogenesis in other adaptive radiations.

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

“…Because populations are isolated from each other, different genetic lineages can persist and diverge within species. However, periods of population isolation were interrupted by secondary contact due to displacements during lake level fluctuations (McGlue et al, 2008), which left signatures of introgression among distinct lineages (Verheyen et al, Genner et al, 2010b). Blue and red refer to the A. compressiceps (but excluding the aberrant northern haplogroup) and A. calvus groups, respectively.…”

“…Credibility intervals for each parameter are represented by the 95% highest posterior density (HPD) interval which is the shortest span that includes 95% of the probability density of a parameter. Parameter estimates for divergence time, rate of gene flow, as well as current and ancestral effective population sizes were translated to absolute values by employing a minimum and maximum substitution rate of 0.0324 (Genner et al, 2007(Genner et al, , 2010b and 0.057 ) per site per million years, respectively.…”

“…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.…”

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

“…Two independent MCMC chains were run for 10 6 generations, with model parameters and trees sampled every 1000 generations. We employed the HKY?G substitution model with a strict molecular clock (as we are looking at mostly intraspecific data; Brown & Yang, 2011) assuming minimum and maximum substitution rates of 3.24 and 5.7% per MY, respectively Genner et al, 2010), and a Bayesian skyline tree prior (Drummond et al, 2005). All other priors were left at default.…”

The puzzling phylogeography of the haplochromine cichlid fishAstatotilapia burtoni

“…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).…”