Complete mitochondrial DNA replacement in a Lake Tanganyika cichlid fish

Abstract

We used nuclear and mitochondrial DNA (mtDNA) sequences from specimens collected throughout Lake Tanganyika to clarify the evolutionary relationship between Lamprologus callipterus and Neolamprologus fasciatus. The nuclear data support the reciprocal monophyly of these two shell-breeding lamprologine cichlids. However, mtDNA sequences show that (i) L. callipterus includes two divergent and geographically disjunct (North-South) mtDNA lineages; and that (ii) N. fasciatus individuals cluster in a lineage sister group to the northern lineage of L. callipterus. The two mtDNA lineages of L. callipterus diverged c. 684 kya to 1.2 Ma, coinciding with a major water level low stand in Lake Tanganyika, which divided the lake into isolated sub-lakes. This suggests that the two mtDNA lineages originated as the result of the separation of L. callipterus populations in different sub-basins. The incongruent phylogenetic position of N. fasciatus can best be explained by an ancient unidirectional introgression from L. callipterus into N. fasciatus. Remarkably, our data indicate that this event resulted in the complete mtDNA replacement in N. fasciatus. Our data suggest that hybridization occurred soon after the divergence of the two L. callipterus mtDNA lineages, probably still during the water level low stand, and that subsequently the invading mtDNA lineage spread throughout the lake.

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

“…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). In contrast, two species that are less strictly restricted to rocky habitat (Lamprologus callipterus and Neolamprologus fasciatus) exhibit clear phylogeographic structure but shallower intraspecific divergence (Nevado et al, 2009), and a highly mobile benthopelagic species (Boulengerochromis microlepis) shows no phylogeographic structure on a lake-wide scale and very shallow intraspecific divergence (Koblmüller et al, 2015a). Similarly, in Lake Malawi, the pelagic species Diplotaxodon limnothrissa shows no phylogeographic structure on a lake-wide scale (Shaw et al, 2000).…”

“…The complete mitochondrial NADH dehydrogenase subunit 2 gene (ND2; 1,047 bp) was amplified and sequenced using the primers Met, ND2.2A, Trp and ND2.T-R in four A. calvus and nine A. compressiceps samples. Furthermore, four nuclear genes (ITS, 1,306 bp; LSU, 676 bp; RAG1 intron 2, 928 bp; RAG1 exon 3, 828 bp) were amplified and sequenced for three A. calvus and eight A. compressiceps according to Nevado et al (2009), using the primers ITS_18D, ITS_28C, ITS_5.8C (ITS; Nevado et al, 2009), LSU_F1, LSU_R1 (LSU; Sonnenberg et al, 2007), KALIF1, CR1, CF1 and CR5 (RAG1 (red, A. calvus; blue, A. compressiceps; green, A. sp. ''shell'').…”

“…Sequences were aligned by eye (protein coding sequences) or using MUSCLE (Edgar, 2004) (for non-coding sequences and rDNA) as implemented in Mega 6.05 (Tamura et al, 2013). Our newly generated sequence data were complemented with previously published sequences of 'ossified group' lamprologines and outgroup taxa Schelly et al, 2006;Koblmüller et al, 2007b;Nevado et al, 2009), downloaded from Genbank (Supplementary Table 2). New sequences are deposited in GenBank (for GenBank accession numbers, see Supplementary Tables 1 and 2).…”

“…Significant genetic differentiation can evolve among fragmented populations within relatively short periods of time. However, large-scale phylogeographic patterns have been shown to be influenced by the long-term history of the species, including range shifts and introgression among differentiated lineages during secondary contact in the course of lake level fluctuations (Verheyen et al, 1996;Sturmbauer et al, 2001;Egger et al, 2007;Nevado et al, 2009). Therefore, distinct population genetic structure may, but need not, go along with a clear-cut phylogeographic pattern; and vice versa, species with high levels of gene flow across the geographical scale of previous population genetic studies may still be genetically structured on a larger scale.…”

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

“…'black' (Van Steenberge, 2014), our new AFLP data, in concordance with Egger et al (2007), do not find evidence for large-scale genomic admixture in these introgressed populations. There is increasing evidence that in animals local or even range wide replacement of mitochondrial DNA, without signatures of nuclear genomic admixis, seems to be more common than previously thought (e.g., Nevado et al, 2009;Tang et al, 2012;Melo-Ferreira et al, 2014;Good et al, 2015;Koblmüller et al, 2016), such that taxonomic assignment based on mitochondrial data alone might be misleading.…”