Repeated Unidirectional Introgression of Nuclear and Mitochondrial DNA Between Four Congeneric Tanganyikan Cichlids

Abstract

With an increasing number of reported cases of hybridization and introgression, interspecific gene flow between animals has recently become a widely accepted and broadly studied phenomenon. In this study, we examine patterns of hybridization and introgression in Ophthalmotilapia spp., a genus of cichlid fish from Lake Tanganyika, using mitochondrial and nuclear DNA from all four species in the genus and including specimens from over 800 km of shoreline. These four species have very different, partially overlapping distribution ranges, thus allowing us to study in detail patterns of gene flow between sympatric and allopatric populations of the different species. We show that a significant proportion of individuals of the lake-wide distributed O. nasuta carry mitochondrial and/or nuclear DNA typical of other Ophthalmotilapia species. Strikingly, all such individuals were found in populations living in sympatry with each of the other Ophthalmotilapia species, strongly suggesting that this pattern originated by repeated and independent episodes of genetic exchange in different parts of the lake, with unidirectional introgression occurring into O. nasuta. Our analysis rejects the hypotheses that unidirectional introgression is caused by natural selection favoring heterospecific DNA, by skewed abundances of Ophthalmotilapia species or by hybridization events occurring during a putative spatial expansion in O. nasuta. Instead, cytonuclear incompatibilities or asymmetric behavioral reproductive isolation seem to have driven repeated, unidirectional introgression of nuclear and mitochondrial DNA into O. nasuta in different parts of the lake.

The puzzling phylogeography of the haplochromine cichlid fishAstatotilapia burtoni

“…Given the deep nuclear DNA (ncDNA) divergence between the northern and southern lineages, this pattern in mtDNA is difficult to explain. On the other hand, evidence is accumulating that the replacement of mtDNA across large geographic distances, without apparent signatures of nuclear genomic admixis is more common than previously thought (e.g., Good, Vanderpool, Keeble, & Bi, 2015; Melo‐Ferreira, Seixas, Cheng, Mills, & Alves, 2014; Nevado, Fazalova, Backeljau, Hanssens, & Verheyen, 2011; Tang, Liu, Yu, Liu, & Danley, 2012). 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).…”

An Important Natural Genetic Resource of Oreochromis niloticus (Linnaeus, 1758) Threatened by Aquaculture Activities in Loboi Drainage, Kenya

“…Recently STRUCTURE has been used [44], [45] to quantify in more details the proportion of individual's genome originating from a different hybridizing species in tilapia from Lake Victoria and in Cichlids from Lake Tanganyika, respectively. Results obtained by these authors concern tilapia species from the Lake Victoria region: O. niloticus and O. esculentus .…”

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

“…Such recent speciation is unusual for Lake Tanganyika cichlids, in which species typically represent reciprocally monophyletic lineages separated by substantial genetic distances (Koblmüller et al, 2004(Koblmüller et al, , 2007cDuftner et al, 2005), except when subject to interspecific introgression (e.g. Rüber et al, 2001;Koblmüller et al, 2007b;Sturmbauer et al, 2010;Nevado et al, 2011). Divergence between the two Altolamprologus species was inferred to have proceeded with little if any gene flow (Table 2), which attributes their polyphyletic relationship mainly to incomplete lineage sorting.…”

“…Mitochondrial replacement in isolated populations and even in entire species is being inferred in an increasing number of taxa (e.g. Nevado et al, 2011;Tang et al, 2012;Melo-Ferreira et al, 2014;Good et al, 2015), including lamprologines (Schelly et al, 2006;Nevado et al, 2009). Lamprologine species can produce interspecific offspring for long periods of time following their divergence (Koblmüller et al, 2007b;Sturmbauer et al, 2010), which may explain the frequency of interspecific introgressions detected in this group.…”