The puzzling phylogeography of the haplochromine cichlid fish Astatotilapia burtoni

Abstract

Astatotilapia burtoni is a member of the “modern haplochromines,” the most species‐rich lineage within the family of cichlid fishes. Although the species has been in use as research model in various fields of research since almost seven decades, including developmental biology, neurobiology, genetics and genomics, and behavioral biology, little is known about its spatial distribution and phylogeography. Here, we examine the population structure and phylogeographic history of A. burtoni throughout its entire distribution range in the Lake Tanganyika basin. In addition, we include several A. burtoni laboratory strains to trace back their origin from wild populations. To this end, we reconstruct phylogenetic relationships based on sequences of the mitochondrial DNA (mtDNA) control region (d‐loop) as well as thousands of genomewide single nucleotide polymorphisms (SNPs) derived from restriction‐associated DNA sequencing. Our analyses reveal high population structure and deep divergence among several lineages, however, with discordant nuclear and mtDNA phylogenetic inferences. Whereas the SNP‐based phylogenetic hypothesis uncovers an unexpectedly deep split in A. burtoni, separating the populations in the southern part of the Lake Tanganyika basin from those in the northern part, analyses of the mtDNA control region suggest deep divergence between populations from the southwestern shoreline and populations from the northern and southeastern shorelines of Lake Tanganyika. This phylogeographic pattern and mitochondrial haplotype sharing between populations from the very North and the very South of Lake Tanganyika can only partly be explained by introgression linked to lake‐level fluctuations leading to past contact zones between otherwise isolated populations and large‐scale migration events.

Immigrant and extrinsic hybrid inviability contribute to reproductive isolation between lake and river cichlid ecotypes

“…Taken together, our data demonstrate that the genetically most divergent and putatively ancestral river population (Pauquet et al. ) has low fitness in the lake environment and is less plastic in comparison to other river populations that are more recently derived from adjacent lake populations (Egger et al. ).…”

“…Other traits that were not investigated in this study, such as gut length, tooth morphology, and immune system in response to parasites could potentially also contribute to the observed differences in performance. Taken together, our data demonstrate that the genetically most divergent and putatively ancestral river population (Pauquet et al 2018) has low fitness in the lake environment and is less plastic in comparison to other river populations that are more recently derived from adjacent lake populations .…”

“…In the present study, we test for reproductive isolation between two lake populations and one river population. We used a lake population from the estuary of the Kalambo River (KaL) on the east coast of Lake Tanganyika, a lake population from the west coast (NdL), and a genetically divergent river population from the west coast -the Lufubu River (LfR) (referred to as Lf2 in Theis et al 2014Theis et al , 2017Egger et al 2017;Pauquet et al 2018) (Fig. 1A).…”

“…; Pauquet et al. ). Adjacent lake and river environments differ in both abiotic and biotic conditions including water chemistry, habitat structure, and prey composition (Theis et al.…”

“…1) is an excellent model to study the early phases of adaptive divergence. Lake and river ecotypes of A. burtoni show habitat specific adaptations, despite varying levels of genetic differentiation among them (Theis et al 2014;Egger et al 2017;Pauquet et al 2018). Adjacent lake and river environments differ in both abiotic and biotic conditions including water chemistry, habitat structure, and prey composition (Theis et al 2014).…”