Genetic linkage of distinct adaptive traits in sympatrically speciating crater lake cichlid fish

Abstract

Our understanding of how biological diversity arises is limited, especially in the case of speciation in the face of gene flow. Here we investigate the genomic basis of adaptive traits, focusing on a sympatrically diverging species pair of crater lake cichlid fishes. We identify the main quantitative trait loci (QTL) for two eco-morphological traits: body shape and pharyngeal jaw morphology. These traits diverge in parallel between benthic and limnetic species in the repeated adaptive radiations of this and other fish lineages. Remarkably, a single chromosomal region contains the highest effect size QTL for both traits. Transcriptomic data show that the QTL regions contain genes putatively under selection. Independent population genomic data corroborate QTL regions as areas of high differentiation between the sympatric sister species. Our results provide empirical support for current theoretical models that emphasize the importance of genetic linkage and pleiotropy in facilitating rapid divergence in sympatry.

Figure 1. Nicaraguan lakes and benthic/limnetic Midas cichlids.

The lake indicated is the crater lake Apoyo. In the inset, pictures of representative specimens of A. astorquii and A. zaliosus, and of typical lower pharyngeal jaws of these species.

Figure 2. QTL mapping.

(a) Bayesian credibility intervals for QTL in LG 3: orange bars for body shape; green bars for pharyngeal jaw shape; violet bar for covariation of body shape and pharyngeal jaw shape. (b) LOD scores at each position in each LG obtained by mapping PLS scores (covariation). The horizontal line identifies the genome-wide significance threshold obtained through permutations (at LOD=3.52). (c) Covariation accounted for by the only QTL (on LG 3) with LOD score higher than the genome-wide significance threshold.

Figure 3. Population genomics.

Manhattan plot of genome-wide differentiation between sympatric Midas species (significance levels for the Fisher test), including regions that co-localize with QTL. Only genomic windows containing RAD markers in the linkage map are plotted. The horizontal line represents a significance threshold obtained from the multiple test correction procedure (−Log₁₀ (P-value)=1.49). Coloured stars represent genomic windows significantly differentiated between species and located in QTL regions (orange for body shape, green for pharyngeal jaw shape). SNPs not located in QTL regions are represented in grey or black, alternating these two colors so that the LGs are distinguishable.