Contrasting signatures of genomic divergence during sympatric speciation

Abstract

The transition from ‘well-marked varieties’ of a single species into ‘well-defined species’—especially in the absence of geographic barriers to gene flow (sympatric speciation)—has puzzled evolutionary biologists ever since Darwin1,2. Gene flow counteracts the buildup of genome-wide differentiation, which is a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that complete the speciation process3. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs4, but empirical tests of this theory are scant because comprehensive data are difficult to collect and synthesize across species, owing to their unique biologies and evolutionary histories5. Here, within a young species complex of neotropical cichlid fishes (Amphilophus spp.), we analysed genomic divergence among populations and species. By generating a new genome assembly and re-sequencing 453 genomes, we uncovered the genetic architecture of traits that have been suggested to be important for divergence. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. By contrast, differentiation among species that have diverged in polygenic traits is genomically widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Thus, we conclude that simple trait architectures are not always as conducive to speciation with gene flow as previously suggested, whereas polygenic architectures can promote rapid and stable speciation in sympatry.

Different Sources of Allelic Variation Drove Repeated Color Pattern Divergence in Cichlid Fishes

“…2019 ; Marques et al. 2019 ; Kautt et al forthcoming ). By a comprehensive analysis of the “stripe locus” with its well-resolved genotype–phenotype connection, we provide additional insights into how ancestral standing genetic variation at the root of adaptive radiations can facilitate rapid phenotypic divergence within species flocks.…”

“…2019 ; Svardal et al. 2020 ; Kautt et al, forthcoming ). However, with a few exceptions ( Colosimo et al.…”

Diversification dynamics and (non-)parallel evolution along an ecological gradient in African cichlid fishes

“…First, the outlier detection method based on lake-stream differences might not be the most appropriate to uncover the genomic basis of morphological evolution. A quantitative traits loci approach might be more appropriate, as has previously been applied to uncover genomic regions underlying body shape differences along a benthic-limnetic axis of differentiation in Midas cichlids ( 55, 56 ). Second, while body shape convergence may be due to adaptive genomic divergence, adaptive phenotypic plasticity also plays a role in body shape evolution.…”

Selection on old variants drives adaptive radiation ofMetrosiderosacross the Hawaiian Islands

“…These patterns contrast with the genetic architecture observed for key traits in animal adaptive radiations. For instance, in butterflies (Nadeau et al 2014), crows (Vijay et al 2016), and cichlids (Kautt et al 2020) where adaptive radiation involves different color morphs, few genomic regions are strongly differentiated due to the simple genetic architecture of color-based traits, which also contribute to assortative mating and further builds up differentiation (Servedio et al 2011). In animal adaptive radiations, in general, differentiation is seemingly localized to a few genomic regions with prominent, broad peaks (Poelstra et al 2014; Malinsky et al 2015; Lamichhaney et al 2015).…”