Abstract
Genomic data has revealed complex histories of colonization and repeated gene flow previously unrecognized in some of the most celebrated examples of sympatric speciation and radiation. However, much of the evidence for secondary gene flow into these radiations comes from summary statistics calculated from sparse genomic sampling without knowledge of which specific genomic regions introgressed. This tells us little about how gene flow potentially influenced sympatric diversification. Here, we investigated whole genomes of Barombi Mbo crater lake cichlids for fine‐scale patterns of introgression with neighboring riverine cichlid populations. We found evidence of secondary gene flow into the radiation scattered across <0.24% of the genome; however, from our analyses, it is not clear if the functional diversity in these regions contributed to the ecological, sexual, and morphological diversity found in the lake. Unlike similar studies, we found no obvious candidate genes for adaptive introgression and we cannot rule out that secondary gene flow was predominantly neutral with respect to the diversification process. We also found evidence for differential assortment of ancestral polymorphisms found in riverine populations between sympatric sister species, suggesting the presence of an ancestral hybrid swarm. Although the history of gene flow and colonization is more complicated than previously assumed, the lack of compelling evidence for secondary gene flow's role in species diversification suggests that we should not yet rule out one of the most celebrated examples of sympatric speciation in nature without a more thorough investigation of the timing and functional role of each introgressed region.
Highlights
Sympatric speciation, the endpoint on the speciation-with-geneflow continuum, is defined as the evolution of reproductive isolation without the aid of geographic barriers under complete panmixia and constant gene flow between diverging populations (Coyne and Orr 2004; Fitzpatrick et al 2008; Mallet et al 2009)
Since we were looking for patterns consistent with secondary gene flow or a hybrid swarm for subclades of the radiation, we focused on topologies where single species or entire subclades were more closely related to outgroups than other Barombi Mbo species, which represented only 0.24% of the genome
EQUIVOCAL EVIDENCE THAT SECONDARY GENE FLOW PROMOTED THE DIVERSIFICATION OF BAROMBI MBO CICHLIDS Our fine-scale investigations of introgression across the genomes of a celebrated putative example of sympatric speciation are consistent with two possible scenarios: (1) sympatric speciation in the presence of continuous neutral secondary gene flow into the radiation, or (2) speciation initiated by secondary gene flow; our data are not consistent with a scenario involving an extensive period of allopatry and secondary contact promoting speciation
Summary
The endpoint on the speciation-with-geneflow continuum, is defined as the evolution of reproductive isolation without the aid of geographic barriers under complete panmixia and constant gene flow between diverging populations (Coyne and Orr 2004; Fitzpatrick et al 2008; Mallet et al 2009). Even in some of the more convincing examples that do meet these criteria, genomic data have revealed more complex evolutionary histories of multiple colonization and repeated gene flow than previously assumed (Papadopolus et al 2011; The Heliconius Genome Consortium et al 2012; Geiger et al 2013; Alcaide et al 2014; Igea et al 2015; Malinsky et al 2015; Martin et al 2015a; Kautt et al 2016; Poelstra et al 2018). Gene flow detected at the genome-wide level from populations outside the sympatric radiation does not by itself constitute evidence that secondary gene flow was involved in the divergence process among incipient species and shaped the radiation
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