Abstract
The formation of species in the absence of geographic barriers (i.e. sympatric speciation) remains one of the most controversial topics in evolutionary biology. While theoretical models have shown that this most extreme case of primary divergence-with-gene-flow is possible, only a handful of accepted empirical examples exist. And even for the most convincing examples uncertainties remain; complex histories of isolation and secondary contact can make species falsely appear to have originated by sympatric speciation. This alternative scenario is notoriously difficult to rule out. Midas cichlids inhabiting small and remote crater lakes in Nicaragua are traditionally considered to be one of the best examples of sympatric speciation and lend themselves to test the different evolutionary scenarios that could lead to apparent sympatric speciation since the system is relatively small and the source populations known. Here we reconstruct the evolutionary history of two small-scale radiations of Midas cichlids inhabiting crater lakes Apoyo and Xiloá through a comprehensive genomic data set. We find no signs of differential admixture of any of the sympatric species in the respective radiations. Together with coalescent simulations of different demographic models our results support a scenario of speciation that was initiated in sympatry and does not result from secondary contact of already partly diverged populations. Furthermore, several species seem to have diverged simultaneously, making Midas cichlids an empirical example of multispecies outcomes of sympatric speciation. Importantly, however, the demographic models strongly support an admixture event from the source population into both crater lakes shortly before the onset of the radiations within the lakes. This opens the possibility that the formation of reproductive barriers involved in sympatric speciation was facilitated by genetic variants that evolved in a period of isolation between the initial founding population and the secondary migrants that came from the same source population. Thus, the exact mechanisms by which these species arose might be different from what had been thought before.
Highlights
Understanding how populations can diverge and become distinct species in the presence of gene flow is a central objective in evolutionary biology [1,2,3]
While this pattern might suggest secondary contact and hybridization, the f3-statistics do not support this explanation. This signal of admixed ancestry did disappear in the Admixture analyses when assuming more than four clusters (S1 Fig). We propose that this pattern in the global Principal Component Analyses (PCAs) might rather reflect a difference in population sizes; our demographic models suggest that the population sizes of A. amarillo and A. viridis have been larger than the other two species and they may have retained more of the ancestral variation
Unlike recent evidence presented for Cameroonian crater lake cichlids [34], our population clustering and phylogenetic analyses are consistent with a scenario of primary divergence-with-gene-flow of the crater lake species
Summary
Understanding how populations can diverge and become distinct species in the presence of gene flow is a central objective in evolutionary biology [1,2,3]. Without a good understanding of the populations’ past it is, often difficult to distinguish between primary divergence-with-gene-flow and the sorting out of already partly diverged populations after secondary contact [3, 14]. This distinction is important as the latter involves a period of geographic isolation in which the abovementioned problem of gene flow and recombination does not arise [2, 15]. In other words, is geographic isolation necessary to reduce gene flow and initiate population divergence in the first place or can speciation commence in a panmictic population? sympatric speciation has for long attracted theoreticians and empiricists alike, not because it is believed to occur frequently, but because—being the endpoint of the continuum of primary divergence-withgene-flow—it may be informative on the ecological conditions and evolutionary mechanisms that can lead to speciation in the presence of gene flow [19, 22, 23]
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