Multispecies Outcomes of Sympatric Speciation after Admixture with the Source Population in Two Radiations of Nicaraguan Crater Lake Cichlids

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.

Author Summary

Speciation is the main driver of biological diversity and how species arise is a central question in evolutionary biology. For speciation to occur in sexually reproducing organisms the exchange of genetic material (gene flow) between populations has to be reduced. Ultimately this has to be due to genetically determined reproductive incompatibilities between species. Yet, whether (an initial period of) geographic isolation is necessary for these incompatibilities to evolve has been subject to one of the most persistent debates in evolutionary biology. Sympatric speciation is the most extreme case of primary divergence-with-gene-flow and lies at the heart of this question. However, only few empirical examples of sympatric speciation are generally accepted and in most of these cases some ambiguities and doubts remain. This study provides evidence that the Nicaraguan crater lake cichlids can indeed be considered a valid example of sympatric speciation in the sense that the species themselves probably started to diverge in the absence of geographic barriers. However, the data also suggests that this divergence in sympatry may have been facilitated by genetic variants that evolved during a time of isolation between an initial founding population and a secondary wave of colonizers stemming from the same source population. This highlights the limitations in the definitions of sympatric speciation when the mosaic nature of genomes is taken into account: some of the genetic regions driving divergence may have evolved in allopatry while the populations themselves diverged in sympatry.