Searching for Sympatric Speciation in the Genomic Era

Abstract

Sympatric speciation illustrates how natural and sexual selection may create new species in isolation without geographic barriers. However, recent genomic reanalyses of classic examples of sympatric speciation reveal complex histories of secondary gene flow from outgroups into the radiation. In contrast, the rich theoretical literature on this process distinguishes among a diverse range of models based on simple genetic histories and different types of reproductive isolating barriers. Thus, there is a need to revisit how to connect theoretical models of sympatric speciation and their predictions to empirical case studies in the face of widespread gene flow. Here, theoretical differences among different types of sympatric speciation and speciation-with-gene-flow models are reviewed and summarized, and genomic analyses are proposed for distinguishing which models apply to case studies based on the timing and function of adaptive introgression. Investigating whether secondary gene flow contributed to reproductive isolation is necessary to test whether predictions of theory are ultimately borne out in nature.

Keywords: cichlids; gene flow; genomics; introgression; selection; sympatric speciation.

Figure 1:. Genomic signatures of sympatric speciation and speciation with gene flow.

Speciation scenarios are grouped into hard sympatric speciation scenarios (yellow box; harder process in theoretical models) and other divergence scenarios which can also occur in sympatry (red box; easier processes, which we refer to broadly as sympatric divergence here). Speciation from a hybrid swarm (orange box) can fall under either class of scenarios and additional information is necessary to determine what category of speciation models best describe this process. A) The timing of gene flow relative to divergence can be used to distinguish between speciation scenarios. The colored arrows represent gene flow events and the colored lines within the tree are simplified representations of a signature of introgression from that gene flow event into the sympatric species. B) Venn diagrams illustrating the number of genomic windows across the entire genome expected to have overlapping signatures of introgression (e.g. f_d outliers), genetic divergence (e.g. F_st and D_xy outliers), and selective sweeps (e.g. SweeD) for each speciation scenario (e.g. see (Richards & Martin 2017)). The highlighted sections of the Venn diagrams indicate the key signature that can be used to distinguish between the scenarios. The scenarios that are expected to leave very similar signatures of overlap are grouped by the bars colored with their respective Venn diagram.

Fig I.

Two equilibrium cases exist for the linkage disequilibrium (LD), a proxy for differentiation into two distinct “species” in this proof-of-concept model, that can be maintained between two loci that are under disruptive selection and determine assortative mating. With little initial LD, the one-species equilibrium is likely to be reached even when the intensity of assortment is high. When LD in the traits is initially large, as can be the case if there is initially divergence in allopatry, the two-species equilibrium can be reached instead. Modified from (Kirkpatrick & Ravigné 2002).

Fig. II

Examples of volcanic crater lakes containing endemic cichlid radiations around the globe: a,d,f) Barombi Mbo, Cameroon and its only outlet stream; b) Lake Apoyo, Nicaragua, c) Lake Massoko, Tanzania, e) Lake Bermin, Cameroon. Satellite images (a-c) from Google Earth; (d-f) by CHM.