Searching for sympatric speciation in the genomic era

Abstract

24Sympatric speciation illustrates how natural and sexual selection may create new species in 25 isolation without geographic barriers. However, recent genomic reanalyses of classic examples 26 of sympatric speciation have revealed complex histories of secondary gene flow. Thus, there is a 27 need to revisit how to connect the diverse theoretical models of sympatric speciation and their 28 predictions to empirical case studies in the face of widespread gene flow. We summarize 29 theoretical differences between sympatric speciation and speciation-with-gene-flow models and 30 propose genomic analyses for distinguishing which models apply to case studies based on the 31 timing and function of adaptive introgression. Investigating whether secondary gene flow 32 contributed to reproductive isolation is necessary to test whether predictions of theory are 33 ultimately borne out in nature. 34 35 36 37 38 39 40 41 42 43 44 45 46 3What is sympatric speciation? 47 As Mayr famously quipped, sympatric speciation is like the Lernean Hydra: "which grew two 48 new heads whenever one of its heads was cut off" (p. 451; [1]). The latest incarnation of this 49 phenomenon has occurred over the past decade: sympatric speciation now means two different 50 things to different research groups. 51In the classic definition, sympatric speciation represents the most extreme endpoint on 52 the divergence with gene flow continuum: panmictic gene flow and no initial divergence at the 53 start of speciation [2][3][4]. In the context of theoretical speciation models, this classic process of 54 sympatric speciation is the most difficult because the starting conditions involve no pre-existing 55 divergence, potentially tied with physical linkage, among loci involved in reproductive isolation. 56 Instead, linkage disequilibrium (see Glossary) must build up through time within a population 57 through the action of disruptive natural selection and strong assortative mating by ecotype, 58 despite the countervailing eroding force of recombination [5][6][7][8]. 59Recently, the definition of sympatric speciation has been expanded to focus more on 60 biogeographical context [9], in which the speciation process is defined as sympatric a) as long as 61 diverging populations are within 'cruising range' of each other and b) regardless of whether 62 secondary gene flow provided alleles contributing to reproductive isolating barriers in sympatry. 63Cruising range provides a practical empirical definition of gene flow between diverging 64 sympatric populations, allowing for some geographic or microallopatric population structure 65 (e.g. [10,11]). However, allowing for secondary gene flow of alleles contributing some or all of 66 the reproductive isolation between sympatric populations expands the definition of sympatric 67 speciation to include both hard and easy processes under one umbrella. Theoretical models show 68 4 that speciation is much easier from starting conditions that involve some level of initial 69 divergence and/or restricted gene flow, fo...

Speciation in protists: Spatial and ecological divergence processes cause rapid species diversification in a freshwater chrysophyte

“…In general, speciation models assume that species may diverge either with or without gene flow, or by secondary contact between the diverging species (Richards, Servedio, & Martin, ). Gene flow restriction is the most commonly documented mechanism (Sobel, Chen, Watt, & Schemske, ), occurring in both spatially structured (allopatry) and well‐mixed, initially randomly mating populations (classical sympatry).…”

Don't throw out the sympatric speciation with the crater lake water: fine-scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation

“…McGirr and Martin 2018). Understanding which traits and genes are involved in speciation is now becoming the difficult problem of functional genetic analyses for anything sweeping within a population (see also Richards et al 2018).…”

Evidence for sympatric speciation in a Wallacean ancient lake

“…Similarly, the admixture before the split of O. nigrimas, if any, was also estimated to have occurred just before that split. This temporal proximity between admixture and divergence suggests that these admixtures triggered their initial sympatric divergences (Richards et al 2019). Further analyses on the functional roles of introgressed genes are necessary to test if the initial divergence between O. nebulosus and O. orthognathus, and the split of O. nigrimas as well, were triggered by the secondary gene flow from Lake Tiu.…”

“…In addition to these standard criteria, the role of introgressive hybridization due to secondary gene flow from outgroup populations in the process of sympatric speciation is recently attracting more attention because sympatric divergence could be aided by secondary gene flow (e.g., Martin et al 2015;Kautt et al 2016;Meier et al 2017;Foote 2018). For example, genetic variants supplied by secondary gene flow may be absorbed into the gene pool, leading to formation of a hybrid swarm and increased genetic variation within the population, which may be sufficient to trigger later sympatric divergence (Richards et al 2019). In contrast, population divergence might occur without reaching panmixia, which will be the case when reproductive isolation between colonists and occupants is strengthened by reinforcement and/or ecological character displacement (Seehausen 2004;Pfennig and Pfennig 2012).…”

“…In these scenarios, genetic variants from outgroups will be differentially sorted into subsequent populations. On the other hand, secondary gene flow may trigger initial sympatric divergence (Richards et al 2019), where differential admixture will not occur. In all above cases, an initial level of divergence between species is triggered by allopatric divergence; this is therefore called "gene flow induced sympatric divergence" as opposed to "hard sympatric speciation" (Richards et al 2019).…”