Structure Versus Speciation
Speciation and structure may occasionally present superficially similar patterns but can theoretically be distinguished by mechanistic hypothesis testing of the underlying processes. Furthermore, the empirical “gray zone” of speciation is oftentimes fairly binary and sharply demarcated (Roux et al. 2016; Dufresnes et al. 2021). When relevant axes such as genomic divergence, ecological adaptation, migration, and phenotypic differentiation are accounted for, an integrative evaluation of speciation hypotheses can discern between the two (Freedman et al. 2023; Prates et al. 2023; Pyron et al. 2023). When divergent ecomorphological selection is driving ecological speciation, we would expect correlated genomic signatures of genetic and phenotypic divergence along environmental axes and reduced rates of migration (e.g., Orsini et al. 2013). In contrast, limited phenotypic diversity and high rates of migration can allow for the long-term persistence of deeply divergent phylogeographic lineages and geographic genetic diversity within genomically cohesive single species over long periods of time (e.g., Postma and van Noordwijk 2005; Kremer et al. 2012; Fitzpatrick et al. 2015).
Correspondingly, we emphasize that the type of deep population structure we describe here is not necessarily simply a point along the speciation continuum (Stankowski and Ravinet 2021) but a distinct pattern resulting from similar processes. The forces we hypothesize to be driving genetic divergence (microhabitat specificity) also limit ecomorphological diversification and promote recurrent secondary contact during glacial cycles as populations expand and contract in and out of physical proximity. We suggest that such mechanisms can generate substantial amounts of stable or enduring phylogeographic diversity that is not intrinsically on a path to speciation (Huang 2020), rather than simply an intermediate or incipient phase along the speciation continuum (Dufresnes et al. 2019). Consequently, this suggests a model in which the underlying processes that generate geographic genetic diversity are similar, but the outcomes of stable or persistent population structure versus ecological speciation differ (Nosil et al. 2009). In the latter, a gray zone of incipient or incomplete speciation along the continuum of ecomorphological divergence may also sometimes be observed (Huang and Knowles 2016).
Ecological speciation may occur via many routes, but any mechanism that promotes high rates of continued migration may act against those processes and maintain population structure without speciation. This is important, given that even extremely low rates of migration (i.e., <<1/generation) can lead to the substantial signal of introgression across the genome (Jiao et al. 2020; Jiao and Yang 2021). While it may not necessarily be easy to distinguish complex spatial and temporal patterns of structure versus speciation (DeRaad et al. 2022; Prates et al. 2023), we provide a framework here for attempting to do so in future studies. Combining analyses of migration, spatial demographics, and adaptive ecomorphological divergence allows us to test for structure versus speciation, conduct species delimitation, and identify potential underlying mechanism and process of speciation itself (Maier et al. 2019; Smith and Carstens 2020; Burbrink et al. 2021; O’Connell et al. 2021; Freedman et al. 2023; Pyron et al. 2023).