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).