What can we learn from such fractal and ephemeral lineages?
In S. occidentalis , geographic isolation of two arms of expansion
maintains genetic differentiation, whereas secondary contact between
lineages leads to genetic merger and the gradual reversion of
divergence. This process is a clear example of Darwinian species
formation, where subspecies evolve into species and back. While
ephemeral lineages (i.e. varieties, subspecies, or races) challenge
binary notions of taxonomy (De Queiroz 2020), such systems have been
prized as examples of clarity for evolutionary biologists (Dobzhansky
1958). The most emblematic examples are perhaps ring species, because,
in a single system, they present the full spectrum of outcomes expected
to occur when incipient lineages come into secondary contact, from
unrestricted gene flow to full reproductive isolation (Pereira & Wake
2009). Yet, systems that have not evolved strong reproductive isolation,
such as S. occidentalis , provide important insights into the
processes that drive species divergence early in lineages’ histories.
These processes are otherwise difficult to observe. Further, the finding
that leaky genetic borders are coincident with environmental
transitions, suggests that natural selection has played a role in
population divergence, but that it is not strong enough to reduce genome
flow genome wide. Studying such permeable boundaries between taxa
remains an important task in evolutionary biology because they allow us
to identify the phenotypes and the associated genomic regions that
remain differentiated in the face of introgression, informing us about
the nature of species boundaries (Harrison & Larson 2014).
For centuries, systematists have been archiving endless forms of
ephemeral lineages in natural history museums through bird skins in
drawers, insects dried on pins, and plants on herbarium sheets. Now is
the time to revisit these classical systems to better understand
speciation. Ephemeral lineages provide an opportunity to ally
information from natural history (e.g. information on species
distribution, their environment, mating traits) to gene-level analyses
to understand both which adaptations persist despite recombination and
their underlying genetic basis. Moreover, these ephemeral lineages also
might explain why intermediate stages of species formation seem absent
in species radiations (Roux et al. 2016), a pattern that has
often been interpreted as resulting from rapid divergence when lineages
approach a “tipping point”. As exemplified by S. occidentalis ,
such pattern could also arise from introgressive hybridization and
swamping between ephemeral lineages, which is consistent with
identification of introgression from ghost populations in extant species
(Kuhlwilm et al. 2019). These dynamics suggests that much of the
population structure we see within species is likely to be ephemeral
(Rosenblum et al. 2012) and that many of the recent radiations we
see on Earth will perhaps be lost to the vagaries of time. As envisioned
by Dobzhansky (Fig. 1A), Bouzid et al. (2021) are demonstrating that
subspecies, varieties and races are not less valuable than “good
species” and that in fact they are key for understanding the formation
of well delineated species.
Figure 1. Ephemeral ring diversification in Sceloporus
occidentalis. A. As envisioned by Dobzhansky, evolutionary lineages
can either merge through gene flow or acquire reproductive isolation
(adapted from Dobzhansky, 1958). B. The genetic patterns of genetic
diversification of S. occidentalis through space recapitulate
patterns expected through time, as lineages establishing secondary
contact become genetically homogeneous and geographically isolated
lineages remain distinct (adapted from Bouzid et al., 2021).