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).