Phylogenomic analysis does not support a classic but controversial hypothesis of progenitor‐derivative origins for the serpentine endemic Clarkia franciscana

Abstract

Budding speciation involves isolation of marginal populations at the periphery of a species range and is thought to be a prominent mode of speciation in organisms with low dispersal and/or strong local adaptation among populations. Budding speciation is typically evidenced by abutting, asymmetric ranges of ecologically divergent sister species and low genetic diversity in putative budded species. Yet these indirect patterns may be unreliable, instead caused by postspeciation processes such as range or demographic shifts. Nested phylogenetic relationships provide the most conclusive evidence of budding speciation. A putative case of budding speciation in the serpentine endemic Clarkia franciscana and two closely related widespread congeners was studied by Harlan Lewis, Peter Raven, Leslie Gottlieb, and others over a 20‐year period, yet the origin of C. franciscana remains controversial. Here, we reinvestigate this system with phylogenomic analyses to determine whether C. franciscana is a recently derived budded species, phylogenetically nested within one of the other two putative progenitor species. In contrast to the hypothesized pattern of relatedness among the three Clarkia species, we find no evidence for recent budding speciation. Instead, the data suggest the three species diverged simultaneously. We urge caution in using contemporary range patterns to infer geographic modes of speciation.

Genomics of plant speciation

“…Phylogenomics has been used, for example, to verify one of the predictions of speciation by genetic drift: that the descendant species is monophyletic within the paraphyletic progenitor (e.g., Andrew et al., 2013 ). In the case of Clarkia franciscana , which was considered a classic example of catastrophic speciation ( Lewis and Raven, 1958 ), phylogenomics did not support this phylogenetic placement, refuting the possibility that speciation occurred by budding ( Sianta and Kay, 2022 ), in line with earlier suspicions based on isozymes ( Gottlieb, 1973 ). Reconstruction of long-term demography could be equally informative, although these methods have been used most often to establish whether divergence occurred with or without gene flow (see Speciation with gene flow, introgression, and hybrid speciation ).…”

“…Overall, these results imply that geographical isolation may not play a critical role in speciation in many groups of plants, with speciation driven instead by divergent adaptation to different local environments ( Anacker and Strauss 2014 ; Papadopulos et al., 2014 ). Gene flow between diverging lineages is expected to be common under such speciation scenarios ( Kisel and Barraclough, 2010 ; although see Sianta and Kay, 2022 ).…”