Genomic analyses overturn two long‐standing homoploid hybrid speciation hypotheses

Abstract

The importance of hybridization in generating biological diversity has been historically controversial. Previously, inference about hybridization was limited by dependence on morphological data; with the advent of the next-generation sequencing tools for nonmodel organisms, the evolutionary significance of hybridization is more evident. Here, we test classic hypotheses of hybrid origins of two species in the Phlox pilosa complex. Morphological intermediacy motivated the hypotheses that Phlox amoena lighthipei and Phlox pilosa deamii were independent homoploid hybrid lineages derived from P. amoena amoena and P. pilosa pilosa. We use double-digest restriction site-associated DNA sequencing of individuals from throughout the range of these taxa to conduct the most thorough analysis of evolutionary history in this system to date. Surprisingly, we find no support for the hybrid origin of P. pilosa deamii or P. amoena lighthipei. Our data do identify a history of admixture in individuals collected at a contemporary hybrid zone between the putative parent lineages. We show that three very different evolutionary histories, only one of which involves hybrid origin, have produced intermediate or recombinant morphological traits between P. amoena amoena and P. pilosa pilosa. Although morphological data are still an efficient means of generating hypotheses about past gene flow, genomic data are now the standard of evidence for elucidating evolutionary history.

Digest: Revisiting morphology‐derived hypotheses of hybridization in the light of genomics

“…2018), and also (ii) validate inferences from tests for introgression, such as those used by Goulet‐Scott et al. (2021). The decomposition of gene flow, by reconstructing its magnitude, direction, and timing, can provide relevant insights into hybridization dynamics, as well as the actual incidence of hybrid speciation in nature.…”

“…Despite finding no support for the hybrid‐speciation hypothesis, Goulet‐Scott et al. (2021) do detect genetically admixed individuals ( P. amoena X pilosa ) in a hybrid zone, likely resulting from genetic exchange between P. pilosa pilosa and P. amoena lineages. Hybrid zones provide a powerful framework to explore environmental factors that may facilitate or prevent the breakdown of boundaries between nascent species.…”

“…Schematic overview of the hypothetical and methodological framework of Goulet‐Scott et al. (2021). Left panel represents the morphological‐informed hypotheses of hybrid speciation, while right panel summarizes the genomic methods used and inferences obtained: (i) the lack of support for the hybrid‐speciation hypothesis, and (ii) the detection of admixed individuals (new lineage C in this figure) compatible with interspecific gene flow in a hybrid zone.…”

“…To reconstruct the diversification and hybridization history of two wildflower species belonging to the Phlox pilosa complex (Fig. 1), Goulet-Scott et al (2021) integrating genome-wide data within a population genetic and phylogenetic framework. Specifically, they evaluate the hypothesis that P. pilosa deamii and P. amoena lighthipei are the results of hybrid speciation events, as previously posited based on microsatellite data and their intermediate morphology with regard to putative parental taxa (P. pilosa pilosa and P. amoena amoena).…”

“…However, untangling whether the observed patterns of genetic admixture are the result of past or recent hybridization, and their potential relationship to hybrid speciation, is challenging. In this context, demographic modeling using coalescent simulations provides an excellent and flexible framework to (i) simultaneously compare alternative demographic scenarios and estimate gene flow and divergence parameters (e.g., Barrera-Guzmán et al 2018), and also (ii) validate inferences from tests for introgression, such as those used by Goulet-Scott et al (2021). The decomposition of gene flow, by reconstructing its magnitude, direction, and timing, can provide relevant insights into hybridization dynamics, as well as the actual incidence of hybrid speciation in nature.…”