Evolution of strong reproductive isolation in plants: broad-scale patterns and lessons from a perennial model group

Abstract

Many recent studies have addressed the mechanisms operating during the early stages of speciation, but surprisingly few studies have tested theoretical predictions on the evolution of strong reproductive isolation (RI). To help address this gap, we first undertook a quantitative review of the hybrid zone literature for flowering plants in relation to reproductive barriers. Then, using Populus as an exemplary model group, we analysed genome-wide variation for phylogenetic tree topologies in both early- and late-stage speciation taxa to determine how these patterns may be related to the genomic architecture of RI. Our plant literature survey revealed variation in barrier complexity and an association between barrier number and introgressive gene flow. Focusing on Populus, our genome-wide analysis of tree topologies in speciating poplar taxa points to unusually complex genomic architectures of RI, consistent with earlier genome-wide association studies. These architectures appear to facilitate the ‘escape’ of introgressed genome segments from polygenic barriers even with strong RI, thus affecting their relationships with recombination rates. Placed within the context of the broader literature, our data illustrate how phylogenomic approaches hold great promise for addressing the evolution and temporary breakdown of RI during late stages of speciation. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Drivers of genomic landscapes of differentiation acrossPopulusdivergence gradient

“…Genetic clustering as indicated by the first two principal components of the PCA (Fig. 2a) is consistent with expected genetic divisions, identifying the species previously described as the most divergent (Shang, et al 2020) grandidentata from the rest (Fig. 2a).…”

“…In this study, we focused on white poplars and aspens from the section Populus which are widely distributed in Eurasia and North America (Supplementary material, Fig. S1 and (Shang, et al 2020).…”

Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers

“…de Vos et al [5] and Meyers et al [35] in this theme issue), theoretical studies highlighting what drives and hinders the evolution of strong RI (e.g. Blanckaert et al [16], Payne & Polechová [17] and Bisschop et al [18] in this issue), metaanalyses (as discussed in Rometsch et al [31] and Shang et al [44] in this issue), the identification of processes defining stages (see Muschick et al [23] and Tinghitella et al [32] in this issue) and combined approaches as outlined in this issue (Coughlan & Matute [30] and Satokangas et al [33]). This theme issue is dedicated to Christian Lexer ( [76], this theme issue).…”

“…The interaction between selection and recombination can generate a sharp discontinuity in the strength of the genomewide barrier to gene flow (e.g. Populus trees in Shang et al [44] and sticklebacks in Yamasaki et al [15] in this issue). In the context of secondary contact, Barton [28] showed that a strong genome-wide barrier is expected when the ratio of selection to recombination (known as the 'coupling coefficient') exceeds a critical value owing to accumulation of incompatibilities (see also [37]).…”

Modern Strategies to Assess and Breed Forest Tree Adaptation to Changing Climate

“…Tree species rich in evolutionary diversity (Shang et al, 2020) could leverage breeding. Hybridization (Nieto Feliner et al, 2020), introgression (Burgarella et al, 2019), and polyploidy (Mason and Wendel, 2020) have already pumped morphological novelty by testing more genetic compatibilities than humans ever will.…”