The puzzle of plant hybridisation: a high propensity to hybridise but few hybrid zones reported.

An interesting conundrum was recently revealed by R. Abbott when he found that the number of hybrid zones reported in the literature for plants is very low, given the propensity of plants to hybridise. In another literature survey on hybrid zones performed over the period 1970-2022, we found that the number of hybrid zones reported for vertebrates was 2.3 times greater than that reported for vascular plants, even though there are about six times more vascular plant species than vertebrates. Looking at the number of papers reporting hybrid zones, there are 4.9 times more on vertebrates than on vascular plants. These figures support the relevance of this conundrum. In this paper we aim to shed light on this question by providing a structured discussion of the causes that may underlie this conundrum. We propose six non-mutually exclusive factors, namely lack or deficit of spatial structure, lack or deficit of genetic structure, effects of hybridisation between non-closely related species, lability of plant hybrid zones over time, botanists' perception of hybridisation, and deficit of population genetic data. There does not appear to be a single factor that explains our puzzle, which applies to all cases of plants where hybridisation is detected but no hybrid zone is reported. It is argued that some plant features suggest that the puzzle is not, at least entirely, due to insufficient knowledge of the specific cases, a hypothesis that should be addressed with a wider range of empirical data across different taxonomic groups.

Demography-driven and adaptive introgression in a hybrid zone of the Armeria syngameon.

Syngameons represent networks of otherwise distinct species connected by limited gene exchange. Although most studies have focused on how species maintain their cohesiveness despite gene flow, there are additional relevant questions regarding the evolutionary dynamics of syngameons and their drivers, as well as the success of their members and the network as a whole. Using a ddRADseq approach, we analysed the genetic structure, genomic clines and demographic history of a coastal hybrid zone involving two species of the Armeria (Plumbaginaceae) syngameon in southern Spain. We inferred that a peripheral population of the sand dune-adapted A. pungens diverged from the rest of the conspecific populations and subsequently hybridized with a locally more abundant pinewood congener, A. macrophylla. Both species display extensive plastid DNA haplotype sharing. Genomic cline analysis identified bidirectional introgression, but more outlier loci with excess A. pungens than A. macrophylla ancestry, suggesting the possibility of selection for A. pungens alleles. This is consistent with the finding that the A. pungens phenotype is selected for in open habitats, and with the strong correlation found between ancestry and phenotype. Taken together, our analyses suggest an intriguing scenario in which bidirectional introgression may, on the one hand, help to avoid reduced levels of genetic diversity due to the small size and isolated location of the A. pungens range-edge population, thereby minimizing demographic risks of stochastic extinction. On the other hand, the data also suggest that introgression into A. macrophylla may allow individuals to grow in open, highly irradiated, deep sandy, salt-exposed habitats.

A snapshot of progenitor-derivative speciation in Iberodes (Boraginaceae).

Traditional classification of speciation modes has focused on physical barriers to gene flow. Allopatric speciation with complete reproductive isolation is viewed as the most common mechanism of speciation. Parapatry and sympatry, by contrast, entail speciation in the face of ongoing gene flow, making them more difficult to detect. The genus Iberodes (Boraginaceae, NW Europe) comprises five species with contrasting morphological traits, habitats and species distributions. Based on the predominance of narrow and geographically distant endemic species, we hypothesized that geographical barriers were responsible for most speciation events in Iberodes. We undertook an integrative study including: (i) phylogenomics through restriction-site-associated DNA sequencing (RAD-seq), (ii) genetic structure analyses, (iii) demographic modelling, (iv) morphometrics, and (v) climatic niche modelling and niche overlap analysis. The results revealed a history of recurrent progenitor-derivative speciation manifested by a paraphyletic pattern of nested species differentiation. Budding speciation mediated by ecological differentiation is suggested for the coastal lineage, deriving from the inland widespread Iberodes linifolia during the Late Pliocene. Meanwhile, geographical isolation followed by niche shifts are suggested for the more recent differentiation of the coastland taxa. Our work provides a model for distinguishing speciation via ecological differentiation of peripheral, narrowly endemic I. kuzinskyanae and I. littoralis from a widespread extant ancestor, I. linifolia. Ultimately, our results illustrate a case of Pliocene speciation in the probable absence of geographical barriers and get away from the traditional cladistic perspective of speciation as producing two species from an extinct ancestor, thus reminding us that phylogenetic trees tell only part of the story.

Hybridization and cryptic speciation in the Iberian endemic plant genus Phalacrocarpum (Asteraceae-Anthemideae).

Understanding the role and impact of reticulation in phylogenetic inquiry has improved with extended use of high throughput sequencing data. Yet, due to the dynamism of genomes over evolutionary time, disentangling old hybridization events remains a serious challenge. Phalacrocarpum (DC.) Willk. is one of the 27 Iberian endemic plant genera, currently considered monotypic but including three subspecies. Its uncertain phylogenetic relationships within tribe Anthemideae (Asteraceae) point to an Early Miocene divergence from its sister group, and its persistent taxonomic instability has been proposed to be due to hybridization. We aim at understanding the evolutionary history of this genus using SNPs called from a genotyping-by-sequencing (GBS) analysis, Sanger sequences-from three plastid DNA regions (psbJ-petA, petB-petD, trnH-psbA) and the nuclear ribosomal ITS regions (cloned)-as well as leaf morphometric multivariate analysis. SNP data and Sanger sequences strongly support the unforeseen existence of a cryptic species in the eastern populations of P. oppositifolium subsp. anomalum. Broad molecular and morphometric patterns of variation found in conflictive populations from the Sanabria Valley region convincingly identify a recent previously undocumented hybrid zone. By contrast, evidence is less conclusive on relationships between subspecies hoffmannseggii, oppositifolium and a second conflictive group distributed along the Galician-Portuguese border (Orense massifs). Although genetic clustering analysis of SNP data suggests that the former subspecies was the maternal progenitor in hybridization events that gave rise to the other two groups, we found considerable uniqueness of ITS ribotypes and plastid haplotypes in them. This result, in the context of Pleistocene climatically-driven range shifts in NW Iberian Peninsula, can be due to periods of isolation, genetic bottlenecks and drift superimposed on old hybridization events. Our study confirms the idea that unravelling old hybridization events may be compromised by the suite of evolutionary processes accumulated subsequently, particularly in areas with a history of climatic instability.