Natural hybridization between two butterfly bushes in Tibet: dominance of F1 hybrids promotes strong reproductive isolation

Abstract

Background It has been recognized that a certain amount of habitat disturbance is a facilitating factor for the occurrence of natural hybridization, yet to date we are unaware of any studies exploring hybridization and reproductive barriers in those plants preferentially occupying disturbed habitats. Buddleja plants (also called butterfly bush) generally do grow in disturbed habitats, and several species with hybrid origin have been proposed, based solely on morphological evidence. Results In the present study, we test the hypothesis that B. × wardii is of natural hybridization origin in two sympatric populations of three taxa including B. × wardii and its parents (B. alternifolia and B. crispa) plus 4 referenced parental populations, using four nuclear genes and three chloroplast intergenic spacers, as well as with 10 morphological characters. Our results suggest that at both sites B. × wardii is likely to be a hybrid between B. alternifolia and B. crispa, and moreover, we confirm that most of the hybrids examined are F1s. That these plants are F1s is further supported by morphology, as no transgressive characters were detected. B. crispa was found to be the maternal parent in the Bahe (BH) population, from cpDNA evidence. However, in the Taji (TJ) population, the direction of hybridization was difficult to establish due to the shared cpDNA haplotypes between B. alternifolia and B. crispa, however we still predicted a similar unidirectional hybridization pattern due to results from cross-specific pollination treatments which supported the “SI × SC rule”. Conclusions The presence of mainly F1 hybrids can successfully impede gene flow and thus maintain species boundaries in parental species in a typical distribution of Buddleja, i.e. in disturbed habitats.

Natural Hybrid Origin of the Controversial “Species” Clematis × pinnata (Ranunculaceae) Based on Multidisciplinary Evidence

“…For example, a C. × pinnata individual in Jiufeng, Beijing, noted only a few normal achenes per year, while most of them did not develop at all. Except for several prerequisites for natural hybridization, e.g., close kinship, overlapping distribution, similar flowering period, shared pollinators, and same chromosome numbers (Ning et al, 2019), habitat disturbance has been often considered as one of the most important factors promoting hybridization (Arnold, 1997;Li et al, 2017;Liao et al, 2021). In the study area of Beijing and Liaoning Province, we found all the C. × pinnata individuals occurred along the mountain roadside.…”

“…Recent studies have shown that F1 hybrids are common in angiosperms and that they can successfully impede gene flow and thus maintain species boundaries between parental species especially in areas where habitat disturbance is high (Liao et al, 2021). Morphologically, C. sect.…”

“…However, studies have shown that many previously recognized plant species represented F1 hybrids, which cannot be accepted as a real species (Zha et al, 2010;Zhang et al, 2020;Li et al, 2017). Because F1 hybrids tend to have similar morphologies due to the complete combination of parental genomes, they have often been recognized as distinct species by taxonomists (Liao et al, 2021). This raises critical problems for morphological-based taxonomy, biodiversity estimations and biological conservation.…”

Unusual patterns of hybridization involving two alpine Salvia species: Absence of both F1 and backcrossed hybrids

“…The significance of differences between the means was determined using standard F statistic, and the Bonferroni test was employed for post hoc pairwise comparisons. Where the data did not satisfy the criterion of homogeneity of variance, a Welch statistic was employed, and post hoc comparisons were performed using the Tamhane’s test ( Liao et al., 2021 ). In addition, single flower anthesis, preference of pollinators, fruit and seed sets between S. flava and S. castanea were assessed using a non-parametric Mann-Whitney U-test.…”

“…Therefore, various patterns of hybridization might occur if RI varied between parental plants and their hybrids. For instance, hybrid zones dominated by F 1 s have been repeatedly detected cross many plant genera and families in recent years ( Milne et al., 2003 ; Zha et al., 2010 ; Liao et al., 2015 ; Zhang et al., 2018 ; Hu et al., 2021a ; Hu et al., 2021b ; Liao et al., 2021 ), indicating that gene flow is fully blocked and RI is nearly complete between parent species. Hybrid zones dominated by F 1 s are usually due to F 1 s having higher habitat-mediated superiority than other genotype classes or a high degree of hybrid sterility ( Milne et al., 2003 ; Yu et al., 2011 ).…”