Genomic instability within a sympatric complex of South American garlics (Nothoscordum spp., Amaryllidaceae)

Abstract

Background and AimsThe evolution of reproductive isolation between previously interbreeding populations is a fundamental driver of plant speciation. Within Amaryllidaceae, Nothoscordum represents an evolutionarily complex genus, characterized by an unusually high incidence of chromosomal rearrangements. During fieldwork, Nothoscordum montevidense and Nothoscordum bonariense were found growing in sympatry, along with individuals exhibiting intermediate morphological traits, suggesting a putative hybrid origin. To test this hypothesis, we employed an integrative approach to characterize the morphologically intermediate specimens and the two sympatric populations. Materials and methodsTo characterize the putative hybrids we have combined morphological, cytogenetic analyses (chromosome counts, CMA/DAPI banding, and FISH) and flow cytometry-based genome size estimation. Phylogenetic relationships and genomic structure were also investigated through Genotyping-by-Sequencing (GBS), complete chloroplast genome assembly, and comparative repetitive DNA analysis. We also performed species distribution modeling and phenological analyses of the putative parental species. Key ResultsMultiple lines of evidence confirm the hybrid origin of the studied plants. Cytogenetic analyses revealed specimens with 2n = 21 (1C {approx} 33 pg = 32.274 Mbp) and 2n = 25 (1C {approx} 37 pg = 36.186 Mbp), accompanied by meiotic irregularities consistent with interspecific hybridization. Chloroplast genome phylogeny identified N. montevidense (2n = 16, 1C {approx} 25 pg) as the maternal lineage, while GBS data confirmed N. bonariense (2n = 26, 1C {approx} 41 pg) as the paternal contributor and revealed evidence of subsequent backcrossing. Comparative analysis of repetitive DNA showed reduced 35S rDNA diversity in the hybrid, indicative of post-hybridization genomic restructuring. Despite the observed genomic complexity, no clear morphological differentiation was detected among hybrid individuals. Phenological analyses and species distribution models demonstrated broad overlap between parental species. ConclusionsOur findings highlight the role of hybridization in shaping genome architecture in cytogenetically labile plant lineages. Furthermore, our results underscore that morphological similarity can mask profound genomic complexity, reinforcing the value of integrative approaches to understand genera characterized by reticulate evolution and genomic instability.