Speciation continuum in non-model organisms: Revisiting the species-pair concept in lichens

Abstract

Evolutionary biologists have long pursued understanding the continuum in which populations flow, interact, and evolve, which can ultimately lead to divergence into distinct species. Lichens, which are often defined as intricate ecosystems, exhibit remarkable evolutionary mechanisms that challenge conventional definitions of speciation. A particularly notable phenomenon in lichens is the species-pair concept, in which closely related taxa only differ in their reproductive strategies − one reproducing sexually, the other asexually. We investigated this concept in the iconic beard-like lichen Usnea by comparing three species pairs: U. aurantiacoatra/U. antarctica, U. florida/U. subfloridana and U. intermedia/U. perplexans. Using reference-based RADseq data and applying multivariate and model-based genomic population methods, we evaluated genomic differentiation across each pair. Our results revealed a gradient of divergence: U. aurantiacoatra/U. antarctica showed strong lineage separation with no genomic admixture, U. intermedia/U. perplexans exhibited moderate differentiation with signs of gene flow, and U. florida/U. subfloridana formed a largely unstructured clade with substantial genomic overlap. These findings place the three species pairs at different positions along the speciation continuum and highlight reproductive mode as a key factor influencing lineage divergence. Our study reframes the species-pair concept within a continuum framework and provides new genomic insights from a non-model system, enhancing our understanding of speciation in lichen-forming fungi.