An integrative genomic and phenomic analysis to investigate the nature of plant species in Escallonia (Escalloniaceae)

Abstract

Abstract What we mean by species and whether they have any biological reality has been debated since the early days of evolutionary biology. Some biologists even suggest that plant species are created by taxonomists as a subjective, artificial division of nature. However, the nature of plant species has been rarely tested critically with data while ignoring taxonomy. We integrate phenomic and genomic data collected across hundreds of individuals at a continental scale to investigate this question in Escallonia (Escalloniaceae), a group of plants which includes 40 taxonomic species (the species proposed by taxonomists). We first show that taxonomic species may be questionable as they match poorly to patterns of phenotypic and genetic variation displayed by individuals collected in nature. We then use explicit statistical methods for species delimitation designed for phenotypic and genomic data, and show that plant species do exist in Escallonia as an objective, discrete property of nature independent of taxonomy. We show that such species correspond poorly to current taxonomic species ( $$< 20\%$$ < 20 % ) and that phenomic and genomic data seldom delimit congruent entities ( $$< 20\%$$ < 20 % ). These discrepancies suggest that evolutionary forces additional to gene flow can maintain the cohesion of species. We propose that phenomic and genomic data analyzed on an equal footing build a broader perspective on the nature of plant species by helping delineate different ‘types of species’. Our results caution studies which take the accuracy of taxonomic species for granted and challenge the notion of plant species without empirical evidence. Note: A version of the complete manuscript in Spanish is available in the Supplemental Materials.