What is a species?

MANUSCRIPT ABSTRACT: Species identity is a cornerstone concept of biology, and correct identification is important for economically and ecologically important organisms. Yet, many organismal groups do not fit any of the standard species concepts, particularly those with clonal reproduction or inbreeding. We studied the global correlation between morphological species identity, geographic provenance, and genomic population structure in an unresolved complex of ambrosia beetles in the genus Xyleborus. These insect pests are highly inbred, globally distributed, and morphologically cryptic, which has hampered the development of a usable and justifiable definition of species. Using the combination of ddRADseq approach and quantitative morphometrics, we have reconstructed the global population structure of three interrelated hypothetical species X. ferrugineus, X. bispinatus, and X. impressus. We have revealed remarkably low genome-level variation across the three morphotypes: only 706 SNPs over 92,486 possible sites. Morphological variation yielded distinct clusters on a local level, but only X. impressus is recognizable as a distinct cluster. On a global level, the same phenotypes appear at different locations and are borne by different genotypes. Therefore, assigning a species name to a particular morphotype across large geographic scales may not be warranted. Identification of these insects using traditional characters underestimated the complexity of their population structure, and overestimated the significance of small morphological differences. Low local genetic variation was likely the result of the predominance of inbreeding, while the lack of global structure suggested high dispersal and a degree of outbreeding greater than previously thought.