Polytypic species concept and subspecies in the genomic era

In PNAS, Dufresnes et al. (1) provide a reasonable justification for the concept of subspecies in its modern understanding (subspecies as a phylogeographic sublineage). In this article, the authors emphasize the utilitarian significance of the concept, such as its importance for conservation and reduction of poorly supported species, thereby avoiding taxonomic inflation. However, in my opinion, two main points are not highlighted clearly enough. First, this concept is well compatible not only with practical needs but also with the actual structure of biological diversity. Second, by supporting the definition of a species as a reproductively isolated lineage that may include distinct but reproductively compatible sublineages (2, 3), the authors are in effect developing the classical concept of a polytypic species.

The concept of subspecies in evolutionary biology developed in the first half of the 20th century. It is inextricably linked with the ideas of biological and polytypic species (4–6). According to the biological concept, species are objective entities that can be identified based on the fact that populations within a species are reproductively compatible while different species are reproductively isolated. Although the criterion of reproductive isolation has numerous limitations and shortcomings, it nevertheless became a guiding light in practical taxonomy of the twentieth century. It has maintained a balance between species oversplitting (describing apparently reproductively compatible forms as species) and species lumping (aggregating apparently incompatible forms).

According to the polytypic concept, biological species can be subdivided geographically. The objective presence of these geographical subdivisions and their existence as discrete evolutionary units are the essence of subspecies (6), rather than mere differences between subspecies in morphology, ecology, or behavior (1, 7). The latter are only signs on the basis of which one can judge possible subspecies. Unfortunately, these signs are often not very reliable. On the one hand, allelic polymorphism and phenotypic plasticity can create the illusion of differentiation where in fact there is no divergence. On the other hand, cryptic evolutionary lineages may not be visible to the eye. Subspecies taxonomy has long lacked a reliable guideline such as the criterion of reproductive isolation in species-level taxonomy. In many organisms, this has led to an excessive number of poorly justified subspecies names and to almost universal skepticism in the use of the subspecies category. The degradation of research using the subspecies concept was well described by Ernst Mayr, who himself, in the second half of his life, moved from subspecies as an “incipient species” to subspecies as an “aggregate of phenotypically similar populations” (7).

This criterion appeared in the molecular era. Molecular data have provided abundant evidence that the concept of polytypic species is correct and that biological species can be composed of geographic units that can be objectively defined (e.g., in plants, ref. 8 and butterflies, ref. 9). These units are phylogeographic sublineages, and their essence as geographic and evolutionary subdivisions of a species exactly corresponds to the definition of a subspecies in the era of evolutionary synthesis (4–6).