For centuries, both scientists and philosophers have discussed the nature of species resulting in c. 35 species concepts proposed to date. However, in our opinion, none of them incorporated neither recent advances in evolutionary genomics nor dimensionality of species in befitting depth. Our attempt to do so resulted in the following conclusions. Due to the continuous nature of evolution (regardless of its rate and constancy), species are inevitably undefinable as natural discontinuous units (except those originating in saltatory speciation) whenever the time dimension is taken into consideration. Therefore, the very existence of species as a natural discontinuous entity is relative to its dimensionality. A direct consequence of the relativity of species is the duality of speciators (e.g., incipient species) meaning that, in a given time, they may be perceived as both being and not being a species. Finally, the most accurate way to reflect both the relativity of species and the duality of speciators in species delimitation is probabilistic. While the novelty of these ideas may be questionable, they still deserve more extensive attention from the biological community. Here, we hope to draw such attention by outlining one of the possible pathways towards a new kind of probabilistic species delimitation methods based on the probability of irreversible divergence of evolutionary lineages. We anticipate that our probabilistic view of speciation has the potential to facilitate some of the most serious and universal issues of current taxonomy and to ensure unity of the species-level taxonomy across the tree of life.

Department of Botany Faculty of Science Palacký University Olomouc Olomouc Czech Republic

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Andersson, L. (1990). The driving force: Species concepts and ecology. Taxon, 39(3), 375-382. https://doi.org/10.2307/1223084

Behnke, A., Friedl, T., Chepurnov, V. A., & Mann, D. G. (2004). Reproductive compatibility and rDNA sequence analyses in the Sellaphora pupula species complex (Bacillariophyta). Journal of Phycology, 40(1), 193-208. https://doi.org/10.1046/j.1529-8817.2004.03037.x

Bobay, L.-M., & Ochman, H. (2017). Biological species are universal across life’s domains. Genome Biology and Evolution, 9(3), 491-501. https://doi.org/10.1093/gbe/evx026

Bock, W. J. (2006). Species concepts versus species categories versus species taxa. Acta Zoologica Sinica, 52, 421-424.

Darwin, F. (Ed.) (1887). The life and letters of Charles Darwin, including an autobiographical chapter (Vol. II, 3rd ed.). John Murray.

de Queiroz, K. (1998). The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. In D. J. Howard, & S. H. Berlocher (Eds.), Endless forms: Species and speciation (pp. 57-75). Oxford University Press.

de Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology, 56(6), 879-886. https://doi.org/10.1080/10635150701701083

Dettman, J. R., Jacobson, D. J., & Taylor, J. W. (2006). Multilocus sequence data reveal extensive phylogenetic species diversity within the Neurospora discreta complex. Mycologia, 98, 437-447.

Dufresnes, C., Pribille, M., Alard, B., Gonçalves, H., Amat, F., Crochet, P.-A., Dubey, S., Perrin, N., Fumagalli, L., Vences, M., & Martínez-Solano, I. (2020). Integrating hybrid zone analyses in species delimitation: Lessons from two anuran radiations of the Western Mediterranean. Heredity, 124, 423-438. https://doi.org/10.1038/s41437-020-0294-z

Durand, E. Y., Patterson, N., Reich, D., & Slatkin, M. (2011). Testing for ancient admixture between closely related populations. Molecular Biology and Evolution, 28(8), 2239-2252. https://doi.org/10.1093/molbev/msr048

Dvořák, P., Poulíčková, A., Hašler, P., Belli, M., Casamatta, D. A., & Papini, A. (2015). Species concepts and speciation factors in cyanobacteria, with connection to the problems of diversity and classification. Biodiversity and Conservation, 24(4), 739-757. https://doi.org/10.1007/s10531-015-0888-6

Fraser, C., Hanage, W. P., & Spratt, B. G. (2007). Recombination and the nature of bacterial speciation. Science, 315(5811), 476-480. https://doi.org/10.1126/science.1127573

Gladieux, P., Wilson, B. A., Perraudeau, F., Montoya, L. A., Kowbel, D., Hann-Soden, C., Fischer, M., Sylvain, I., & Jacobson, D. J., & Taylor, J. W. (2015). Genomic sequencing reveals historical, demographic and selective factors associated with the diversification of the fire-associated fungus Neurospora discreta. Molecular Ecology, 24(22), 5657-5675. https://doi.org/10.1111/mec.13417

Han, F., Lamichhaney, S., Grant, B. R., Grant, P. R., Andersson, L., & Webster, M. T. (2017). Gene flow, ancient polymorphism, and ecological adaptation shape the genomic landscape of divergence among Darwin’s finches. Genome Research, 1-12, https://doi.org/10.1101/gr.212522.116.27

Hudson, R. R., Slatkin, M., & Maddison, W. P. (1992). Estimation of levels of gene flow from DNA sequence data. Genetics, 132(2), 583-589.

Malinsky, M., Challis, R. J., Tyers, A. M., Schiffels, S., Terai, Y., Ngatunga, B. P., Miska, E. A., Durbin, R., Genner, M. J., & Turner, G. F. (2015). Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake. Science, 350(6267), 1493-1498. https://doi.org/10.1126/science.aac9927

Mann, D. G., McDonald, S. M., Bayer, M. M., Droop, S. J. M., Chepurnov, V. A., Loke, R. E., Ciobanu, A., & du Buf, J. M. H. (2004). The Sellaphora pupula species complex (Bacillariophyceae): Morphometric analysis, ultrastructure and mating data provide evidence for five new species. Phycologia, 43(4), 459-482. https://doi.org/10.2216/i0031-8884-43-4-459.1

Martin, S. H., Dasmahapatra, K. K., Nadeau, N. J., Salazar, C., Walters, J. R., Simpson, F., Blaxter, M., Manica, A., Mallet, J., & Jiggins, C. D. (2013). Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Research, 23(11), 1817-1828. https://doi.org/10.1101/gr.159426.113

Mayr, E. (1942). Systematics and the origin of species. Columbia University Press.

Mayr, E. (1963). Animal species and evolution. Harvard University Press.

Mayr, E. (1982). The growth of biological thought (11th ed.). Harvard University Press. https://doi.org/10.1525/aa.1986.88.2.02a00160

Mayr, E. (2004). What makes biology unique?. Cambridge University Press.

Menkis, A., Bastiaans, E., Jacobson, D. J., & Johannesson, H. (2009). Phylogenetic and biological species diversity within the Neurospora tetrasperma complex. Journal of Evolutionary Biology, 22, 1923-1936.

Popa, O., Hazkani-Covo, E., Landan, G., Martin, W., & Dagan, T. (2011). Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes. Genome Research, 21, 599-609. https://doi.org/10.1101/gr.115592.110

Poulíčková, A., Mayama, S., Chepurnov, V. A., & Mann, D. G. (2007). Heterothallic auxosporulation, incunabula and perizonium in Pinnularia (Bacillariophyceae). European Journal of Phycology, 42(4), 367-390. https://doi.org/10.1080/09670260701476087

Richards, E. J., Poelstra, J. W., & Martin, C. H. (2018). Don’t throw out the sympatric speciation with the crater lake water: Fine-scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation. Evolution Letters, 2(5), 524-540. https://doi.org/10.1002/evl3.78

Riesch, R., Muschick, M., Lindtke, D., Villoutreix, R., Comeault, A. A., Farkas, T. E., Lucek, K., Hellen, E., Soria-Carrasco, V., Dennis, S. R., de Carvalho, C. F., Safran, R. J., Sandoval, C. P., Feder, J., Gries, R., Crespi, B. J., Gries, G., Gompert, Z., & Nosil, P. (2017). Transitions between phases of genomic differentiation during stick-insect speciation. Nature Ecology & Evolution, 1, 0082. https://doi.org/10.1038/s41559-017-0082

Simpson, G. G. (1951). The species concept. Evolution, 5(4), 285-298.

Simpson, G. G. (1961). Principles of animal taxonomy. Columbia University Press.

Sober, E. (1984). Sets, species, and evolution: Comments on Philip Kitcher’s “species”. Philosophy of Science, 51(2), 334-341. https://doi.org/10.1086/289183

Sonneborn, T. M. (1957). Breeding systems, reproductive methods, and species problems in protozoa. In E. Mayr (Ed.), The species problem (pp. 155-324). American Association for the Advancement of Science.

Stamos, D. N. (2004). The species problem, biological species, ontology and the metaphysics of biology. Lexington Books.

The Heliconius Genome Consortium (2012). Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature, 487, 94-98.

Van Valen, L. (1976). Ecological species, multispecies, and oaks. Taxon, 25(2), 233-239. https://doi.org/10.2307/1219444

Wheeler, Q. D., & Meier, R. (2000). In Q. D. Wheeler, & R. Meier (Eds.), Species concepts and phylogenetic theory: A debate. Columbia University Press.

Wiley, E. O. (1978). The evolutionary species concept reconsidered. Systematic Zoology, 27, 17-26. https://doi.org/10.2307/2412809

Wiley, E. O., & Mayden, R. L. (2000). The evolutionary species concept. In Q. D. Wheeler, & R. Meier (Eds.), Species concepts and phylogenetic theory (pp. 70-89). Columbia University Press.

Wilkins, J. S. (2009). Species: A history of the idea (1st ed.). University of California Press.

Wolf, J. B., & Ellegren, H. (2017). Making sense of genomic islands of differentiation in light of speciation. Nature Reviews Genetics, 18, 87-100. https://doi.org/10.1038/nrg.2016.133

Wu, C. I. (2001). The genic view of the process of speciation. Journal of Evolutionary Biology, 14(6), 851-865. https://doi.org/10.1046/j.1420-9101.2001.00335.x

Zachos, F. E. (2016). Species concepts in biology. Springer. https://doi.org/10.1007/978-3-319-44966-1

Population genomics and morphological data bridge the centuries of cyanobacterial taxonomy along the continuum of Microcoleus species

The global speciation continuum of the cyanobacterium Microcoleus

High genomic differentiation and limited gene flow indicate recent cryptic speciation within the genus Laspinema (cyanobacteria)