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The family Arthrodermataceae, the dermatophytes and allies, ancestrally began with Ascomycetous bifactorial sexual cycles built into an ecology that also featured considerable clonal propagation via conidia. When keratinolytic capabilities made ecological crossover to dermatopathogenicity possible, that conventional cycle, requiring moist, deposited keratinous material, could only be maintained by pathogens infecting animals burrowing or denning in habitats with soil. Lineages adapted to animals not nesting in soil became established clonally from representatives of single mating types. They became transformed in morphology and physiology, tending to develop reduced conidiation and more exogenous growth factor requirements in addition to retaining specific host adaptations. Viewing this speciation process through the lens of population biology tools designed for interbreeding populations can give a distorted picture, since the often ecologically neutral factors considered, like spacer regions, introns, restriction sites and single nucleotide polymorphisms, likely have a slower rate of change over time than the directly adaptive factors enabling these unifactorial radiate host switching events. The current state of species concepts in the dermatophytes and related, mostly nonpathogenic dermatophytoids is reviewed in light of this contrast of perspectives. Practical steps that can be taken in the clinical laboratory to make accurate identifications based on accurate species concepts are addressed. Some species concepts are supported in lineages that have previously reduced to lower rank, such as Trichophyton indotineae, T. interdigitale, and T. soudanense. The diversity of internal transcribed spacer barcodes in T. tonsurans suggests that research into clinical differences among genotypes is warranted.