Ecology of Dermatophytes and Origin of Zoophilic Species
The Mesozoic era (252-66 million years ago) was associated with a significant ecological morphological diversification of early mammals, a prerequisite for evolutionary success after extinction of the nonavian dinosaurs 66 million years ago.
It was assumed based on molecular dating that dermatophytes could radiate approximately 50 million years ago (Harmsen et al. 1995) closely linked to early Cenozoic adaptive explosion of mammals. However, more recently fossil evidence of dermatophytosis in mammals was estimated to be approximately 125 million-year- old (Martin et al. 2015). Despite numerous uncertainties, it seems quite clear that dermatophytes are evolutionary young group of fungi that diverged later than other groups of pathogenic fungi (Wu et al. 2009).Significant part of the diversity of dermatophytes is represented by geophilic species that act as uncommon causal agents of infections without significant contagious potential. They occur in soil around burrows and nests of terrestrial vertebrates and birds, can be carried in the fur, and therefore cause diagnostic doubts when they are isolated from healthy animals or animals with ambiguous symptoms. Geophilic species are characterized by relatively high intraspecies diversity, and they are all sexual and heterothallic (isolates of two opposite mating types are present in population) with only few exceptions. The sexual process takes place in the soil on the keratinized substrates. Geophilic species are considered an ancestral (“primitive”) group of dermatophytes, while “advanced” ecological groups of zoophilic and anthropophilic are derived from geophilic species. The phylogenetic grouping of anthropophilic and zoophilic species of Trichophyton and Microsporum into monophyletic clades and geophilic species from genera Arthroderma, Nannizzia, and Paraphyton into another monophyletic clades supports the hypothesis that ecology has been crucial driver of the evolution in dermatophytes (Graser et al.
2008; de Hoog et al. 2017).Specialized pathogens of animals and human, zoophilic and anthropophilic species, respectively, are primarily associated with one or few related host species but have potential to cause infection in a broad spectrum of animals (Table 3.1). They usually cause mild (chronic) or asymptomatic infections in primary host, often
Table 3.1 Ecology of zoophilic or possibly zoophilic dermatophytes
| Species | Principal host(s)/ source, other hosts | Distribution | Epidemic potential in principal hosts | Zoonotic risk for human |
| Microsporum canis (syn. M. equinum) | Cat, dog, horse, all mammals | Worldwide | High | High |
| L. gallinae (syn. M. vanbreuseghemii)a | Chicken, soil, birds, mammals | Worldwide | Low | Low |
| T. benhamiae | Guinea pig, other rodents, dogs | Worldwide | High | High |
| T. bullosum | Horse, donkey, mole? | Syria, Sudan, Tunisia, France, Czech Republic | Insufficient data | Insufficient data |
| T. equinum | Horse | Worldwide | High | Low |
| T. erinacei | Hedgehogs (Erinaceus europaeus, Atelerix albiventris) | Europe, New Zealand, Africa (kept as pet worldwide) | High | Probably high |
| T. eriotrephon | Unknown | Netherlands, Iran | Insufficient data | Insufficient data |
| T. mentagrophytes | Rabbits, rodents, cats, and dogs (especially free roaming and hunting) | Worldwide | High | High |
| T. quinckeanum | Rodents (mice) | Worldwide | High | High |
| T. simiia | Soil, monkeys, chicken, dog | Worldwide | Low | Low |
| T. verrucosum | Cattle, other ruminants, all mammals, birds | Worldwide | High | High |
aThese species are probably geophilic—see Sect. 3.9
being widespread and epidemic/epizootic. In contrast, the infections in less common hosts tend to be acute and highly inflammatory. The population structure of many primary pathogenic species is nearly clonal, and they have unknown sexual state. It was suggested that these “species” spread clonally by asexual propagation in the population of host without having a terrestrial reservoir and thus reducing the probability of encountering a partner of the opposite sex (Summerbell 2002). Consequently, these “species” (clonal offshoots) derived from their sexual ancestors possess predominantly only strains with identical mating type across global population. Kano et al. (2014) demonstrated that strains of T. verrucosum have consistently only MAT1-2-1 gene corresponding to the mating type (—). Similarly, single mating is also present in anthropophilic species T. tonsurans (mating type —), T. rubrum (mating type —), and T. violaceum (mating type —) but also in zoophilic T. equinum with mating type + (Graser et al. 2008; Metin and Heitman 2017). The intraspecies variability in these taxa is mostly generated by fixation of neutral mutations.
Historically, species and populations tended to remain within limited geographic areas such as continents, a condition leading to structuration of global population. With human migration and animal trade, however, geographically restricted genotypes can be rapidly distributed over large geographic areas, leading to reduction of polymorphism within widely dispersed entities (Graser et al. 2006).In contrast to abovementioned species, both mating types are present in population of T. benhamiae (Kano et al. 2011; Symoens et al. 2013; Cmokova 2015), T. mentagrophytes (Symoens et al. 2011), and M. canis (Hironaga et al. 1980) suggesting that sexual reproduction naturally occurs in these species and probably takes place in burrows of wild animals or their close neighborhood rather than in association with dwellings of domestic animals. The distribution of mating-type genes is commonly unequal in mentioned species or at least in some subpopulations. This may be caused by clonal horizontal propagation of single or several clones in the population of the host. Assessment of species boundaries by mating experiments is in general well applicable in geophilic species (Stockdale 1964; Hubka et al. 2015). In contrast, biological compatibilities can considerably disagree with the concept of classical species of anthropophilic and zoophilic dermatophytes. These species are phylogenetically young, and prezygotic reproductive barriers are incomplete resulting in positive mating experiments even between phylogenetically distant species (Anzawa et al. 2010; Kawasaki et al. 2010; Kawasaki 2011). It is however highly unlikely that this kind of hybridization occurs naturally due to different ecological niches of species.
3.5