Hybridization Facilitates Adaptive Evolution in Two Major Fungal Pathogens

Abstract

Hybridization is increasingly recognized as an important force impacting adaptation and evolution in many lineages of fungi. During hybridization, divergent genomes and alleles are brought together into the same cell, potentiating adaptation by increasing genomic plasticity. Here, we review hybridization in fungi by focusing on two fungal pathogens of animals. Hybridization is common between the basidiomycete yeast species Cryptococcusneoformans × Cryptococcusdeneoformans, and hybrid genotypes are frequently found in both environmental and clinical settings. The two species show 10-15% nucleotide divergence at the genome level, and their hybrids are highly heterozygous. Though largely sterile and unable to mate, these hybrids can propagate asexually and generate diverse genotypes by nondisjunction, aberrant meiosis, mitotic recombination, and gene conversion. Under stress conditions, the rate of such genetic changes can increase, leading to rapid adaptation. Conversely, in hybrids formed between lineages of the chytridiomycete frog pathogen Batrachochytriumdendrobatidis (Bd), the parental genotypes are considerably less diverged (0.2% divergent). Bd hybrids are formed from crosses between lineages that rarely undergo sex. A common theme in both species is that hybrids show genome plasticity via aneuploidy or loss of heterozygosity and leverage these mechanisms as a rapid way to generate genotypic/phenotypic diversity. Some hybrids show greater fitness and survival in both virulence and virulence-associated phenotypes than parental lineages under certain conditions. These studies showcase how experimentation in model species such as Cryptococcus can be a powerful tool in elucidating the genotypic and phenotypic consequences of hybridization.

Keywords: AD hybrids; Cryptococcus; aneuploidy; frog chytrid; reproductive incompatibilities.

Figure 1

The currently recognized species in the pathogenic Cryptococcus species complex. The seven species of this complex can be distinguished based on genetic and molecular differences, and each is assigned a distinct molecular type based on clade assignment using multilocus sequence typing markers. Historically, cryptococcal strains were broadly categorized into serotypes based on the antigens found at the cell surface. Hybrids arising from mating between species are named based on the serotypes of the parental strains.

Figure 2

Genomic changes of Cryptococcus occur by sexual and asexual processes. (A) In sexual mating and subsequent meiosis, resulting in the formation of recombinant cells, both euploidy and aneuploidy can be observed; (B) Asexual replication can undergo nondisjunction, endoreduplication, or the formation of titan cells to cause genomic changes.

Figure 3

Parasexuality is a process of reproducing without a reductive cell division (meiosis). With parasexuality, a tetraploid offspring is produced, which is a transient stage followed by random loss of chromosomes during vegetative growth.