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 Cryptococcus neoformans × Cryptococcus deneoformans, 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 Batrachochytrium dendrobatidis (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.

Genomic evidence for a hybrid origin of the yeast opportunistic pathogen Candida albicans

“…From a clinical perspective, hybridization can be regarded as a source of new potentially pathogenic lineages [1]. Many hybrids are becoming important agents of human infection, as it is the case of Candida or Cryptococcus species [2,3,[18][19][20]37], with hybridization being also associated to a possible increase in virulence [4]. In a world where globalization and global warming are a reality promoting the expansion of certain species to locations where they have never been, the chances of new events of hybridization are possibly increasing.…”

“…In fungi, advances in nextgeneration sequencing have recently allowed the identification of many hybrid lineages as well [13,14], of which some have importance for biotechnology and food or beverage industries [15][16][17]. Hybrids with medical relevance have also been described, particularly in Cryptococcus and Candida clades [1][2][3][18][19][20], with earlier studies suggesting that hybridization might be related to the emergence of virulence traits in some of these species [1][2][3][4].…”

Fungal species concepts in the genomics era

“…At the genetic level, incomplete lineage sorting could also result in false signals in population relationships (Steenkamp et al 2018). With increasing commercial trade and human travel, as well as our increasing influence on the environment, both the genotypic and phenotypic features of fungal populations and species could be severely impacted (e.g., Xu et al 1997;Chen et al 2016;Samarasinghe et al 2020). In the section below, I highlight some of the features of fungi and their implications for fungal species concepts.…”

“…On the other hand, divergent populations with significant genome sequence and chromosome structure differences can mate and generate viable sexual progeny (e.g., Samarasinghe and Xu 2018;Steenkamp et al 2018;You and Xu 2018). Furthermore, sterile fungal hybrids can reproduce asexually by mitosis and generate abundant genetic diversity through mitotic recombination, contributing to their rapid adaptations to novel environmental conditions (Mixao and Gabaldon 2018; Dong et al 2020;Samarasinghe et al 2020). Indeed, the uniqueness of fungal reproduction has made the application of bio-logical species concepts to define fungal species often not practical (Singer 1986;Kurtzman et al 2011).…”

Emerging Cryptococcus gattii species complex infections in Guangxi, southern China

“…Hybridization between the two cryptococcal species complexes seems to be a much rarer event in nature compared to hybridization between C. neoformans species complex lineages [42]. Even though the mating between the parental lineages can be induced in the laboratory, their progenies were not commonly reported in the environmental and clinical samples [43]. Recombination may also occur between the AFLP4/VGI and AFLP6/VGII isolates in China because previous research has highlighted possible gene transfer (introgression) between different C. gattii s.l.…”