Clonal Evolution

Naranjo-Ortiz & Gabaldon (2019) — Fungal Evolution: Major Ecological Adaptations and Evolutionary Transitions

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tagsreview, conceptual-synthesis, foundations, selection

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Bibliographic Reference

Naranjo-Ortiz, M. A., & Gabaldon, T. (2019). Fungal evolution: major ecological adaptations and evolutionary transitions. Biological Reviews, 94(4), 1443-1476. https://doi.org/10.1111/brv.12510

Core Argument

This review surveys the major evolutionary and ecological processes that have generated fungal diversity across the kingdom, using a comparative-genomic and phylogenetic framework to reconstruct the transitions from aquatic zoosporic parasitoids to the diverse terrestrial lifestyles that dominate modern ecosystems. The authors argue that the most defining evolutionary novelty within Fungi is terrestrialization — the adaptation to land environments — and propose a novel “white scenario” in which icy environments acted as transitory niches between water and emerged land. Throughout, they advocate that fungi should be studied under traditional ecological principles (niche theory, population dynamics) and that genome-enabled inferences are essential for constructing plausible narratives and testable hypotheses about ancient evolutionary events. The paper explicitly defines “evolutionary transition” as “the acquisition — within a lineage — of a new, sufficiently distinct lifestyle from a previous state” (p. 1444), and applies this framework across the full breadth of fungal ecological diversity.

Methods

This is a narrative synthesis review that integrates evidence from multiple methodological traditions: (a) comparative genomics (drawing on genome sequences from diverse fungal lineages, including early-diverging groups, mycoparasites, lichen mycobionts, black fungi, and yeasts); (b) phylogenetic analyses of ancestral character reconstruction and molecular dating; (c) environmental sequencing and barcoding studies (18S rRNA, ITS); (d) fossil evidence (Rhynie Chert, Ediacaran fossils); and (e) traditional culture-based and morphological characterization. The authors describe their approach as deliberately “narrative” — using intuition and extrapolation to construct hypothetical evolutionary scenarios, analogous to paleontological reconstruction — and note that this is both a strength (generating testable hypotheses) and a limitation (requiring caution against overinterpretation).

Key Findings

The paper’s conclusions are presented as 9 numbered points in Section XI, supplemented by major findings from each substantive section. Key findings include:

  1. Zoosporic ancestry. The first fungi were zoosporic parasitoids of other unicellular eukaryotes. This lifestyle is retained in the Opisthosporidia, Chytridiomycota, and Blastocladiomycota. The last common fungal ancestor (LCFA) was likely a parasitoid of microalgae with phagotrophic capabilities, amoeboid and flagellar motility, and chitinous cell walls in at least some life stages (Section II).

  2. Terrestrialization scenarios. The authors propose three scenarios for the colonization of land: the “green” scenario (co-evolution with Streptophyta and land plants), the “brown” scenario (colonization of protosoils and sediments, independent of plants), and the novel “white” scenario, in which icy environments — characterized by high spatial heterogeneity, osmotic microniches, and algal necromass — served as transitional habitats. The “white” scenario notes that estimated dates of terrestrial fungal radiation coincide with Precambrian glaciations (the Cryogenian, “Snowball Earth”). The authors suggest the three factors may have acted sequentially or in combination (Section III).

  3. Mycoparasitism as an early and versatile lifestyle. Mycoparasitic associations appear very early in fungal evolution (found in the Rhynie Chert, ~410 Ma) and are widespread across early-diverging lineages. The authors document that mycoparasitism has evolved independently through different molecular strategies (e.g., expanded chitinases in Trichoderma, loss of metabolic pathways in biotrophic mycoparasites), and that a relationship exists between mycoparasites and pathogens of invertebrates, with interconversion between lifestyles common in the Hypocreales (Section IV.1).

  4. Animal parasitism: obligate to facultative. Several clades have independently acquired obligate animal parasitism with hallmarks of genomic and metabolic reduction (Microsporidia, Pneumocystis, Laboulbeniomycetes). Invertebrate parasites are evolutionarily linked to mycoparasites and amoebophagous fungi, using chitin-degrading abilities to attack hosts. Vertebrate parasites, by contrast, seem to emerge from commensalism, usually as facultative pathogens. The paper emphasizes that “[f]ungal infections in humans are a cause of great public health concern” (Section V).

  5. Plant-fungus relationships are ancient. The relationship between fungi and plants predates land colonization. Plant parasitism follows two main strategies — biotrophy and necrotrophy — that impose “radically different evolutionary pressures … reflected in their genome characteristics.” Biotrophs tend toward genome reduction (loss of metabolic pathways, smaller gene numbers), while host-restricted necrotrophs also show genome compaction relative to broad-spectrum pathogens. The two-speed evolution model (pathogenesis islands in rapidly evolving chromosomal regions) and hybridization are identified as important sources of rapid adaptation (Section VI).

  6. Lignin degradation evolved once. The ability to fully degrade lignin evolved only once in the biosphere, within the Agaricomycetes (white rot fungi). This capacity, related to expansions of secreted laccases and heme-peroxidases, likely arose in response to lignin accumulation during the Carboniferous and “greatly affected global carbon cycles and propelled the diversification of the Agaricomycetes” (Section VI.4).

  7. Lichenization is ancient and dynamic. Around 20,000 species of Pezizomycotina (nearly half the subphylum) have adopted the lichen lifestyle. Multiple independent origins are now favored over a single ancestral event, with “the loss and acquisition of a lichenic lifestyle being much more common than previously thought.” Lichen mycobionts show genomic hallmarks including expansions in nitrogen/magnesium transporters, desiccation-protection proteins, and evidence of horizontal gene transfer from bacteria (Section VII).

  8. Black fungi as polyextremophilic specialists. Black fungi (Dothideomycetes, Eurotiomycetes) are characterized by extreme melanization, tolerance to desiccation, ionizing radiation, heavy metals, oligotrophy, and near-saturation salt concentrations. They share phylogenetic proximity with lichen-forming fungi, suggesting a functional relationship. Whole-genome duplication in Hortaea werneckii (recently duplicated ion pumps and channels) represents the only described example of WGD in black fungi (Section VIII).

  9. The yeast lifestyle is a convergent prokaryote-like strategy. The authors propose a formal definition of the “yeast lifestyle” as a unicellular or dimorphic life strategy with reduced extracellular metabolism, compact genome (increased gene density, reduced introns/intergenic content), and streamlined regulatory networks — a “prokaryote-like lifestyle in fungi.” This lifestyle evolved independently in Saccharomycotina, Taphrinomycotina, Pucciniomycotina, and Ustilaginomycotina. Yeasts compete with prokaryotes in high-osmotic, carbon-rich environments and dominate marine fungal communities. The paper notes that “[t]ransition to a yeast lifestyle is often accompanied by convergent changes in regulatory networks” (Section IX).

  10. Genomics needs integration with traditional approaches. The concluding remark states that “while genomics has revolutionized our view of fungi, there is a growing need to merge this type of approaches with more traditional ones, such as biochemical, genetic, ecological, morphological and ontological in order to provide testable hypotheses regarding fungal biology” (Conclusion 9).

Concepts Introduced or Used

  • Evolutionary transition — defined as the acquisition within a lineage of a new, sufficiently distinct lifestyle from a previous state (Section I). Examples include parasitism from free-living ancestors, lichenization, and radical changes in body plan or cellular organization.
  • Mould lifestyle — the generalized fungal lifestyle: mycelial thallus with hyphae, chitinous cell wall, extracellular digestion, territorial chemical warfare, and spore dispersal. Used as a reference paradigm, though not ancestral within the kingdom.
  • Yeast lifestyle — a formally proposed ecotype: unicellular or dimorphic fungi with a main unicellular stage, highly limited extracellular metabolism, reduced secondary metabolism, compact genome, rapid growth, and occupation of prokaryote-like niches (high-osmotic, carbon-rich environments). Distinct from the traditional taxonomic term “yeast.”
  • Terrestrialization — the evolutionary transition from aquatic to terrestrial habitats; the most definitory novelty within Fungi, involving hyphal growth, loss of the flagellum, and recalibrated calcium homeostasis.
  • Mycoparasitism — the parasitism of fungi by other fungi. Both biotrophic and necrotrophic forms exist, with the former showing reduced metabolic capacity and narrow host range, and the latter showing high aggressiveness and broad host range.
  • Biotrophy vs. necrotrophy — biotrophic pathogens feed on living host tissue using specialized mechanisms to avoid host defenses; necrotrophic pathogens kill host tissue and feed on the necromass. These strategies impose opposing evolutionary pressures on genome size, gene content, and metabolic capacity.
  • Lichenization — the symbiotic association between a fungal mycobiont (usually Pezizomycotina) and a photobiont (cyanobacteria or chlorophyte), forming a macroscopic composite thallus.
  • Horizontal gene transfer (HGT) — gene exchange between species, likely facilitated by mycoparasitism (through cell wall degradation removing physical barriers to DNA acquisition). Documented cases include bacterial-to-lichen, fungal-to-alga, and mycoparasite-to-host transfers.
  • Niche theory — the paper argues that traditional ecological principles, including niche theory and population dynamics, are applicable to fungal ecology despite the radically different spatial scales of microbial habitats.
  • Genomic compaction — increased gene density, reduced intron and intergenic content, observed convergently across yeast lineages and in host-restricted parasites.
  • Convergent evolution in fungi — the independent evolution of similar ecological traits (yeast lifestyle, mycoparasitism, entomopathogenicity, nematophagy) across phylogenetically distant lineages, often through different molecular mechanisms.
  • Two-speed evolution model — the concentration of rapidly evolving pathogenesis-related genes in specific chromosomal regions or small chromosomes, enabling rapid host adaptation while maintaining conserved functions in the rest of the genome (Section VI.3).
  • “White” scenario — the proposal that icy environments (glaciers, cryoconites, brine channels) served as transitional niches between aquatic and terrestrial habitats during fungal terrestrialization, particularly during the Cryogenian glaciations.

Entities Referenced

Major fungal phyla and subphyla: Opisthosporidia (Rozellida, Aphelida, Microsporidia), Chytridiomycota, Blastocladiomycota, Neocallimastigomycota, Zoopagomycota (Entomophthoromycotina, Kickxellomycotina, Zoopagomycotina), Mucoromycota (Mucoromycotina, Mortierellomycotina), Glomeromycota, Ascomycota (Taphrinomycotina, Saccharomycotina, Pezizomycotina), Basidiomycota (Pucciniomycotina, Ustilaginomycotina, Agaricomycotina), Dikarya.

Specific genera and species mentioned (representative selection): Rozella, Batrachochytrium dendrobatidis, Batrachochytrium salamandrivorans, Allomyces, Catenaria, Rhizophagus irregularis, Glomus tenue, Geosiphon, Densospora, Trichoderma, Hypocrea, Ampelomyces, Beauveria, Cordyceps, Ophiocordyceps, Tolypocladium, Clonostachys, Escovopsis, Arthrobotrys, Coprinus, Pleurotus, Armillaria, Moniliophthora, Cryptococcus (Filobasidiella), Malassezia, Candida albicans, Nakaseomyces glabratus (syn. Candida glabrata), Saccharomyces cerevisiae, Schizosaccharomyces pombe, Yarrowia lipolytica, Aspergillus, Penicillium, Fusarium, Pneumocystis, Histoplasma, Coccidioides, Blastomyces, Paracoccidioides, Pseudogymnoascus destructans, Hortaea werneckii, Cryomyces antarcticus, Rachicladosporium, Entomophthora muscae, Basidiobolus, Conidiobolus, Ustilago, Rhizoctonia solani, Erysiphe necator, Endocarpon pusillum.

Limitations

The authors explicitly identify several limitations throughout the review:

  1. Culture-based biases. Standard isolation protocols can only recover a fraction of natural fungal diversity — “whether because nutritional requirements are not met, inter-species relationships are broken or simply because faster growing microbes out-compete slower ones in culture environments” (Section X).

  2. Limited genomic data for many clades. For many important groups — early-diverging lineages, biotrophic mycoparasites, lichen mycobionts, black fungi, Laboulbeniomycetes, Harpellales — genomic data “remains very limited” or comes from single species. The authors note that “for many microbial clades, we know little more than the fact they exist, even though some are very abundant in nature” (Section X).

  3. Narrative approach as both strength and limitation. The paper explicitly acknowledges that evidence for ancient evolutionary scenarios (terrestrialization, origin of mycorrhizae) is “necessarily only circumstantial and mostly based on extrapolations from our knowledge of modern environments” (Section III). They defend the narrative approach as necessary for hypothesis generation but emphasize that it imposes “the biggest challenge in this field” (Section X).

  4. Difficulty reconstructing ancient events. The lack of a clear fossil record for early fungal evolution (particularly for parasitoids and microbes with low preservation potential) makes key inferences tentative. The phylogenetic position of the Chytridiomycota “remains poorly resolved” (Section II), and the timing and order of terrestrialization events are contested.

  5. Taxonomic challenges. Many genera (e.g., Rhodotorula) are “clearly paraphyletic” (Section IX), and cryptic diversity is likely vast. Basidiolichen diversity is “hugely underestimated” (Section VII).

  6. Methodological barriers. Biotrophic fungi are difficult to culture; lichen mycobionts require either independent culture or metagenomic approaches; black fungi have “extremely resistant cells” that “make DNA extraction very difficult” (Section VIII); sequence-based approaches are “prone to biases and artefacts, both experimental and computational” (Section X).

  7. Knowledge gaps in mycoparasitism and protozoan interactions. The authors state that “our knowledge on mycoparasitic interactions remains very limited” (Section IV.1) and that “the relationship between fungi and amoeboid protozoans is largely unexplored” (Section IV.2), with the scope and ecological relevance of both “not yet accurately estimated.”

Relevance to Clonal Evolution

This review provides a rich formal framework for conceptualizing evolutionary transitions that is directly applicable to cancer evolution. The paper’s definition of an “evolutionary transition” — the acquisition of a new, sufficiently distinct lifestyle from a previous state — parallels the transitions cancer cell populations undergo during disease progression: from localized growth to invasive dissemination, from therapy-sensitive to therapy-resistant, and from angiogenesis-dependent to angiogenesis-independent. Several specific parallels are notable:

Niche colonization and metastasis. The paper’s detailed treatment of how fungi colonize novel habitats — from aquatic environments to soil, from soil to host tissues, from one host type to another — mirrors the ecological theory of metastasis as niche colonization. Fungi that are “facultative parasites” that “use specialized adaptations to invade the animal host” while also existing “as free-living organisms in the environment” (Section V.1) parallel circulating tumor cells that must adapt to both primary and metastatic microenvironments.

Lifestyle switching and phenotypic plasticity. The documented interconversion between mycoparasitic, entomopathogenic, endophytic, and saprotrophic lifestyles — particularly in the Hypocreales — maps onto cancer cell phenotypic plasticity, where cells transition between proliferative, invasive, and drug-tolerant states. The authors note that “interconversion between these different lifestyles seems to have been common in the Hypocreales” (Section V.3), illustrating how a single lineage can harbor multiple ecological competencies.

Mycoparasitism and clonal competition. Mycoparasitic interactions — where one fungus infects, competes with, or eliminates another — are a direct ecological parallel to clonal competition in tumors. The description of necrotrophic mycoparasites as “highly aggressive” with a “broad range of hosts” (Section IV.1) resembles aggressive subclones that outcompete less fit neighbors. The paper’s observation that mycoparasites produce “toxic secondary metabolites, melanin, and reactive oxygen species” for defense (Section IV.1) parallels the microenvironmental warfare between cancer subclones.

Horizontal gene transfer and genomic instability. The review discusses how mycoparasites can “serve as donors and facilitators for horizontal gene transfer (HGT), by either donating DNA directly to the host or by removing the host cell wall” (Section IV.1), and notes that HGT has been demonstrated in laboratory conditions (from Parasitella to Absidia). This is mechanistically analogous to horizontal DNA transfer in tumors (via extracellular vesicles, apoptotic bodies, or cell fusion) and to the genomic instability that drives subclonal diversification.

Genome compaction and the driver/passenger distinction. The yeast lifestyle’s convergent genomic compaction — reduced intergenic content, streamlined regulatory networks, loss of dispensable metabolic pathways — provides an ecological framework for understanding the distinction between driver mutations (genes essential for the “yeast lifestyle” of rapid proliferation under selection) and passenger mutations (the genomic equivalent of non-essential secondary metabolism). The paper’s observation that “[t]ransition to a yeast lifestyle is often accompanied by convergent changes in regulatory networks” (Section IX) parallels the convergent emergence of hallmark capabilities across cancer types.

The “evolutionary transition” concept as a formal framework. Perhaps most significantly, this paper operationalizes “evolutionary transition” as a formal concept that can be applied across kingdoms. The authors’ framework — identifying the ancestral state, the selective pressures driving the transition, the genomic and phenotypic changes that enable it, and the new ecological opportunities it unlocks — is directly transferable to cancer evolution, where transitions such as the acquisition of metastatic ability, immune evasion, or therapy resistance can be analyzed through the same lens. The paper’s emphasis on combining genomic data with ecological and population-level thinking (Section X) mirrors the emerging synthesis in cancer evolution between clonal-evolution theory, dual-regime-evolution models, and ecology-invasion-olog frameworks.

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