Genetic structure of Metarhizium species in western USA: finite populations composed of divergent clonal lineages with limited evidence for recombination

Authors: Rehner, Stephen

Submitted to: Journal of Invertebrate Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/10/2020
Publication Date: 10/16/2020
Citation: Rehner, S.A. 2020. Genetic structure of Metarhizium species in western USA: finite populations composed of divergent clonal lineages with limited evidence for recombination. Journal of Invertebrate Pathology. 177(1). https://doi.org/10.1016/j.jip.2020.107491.
DOI: https://doi.org/10.1016/j.jip.2020.107491

Interpretive Summary: Little is known about the genetic diversity in natural populations of fungi used for biological control of pest insects. This study demonstrates that populations of five species of the fungal insect pathogen Metarhizium in western North America are characterized by very small numbers of individuals that reproduce and evolve asexually. This result is significant because it shows that natural populations over large areas display limited genetic diversity and evidence of genetic exchange. The latter observation is significant because it suggests that release of strains for insect control are unlikely to interbreed and exchange genes with indigenous strains. Information from this study will be used by insect pathologists and mycologists investigating fungal diseases of insects in support of pest management programs for field crop and forest pests.

Technical Abstract: Genomic evidence indicates that globally distributed, soil-associated Metarhizium species used in insect biological control are facultatively sexual, yet their sexual morphs have not been observed and genetic confirmation that they recombine in nature is limited. We describe community-wide genetic diversity of Metarhizium species among 492 soil isolates from 14 states of western USA to assess the contributions of clonality and recombination in determining their population structures. Seven species lineages, varying >100-fold in relative abundance, were identified by phylogenetic analysis of 5’ EF1-'' (5TEF), including M. robertsii (n=292), M. guizhouense (n=48), M. brunneum (n=37), M. lepidiotae (n=14), M. pemphigi (n=11), M. anisopliae (n=7) and M. pingshaense (n=2). Analyses of composite multilocus genotypes integrating 5TEF sequence, multilocus microsatellite and mating type alleles were conducted on a subset of 242 isolates reveal that all populations display significant clonal structure. Remarkably, following clone-correction to remove duplicated genotypes and collapse clonal lineages, all populations were found to be composed of a dozen or fewer genetically unique individuals. M. robertsii was the only population determined to be in linkage equilibrium. However, the high proportion of private alleles differentiating M. robertsii clonal lineages indicate the absence of panmixia and that the recombination signal detected may be historical and not contemporary. Also, within M. robertsii, M. brunneum and M. guizhouense, there are isolates with closely related genotypes of opposite mating type, which suggests that the sexual cycle, when it occurs, tend to involve closely related individuals. The finite number of unique genetic individuals observed may signify that Metarhizium species in western North America represent isolated peripheral populations established by limited numbers of founders within which there has been little recombination relative to the pace of clonal expansion and evolution.