The Population Biology of Fungal Invasions

Abstract

Fungal invasions are increasingly recognized as a significant component of global changes, threatening ecosystem health and damaging food production. Invasive fungi also provide excellent models to evaluate the generality of results based on other eukaryotes. We first consider here the reasons why fungal invasions have long been overlooked: they tend to be inconspicuous, and inappropriate methods have been used for species recognition. We then review the information available on the patterns and mechanisms of fungal invasions. We examine the biological features underlying invasion success of certain fungal species. We review population structure analyses, revealing native source populations and strengths of bottlenecks. We highlight the documented ecological and evolutionary changes in invaded regions, including adaptation to temperature, increased virulence, hybridization, shifts to clonality and association with novel hosts. We discuss how the huge census size of most fungi allows adaptation even in bottlenecked, clonal invaders. We also present new analyses of the invasion of the anther-smut pathogen on white campion in North America, as a case study illustrating how an accurate knowledge of species limits and phylogeography of fungal populations can be used to decipher the origin of invasions. This case study shows that successful invasions can occur even when life history traits are particularly unfavourable to long-distance dispersal and even with a strong bottleneck. We conclude that fungal invasions are valuable models to contribute to our view of biological invasions, in particular by providing insights into the traits as well as ecological and evolutionary processes allowing successful introductions.

Effects of Host Variability on the Spread of Invasive Forest Diseases

“…Most vectors of forest pathogens are usually, but not always, insects, and are sometimes referred to as alternate hosts or as having 'hitchhiking' dispersal. Hitchhiking dispersal is favored by typical fungal features such as inconspicuousness, and the production of numerous small propagules [46]. For vector-dependent fungi, if no alternate host exists, the infection cycle is broken.…”

“…Additional uncertainty may be provided by the ability of some pathogens to overcome the so-called 'host species barrier' and infect a new host ('host jump'; [141]), which could accelerate the spread and amplify the consequences of an invasion. Similarly, hybridization events of an established invasive pathogen with native or other similar invasive species [46] could originate new, rapidly-spreading invasive species. Unfortunately, both host jumps and hybridization events of invasive species are particularly difficult to predict.…”

Overlap of latent pathogens in the Botryosphaeriaceae on a native and agricultural host

“…These fungi illustrate an increasingly alarming pattern where many tree pathogens are being moved around the world unknowingly via infected plant tissue. They are consequently being introduced into novel areas where they can then infect a broad range of native and non-native hosts, potentially with negative consequences (Desprez-Loustau et al 2007;Gladieux et al 2015;Liebhold et al 2012;Wingfield et al 2015). Zealand and South Africa (Heath et al 2011).…”

“…Previous studies have noted the ability of these fungi to infect multiple tree species concurrently, including natives and non-natives (Begoude et al 2012;Jami et al 2014;Sakalidis et al 2011). Added to this is the concern of introducing novel genotypes of a species already present in an area, which can become established and/or recombine with other genotypes already present to produce novel genotypes capable of infecting naïve hosts (Gladieux et al 2015). The ability of these fungi to migrate among host plants can facilitate infections of novel hosts and threaten the sustainability of both commercially important plants as well as native ecosystems (Desprez-Loustau et al 2007;Fisher et al 2012).…”

Biological invasions increase the richness of arbuscular mycorrhizal fungi from a Hawaiian subtropical ecosystem

“…For plants with high mycorrhizal dependency, success in new areas is linked to the success of their mutualistic partners. However, in addition to partner compatibility, there are several abiotic and biotic filters underlying the establishment of mycorrhizal plants and fungi (Gladieux et al 2015). We studied the impact of tree-dominated plant invasions on the richness, community composition and phylogenetic structure of AM fungi in Hawaiian soils.…”