Hybridization and introgression drive genome evolution of Dutch elm disease pathogens

Hessenauer, Pauline; Fijarczyk, Anna; Martin, Hélène; Prunier, Julien; Charron, Guillaume; Chapuis, Jérôme; Bernier, Louis; Tanguay, Philippe; Hamelin, Richard; Landry, Christian R.

doi:10.1038/s41559-020-1133-6

Cited by 54 publications

(73 citation statements)

References 112 publications

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“…High divergence between recombined lineages and relatively little divergence between local populations led us to conclude that recent hybridization was followed by rapid expansion of a recombinant G. bulllatarudis strain. Similar patterns of successful admixed hybrid genotypes have been reported for many other parasites, including schistosomes (Kincaid-Smith et al, 2019; Platt et al, 2019), Trypanosoma (see Tihon et al, 2017) and Leishmania (see Rogers et al, 2014) species, as well as Dutch elm disease pathogens (Brasier, 2001; Hessenauer et al, 2020) and other fungi pathogens (Mixão & Gabaldón, 2018) highlighting the role of recombination between divergent genomes in parasite evolution. Our analysis of G. turnbulli genomes indicates, that unlike its congener G. bullatarudis , natural expansion occurred without prior recombination.…”

Section: Discussionsupporting

confidence: 66%

Expansion of frozen hybrids in the guppy ectoparasite,Gyrodactylus turnbulli

Konczal

Przesmycka

Mohammed

et al. 2020

Preprint

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18Hybridization is one of the major factors contributing to the emergence of highly successful parasites. 19Hybrid vigor can play an important role in this process, but its contribution to the evolutionary 20 success of parasites has not been demonstrated. Here, we identify an invasion of a "frozen hybrid" 21 genotype in natural populations of Gyrodactylus turnbulli, ectoparasitic flatworms with facultative 22 sexual reproduction and significant impact on cultured fish. We re-sequenced genomes of these 23 parasites infecting guppies from six Trinidad and Tobago populations, and found surprisingly high 24 discrepancy in genome-wide nucleotide diversity between islands. The elevated heterozygosity on 25 Tobago is maintained by predominantly clonal reproduction of hybrids formed from two diverged 26 genomes. Hybridization has been followed by spread of the hybrids across the island, implying a 27 selective advantage compared to native genotypes. Our results highlight the potential consequences 28 of heterosis in the epidemiology of parasite hybrids and its impact on population genomic diversity. 29 30 conditions (Laine et al., 2019). The probability of hybridization increases when species co-infect the 46 same host, and such systems may be considered hotspots for studying its phenotypic effects. 47 157

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Section: Discussionsupporting

confidence: 66%

Expansion of frozen hybrids in the guppy ectoparasite,Gyrodactylus turnbulli

Konczal

Przesmycka

Mohammed

et al. 2020

Preprint

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“…The climatic niches in the invasive ranges of DED showed the highest degrees of niche filling compared to the native range possibly due to limited sampling of the pathogen in the presumed native range [82]. The niche expansion in North America and Europe could be linked to the differences in the fungal pathogen adaptation, the observed hybridization among the subpopulations of the pathogen and the availability of highly susceptible host species [33,37,83,84]. Brasier [83] has described the expansion of the Dutch elm disease outbreak (the second pandemic) following the appearance of a second species, O. novo-ulmi, that had optimum growth temperature (22 • C) lower than that of the original pathogen, O. ulmi (27.5-30 • C); it is likely that O. novo-ulmi is better adapted to more temperate and cooler climates than O. ulmi, which is considered to be better adapted to subtropical climates [33,85].…”

Section: Discussionmentioning

confidence: 99%

“…We compiled an occurrence database of WW, ALB, SOD, and DED from various sources, including, (1) records provided by the Canadian Food Inspection Agency (CFIA); (2) Global Biodiversity Information Facility database, an online database for species occurrences; (3) Centre for Agriculture and Bioscience International (CABI) invasive species compendium; and (4) scientific articles and maps ( Figure 1) [32,[37][38][39]. We used Google Earth (Google Inc 2020, Mountain View, CA, USA) to obtain proxy coordinates for records lacking geographic coordinates.…”

Section: Occurrence Datamentioning

confidence: 99%

Assessing Niche Shifts and Conservatism by Comparing the Native and Post-Invasion Niches of Major Forest Invasive Species

Srivastava

Liang

Keena

et al. 2020

Insects

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Invasive species experience biotic and abiotic conditions that may (or may not) resemble their native environment. We explored the methodology of determining climatic niches and compared the native and post-invasion niches of four invasive forest pests to determine if these species experienced shifts or changes in their new climatic niches. We used environmental principle components analysis (PCA-env) method to quantify climatic niche shifts, expansions, and temporal changes. Furthermore, we assessed the effect of variable selection in the delineation and comparison of niche space. We found that variable selection influenced the delineation and overlap of each niche, whereas the subset of climatic variables selected from the first two PCA-env axes explained more variance in environmental conditions than the complete set of climatic variables for all four species. Most focal species showed climatic niche shifts in their invasive range and had not yet fully occupied the available niche within the invaded range. Our species varied the proportion of niche overlap between the native and invasive ranges. By comparing native and invasive niches, we can help predict a species’ potential range expansion and invasion potential. Our results can guide monitoring and help inform management of these and other invasive species.

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“…Instances of inter- and intra-kingdom HGT, genetic introgression following hybridization, and meiotic drive elements have all been shown to be strong forces of genomic evolution and have thus received increased attention over the last decade. Robust whole-genome sequencing of isolates within a species as well as the increasing diversity of fungal species sequenced have allowed for the identification of these allelic transmission events and mechanisms and also shed light on their origins 12 – 14 , 85 – 91 .…”

Section: Small-scale Evolution Of Fungal Genomesmentioning

confidence: 99%

“…Two recent examples include 1) the loss and regain of fermentation capacity by Kluyveromyces lactis, which was demonstrated to be a result of introgression of a subtelomeric locus from Kluyveromyces marxianus , and 2) finding that a lichen-forming Rhizoplaca species likely originated from an introgressive hybridization event 12 , 13 . In another intriguing study, introgression following hybridization was shown to be the primary force of evolution in the fungal pathogen responsible for Dutch elm disease, driving changes in host–pathogen interactions via introgression of virulence-associated genes and changes in sexual reproduction via introgression of mating-type loci 14 .…”

Section: Small-scale Evolution Of Fungal Genomesmentioning

confidence: 99%

Advances in understanding the evolution of fungal genome architecture

2020

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Diversity within the fungal kingdom is evident from the wide range of morphologies fungi display as well as the various ecological roles and industrial purposes they serve. Technological advances, particularly in long-read sequencing, coupled with the increasing efficiency and decreasing costs across sequencing platforms have enabled robust characterization of fungal genomes. These sequencing efforts continue to reveal the rampant diversity in fungi at the genome level. Here, we discuss studies that have furthered our understanding of fungal genetic diversity and genomic evolution. These studies revealed the presence of both small-scale and large-scale genomic changes. In fungi, research has recently focused on many small-scale changes, such as how hypermutation and allelic transmission impact genome evolution as well as how and why a few specific genomic regions are more susceptible to rapid evolution than others. High-throughput sequencing of a diverse set of fungal genomes has also illuminated the frequency, mechanisms, and impacts of large-scale changes, which include chromosome structural variation and changes in chromosome number, such as aneuploidy, polyploidy, and the presence of supernumerary chromosomes. The studies discussed herein have provided great insight into how the architecture of the fungal genome varies within species and across the kingdom and how modern fungi may have evolved from the last common fungal ancestor and might also pave the way for understanding how genomic diversity has evolved in all domains of life.

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Hybridization and introgression drive genome evolution of Dutch elm disease pathogens

Cited by 54 publications

References 112 publications

Expansion of frozen hybrids in the guppy ectoparasite,Gyrodactylus turnbulli

Expansion of frozen hybrids in the guppy ectoparasite,Gyrodactylus turnbulli

Assessing Niche Shifts and Conservatism by Comparing the Native and Post-Invasion Niches of Major Forest Invasive Species

Advances in understanding the evolution of fungal genome architecture

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