Enhanced Outcrossing, Directional Selection and Transgressive Segregation Drive Evolution of Novel Phenotypes in Hybrid Swarms of the Dutch Elm Disease Pathogen <i>Ophiostoma novo-ulmi</i>
In the 1970s, clones of the two subspecies of <i>Ophiostoma novo-ulmi</i>, subsp. <i>americana</i> (SSAM) and subsp. <i>novo-ulmi</i> (SSNU) began to overlap in Europe, resulting in hybrid swarms. By 1983–1986, hybrids with high, SSAM-like growth and pathogenic fi...
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MDPI AG
2021-06-01
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| Series: | Journal of Fungi |
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| Online Access: | https://www.mdpi.com/2309-608X/7/6/452 |
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| author | Clive Brasier Selma Franceschini Jack Forster Susan Kirk |
| author_facet | Clive Brasier Selma Franceschini Jack Forster Susan Kirk |
| author_sort | Clive Brasier |
| collection | DOAJ |
| description | In the 1970s, clones of the two subspecies of <i>Ophiostoma novo-ulmi</i>, subsp. <i>americana</i> (SSAM) and subsp. <i>novo-ulmi</i> (SSNU) began to overlap in Europe, resulting in hybrid swarms. By 1983–1986, hybrids with high, SSAM-like growth and pathogenic fitness comprised ~75% of popula-tions at Limburg, Netherlands and Orvieto, Italy. We resampled these populations in 2008 to examine trends in hybrid fitness traits. Since preliminary sampling in 1979–1980, <i>MAT-1</i> locus frequency had increased from ~0% to ~32% at Orvieto and 5% to ~43% at Limburg, and vegeta-tive incompatibility type frequency had changed from near clonal to extremely diverse at both sites. This represents an enormous increase in outcrossing and recombination potential, due in part to selective acquisition (under virus pressure) of <i>MAT-1</i> and <i>vic</i> loci from the resident <i>O. ulmi</i> and in part to SSAM × SSNU hybridisation. Overt virus infection in the 2008 samples was low (~4%), diagnostic SSAM and SSNU <i>cu</i> and <i>col1</i> loci were recombinant, and no isolates exhib-ited a parental SSAM or SSNU colony pattern. At both sites, mean growth rate and mean patho-genicity to 3–5 m clonal elm were high SSAM-like, indicating sustained directional selection for these characters, though at Orvieto growth rate was slower. The once frequent SSNU-specific <i>up-mut</i> colony dimorphism was largely eliminated at both sites. Perithecia formed by Limburg isolates were mainly an extreme, long-necked SSNU-like form, consistent with transgressive segregation resulting from mismatch of SSAM and SSNU developmental loci. Orvieto isolates produced more parental-like perithecia, suggesting the extreme phenotypes may have been se-lected against. The novel phenotypes in the swarms are remodelling <i>O. novo-ulmi</i> in Europe. Locally adapted genotypes may emerge. |
| first_indexed | 2024-03-10T10:40:19Z |
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| issn | 2309-608X |
| language | English |
| last_indexed | 2024-03-10T10:40:19Z |
| publishDate | 2021-06-01 |
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| spelling | doaj.art-b6b4bef367b5469eba4a33e07cd47f3e2023-11-21T22:59:10ZengMDPI AGJournal of Fungi2309-608X2021-06-017645210.3390/jof7060452Enhanced Outcrossing, Directional Selection and Transgressive Segregation Drive Evolution of Novel Phenotypes in Hybrid Swarms of the Dutch Elm Disease Pathogen <i>Ophiostoma novo-ulmi</i>Clive Brasier0Selma Franceschini1Jack Forster2Susan Kirk3Forest Research, Alice Holt Lodge, Farnham, Surrey GU10 4LH, UKForest Research, Alice Holt Lodge, Farnham, Surrey GU10 4LH, UKForest Research, Alice Holt Lodge, Farnham, Surrey GU10 4LH, UKForest Research, Alice Holt Lodge, Farnham, Surrey GU10 4LH, UKIn the 1970s, clones of the two subspecies of <i>Ophiostoma novo-ulmi</i>, subsp. <i>americana</i> (SSAM) and subsp. <i>novo-ulmi</i> (SSNU) began to overlap in Europe, resulting in hybrid swarms. By 1983–1986, hybrids with high, SSAM-like growth and pathogenic fitness comprised ~75% of popula-tions at Limburg, Netherlands and Orvieto, Italy. We resampled these populations in 2008 to examine trends in hybrid fitness traits. Since preliminary sampling in 1979–1980, <i>MAT-1</i> locus frequency had increased from ~0% to ~32% at Orvieto and 5% to ~43% at Limburg, and vegeta-tive incompatibility type frequency had changed from near clonal to extremely diverse at both sites. This represents an enormous increase in outcrossing and recombination potential, due in part to selective acquisition (under virus pressure) of <i>MAT-1</i> and <i>vic</i> loci from the resident <i>O. ulmi</i> and in part to SSAM × SSNU hybridisation. Overt virus infection in the 2008 samples was low (~4%), diagnostic SSAM and SSNU <i>cu</i> and <i>col1</i> loci were recombinant, and no isolates exhib-ited a parental SSAM or SSNU colony pattern. At both sites, mean growth rate and mean patho-genicity to 3–5 m clonal elm were high SSAM-like, indicating sustained directional selection for these characters, though at Orvieto growth rate was slower. The once frequent SSNU-specific <i>up-mut</i> colony dimorphism was largely eliminated at both sites. Perithecia formed by Limburg isolates were mainly an extreme, long-necked SSNU-like form, consistent with transgressive segregation resulting from mismatch of SSAM and SSNU developmental loci. Orvieto isolates produced more parental-like perithecia, suggesting the extreme phenotypes may have been se-lected against. The novel phenotypes in the swarms are remodelling <i>O. novo-ulmi</i> in Europe. Locally adapted genotypes may emerge.https://www.mdpi.com/2309-608X/7/6/452hybridisationpandemicinvasive speciesfitness traitsperitheciamating type |
| spellingShingle | Clive Brasier Selma Franceschini Jack Forster Susan Kirk Enhanced Outcrossing, Directional Selection and Transgressive Segregation Drive Evolution of Novel Phenotypes in Hybrid Swarms of the Dutch Elm Disease Pathogen <i>Ophiostoma novo-ulmi</i> Journal of Fungi hybridisation pandemic invasive species fitness traits perithecia mating type |
| title | Enhanced Outcrossing, Directional Selection and Transgressive Segregation Drive Evolution of Novel Phenotypes in Hybrid Swarms of the Dutch Elm Disease Pathogen <i>Ophiostoma novo-ulmi</i> |
| title_full | Enhanced Outcrossing, Directional Selection and Transgressive Segregation Drive Evolution of Novel Phenotypes in Hybrid Swarms of the Dutch Elm Disease Pathogen <i>Ophiostoma novo-ulmi</i> |
| title_fullStr | Enhanced Outcrossing, Directional Selection and Transgressive Segregation Drive Evolution of Novel Phenotypes in Hybrid Swarms of the Dutch Elm Disease Pathogen <i>Ophiostoma novo-ulmi</i> |
| title_full_unstemmed | Enhanced Outcrossing, Directional Selection and Transgressive Segregation Drive Evolution of Novel Phenotypes in Hybrid Swarms of the Dutch Elm Disease Pathogen <i>Ophiostoma novo-ulmi</i> |
| title_short | Enhanced Outcrossing, Directional Selection and Transgressive Segregation Drive Evolution of Novel Phenotypes in Hybrid Swarms of the Dutch Elm Disease Pathogen <i>Ophiostoma novo-ulmi</i> |
| title_sort | enhanced outcrossing directional selection and transgressive segregation drive evolution of novel phenotypes in hybrid swarms of the dutch elm disease pathogen i ophiostoma novo ulmi i |
| topic | hybridisation pandemic invasive species fitness traits perithecia mating type |
| url | https://www.mdpi.com/2309-608X/7/6/452 |
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