title: Genetic and genomic evidence of niche partitioning and adaptive radiation in mountain pine beetle fungal symbionts.
abstract: Bark beetles form multipartite symbiotic associations with blue stain fungi (Ophiostomatales, Ascomycota). These fungal symbionts play an important role during the beetle's life cycle by providing nutritional supplementation, overcoming tree defences and modifying host tissues to favour brood development. The maintenance of stable multipartite symbioses with seemingly less competitive symbionts in similar habitats is of fundamental interest to ecology and evolution. We tested the hypothesis that the coexistence of three fungal species associated with the mountain pine beetle is the result of niche partitioning and adaptive radiation using SNP genotyping coupled with genotype-environment association analysis and phenotypic characterization of growth rate under different temperatures. We found that genetic variation and population structure within each species is best explained by distinct spatial and environmental variables. We observed both common (temperature seasonality and the host species) and distinct (drought, cold stress, precipitation) environmental and spatial factors that shaped the genomes of these fungi resulting in contrasting outcomes. Phenotypic intraspecific variations in Grosmannia clavigera and Leptographium longiclavatum, together with high heritability, suggest potential for adaptive selection in these species. By contrast, Ophiostoma montium displayed narrower intraspecific variation but greater tolerance to extreme high temperatures. Our study highlights unique phenotypic and genotypic characteristics in these symbionts that are consistent with our hypothesis. By maintaining this multipartite relationship, the bark beetles have a greater likelihood of obtaining the benefits afforded by the fungi and reduce the risk of being left aposymbiotic. Complementarity among species could facilitate colonization of new habitats and survival under adverse conditions.
authors.affiliation: Department of Forest and Conservation Sciences, The University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada, V6T 1Z4.
authors.forename: Dario I
authors.initials: DI
authors.lastname: Ojeda Alayon
authors.affiliation: Department of Forest and Conservation Sciences, The University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada, V6T 1Z4.
authors.forename: Clement K M
authors.initials: CK
authors.lastname: Tsui
authors.affiliation: Department of Forest and Conservation Sciences, The University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada, V6T 1Z4.
authors.forename: Nicolas
authors.initials: N
authors.lastname: Feau
authors.affiliation: Department of Forest and Conservation Sciences, The University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada, V6T 1Z4.
authors.forename: Arnaud
authors.initials: A
authors.lastname: Capron
authors.affiliation: Department of Forest and Conservation Sciences, The University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada, V6T 1Z4.
authors.forename: Braham
authors.initials: B
authors.lastname: Dhillon
authors.affiliation: Department of Forest and Conservation Sciences, The University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada, V6T 1Z4.
authors.forename: Yiyuan
authors.initials: Y
authors.lastname: Zhang
authors.affiliation: Department of Wood Science, The University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada, V6T 1Z4.
authors.forename: Sepideh
authors.initials: S
authors.lastname: Massoumi Alamouti
authors.affiliation: Ecosystem Science and Management Program, University of Northern British Columbia, 3333 University Way, Prince George, BC, Canada, V2N 4Z9.
authors.forename: Celia K
authors.initials: CK
authors.lastname: Boone
authors.affiliation: Department of Forest and Conservation Sciences, The University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada, V6T 1Z4.
authors.forename: Allan L
authors.initials: AL
authors.lastname: Carroll
authors.affiliation: Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada, T6G 2R3.
authors.forename: Janice E K
authors.initials: JE
authors.lastname: Cooke
authors.affiliation: Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada, T6G 2R3.|Natural Resources Canada, Canadian Forest Service, Great Lakes Forestry Centre, 1219 Queen St E, Sault Ste. Marie, ON, Canada, P6A 2E5.
authors.forename: Amanda D
authors.initials: AD
authors.lastname: Roe
authors.affiliation: Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada, T6G 2R3.
authors.forename: Felix A H
authors.initials: FA
authors.lastname: Sperling
authors.affiliation: Department of Forest and Conservation Sciences, The University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada, V6T 1Z4.|Institut de Biologie Intégrative des Systèmes, Université Laval, 1030 Avenue de la Médecine, Québec City, QC, Canada, G1V 0A6.
authors.forename: Richard C
authors.identifier: http://orcid.org/0000-0003-4006-532X
authors.initials: RC
authors.lastname: Hamelin
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D000818:Animals; D005075:Biological Evolution; D001517:Coleoptera / Q000382:microbiology*; D004271:DNA, Fungal / Q000235:genetics; D017753:Ecosystem; D004777:Environment; D005787:Gene Frequency; D005828:Genetics, Population; D023281:Genomics; D055155:Ophiostomatales / Q000235:genetics*; D010641:Phenotype; D020641:Polymorphism, Single Nucleotide; D013559:Symbiosis
chemical_list: D004271:DNA, Fungal
keywords: 
  Dendroctonus
  ; 
  Grosmannia
  ; 
  Leptographium
  ; 
  Ophiostoma
  ; blue stain fungi; genotype-environment association; multipartite symbionts; outbreak; pine pathogens; tree disease