Genetic and genomic evidence of niche partitioning and adaptive radiation in mountain pine beetle fungal symbionts

Molecular Ecology

Volumn 26, Issue 7, 2017, Pages 2077-2091

  Ojeda Alayon, Dario I ^a   Tsui, Clement K M ^a   Feau, Nicolas ^a   Capron, Arnaud ^a   Dhillon, Braham ^a   Zhang, Yiyuan ^a   Massoumi Alamouti, Sepideh ^a   Boone, Celia K ^b   Carroll, Allan L ^a   Cooke, Janice E K ^c   Roe, Amanda D ^c,d   Sperling, Felix A H ^c   Hamelin, Richard C ^a,e  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF NORTHERN BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

^d GREAT LAKES FORESTRY CENTRE   (Canada)

^e UNIVERSITÉ LAVAL   (Canada)

Author keywords

blue stain fungi; Dendroctonus; genotype environment association; Grosmannia; Leptographium; multipartite symbionts; Ophiostoma; outbreak; pine pathogens; tree disease

Indexed keywords

FUNGAL DNA;

ADAPTATION; ANIMAL; BEETLE; ECOSYSTEM; ENVIRONMENT; EVOLUTION; GENE FREQUENCY; GENETICS; GENOMICS; MICROBIOLOGY; OPHIOSTOMATALES; PHENOTYPE; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM; SYMBIOSIS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BEETLES; BIOLOGICAL EVOLUTION; DNA, FUNGAL; ECOSYSTEM; ENVIRONMENT; GENE FREQUENCY; GENETICS, POPULATION; GENOMICS; OPHIOSTOMATALES; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; SYMBIOSIS;

EID: 85017208792     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.14074     Document Type: Article

References (82)

1. Adams AS, Six DL (2007) Temporal variation in mycophagy and prevalence of fungi associated with developmental stages of Dendroctonus ponderosae (Coleoptera: Curculionidae). Environmental Entomology, 1, 64–72.
2. Addison AL, Powell JA, Six D, Moore M, Bentz BJ (2013) The role of temperature variability in stabilizing the mountain pine beetle–fungus mutualism. Journal of Theoretical Biology, 335, 40–50.
3. Agapow PM, Burt A (2001) Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1, 101–102.
4. Alamouti SM, Wang V, Diguistini S et al. (2011) Gene genealogies reveal cryptic species and host preferences for the pine fungal pathogen Grosmannia clavigera. Molecular Ecology, 20, 2581–2602.
5. Alamouti SM, Haridas S, Feau N et al. (2014) Comparative genomics of the pine pathogens and beetle symbionts in the genus Grosmannia. Molecular Biology and Evolution, 31, 1454–1474.
6. Amarasekare P (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecology Letters, 6, 1109–1122.
7. Aylward FO, Currie CR, Suen G (2012) The evolutionary innovation of nutritional symbioses in leaf-cutter ants. Insects, 3, 41–61.
8. Ayres MP, Wilkens RT, Ruel JJ, Lombardero MJ, Vallery E (2000) Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi. Ecology, 81, 2198–2210.
9. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1–48.
10. Batista PD, Janes JK, Boone CK, Murray BW, Sperling FAH (2016) Adaptive and neutral markers both show continent-wide population structure of mountain pine beetle (Dendroctonus ponderosae). Ecology and Evolution, 6, 6292–6300.
11. Bentz BJ, Six DL (2006) Ergosterol content of fungi associated with Dendroctonus ponderosae and Dendroctonus rufipennis (Coleoptera: Curculionidae, Scolytinae). Annals of the Entomological Society of America, 99, 189–194.
12. Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology, 89, 2623–2632.
13. Bleiker KP, Six DL (2007) Dietary benefits of fungal associates to an eruptive herbivore: potential implications of multiple associates on host population dynamics. Environmental Entomology, 36, 1384–1396.
14. Bleiker KP, Six DL (2009a) Competition and coexistence in a multi-partner mutualism: interactions between two fungal symbionts of the mountain pine beetle in beetle-attacked trees. Microbial Ecology, 57, 191–202.
15. Bleiker KP, Six DL (2009b) Effects of water potential and solute on the growth and interactions of two fungal symbionts of the mountain pine beetle. Mycological Research, 113, 3–15.
16. Boc A, Diallo Alpha B, Makarenkov V (2012) T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Research, 40, W573–W579.
17. Borchers HW (2016) Pracma: Practical numerical math functions. R package version 1.9.5. https://CRAN.R-project.org/package=pracma.
18. Campbell EM, Alfaro RI, Hawkes B (2007) Spatial distribution of mountain pine beetle outbreaks in relation to climate and stand characteristics: a dendroecological analysis. Journal of Integrative Plant Biology, 49, 168–178.
19. Cardinale BJ (2011) Biodiversity improves water quality through niche partitioning. Nature, 472, 86–89.
20. Chesson P (2000) Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics, 31, 343–366.
21. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674–3676.
22. Cook SP, Shirley BM, Zambino PJ (2010) Nitrogen concentration in mountain pine beetle larvae reflects nitrogen status of the tree host and two fungal associates. Environmental Entomology, 39, 821–826.
23. Coop G, Witonsky D, Di Rienzo A, Pritchard JK (2010) Using environmental correlations to identify loci underlying local adaptation. Genetics, 185, 1411–1423.
24. DiGuistini S, Ralph SG, Lim YW et al. (2007) Generation and annotation of lodgepole pine and oleoresin-induced expressed sequences from the blue-stain fungus Ophiostoma clavigerum, a mountain pine beetle-associated pathogen. FEMS Microbiology Letters, 267, 151–158.
25. DiGuistini S, Wang Y, Liao NY et al. (2011) Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen. Proceedings of the National Academy of Sciences of the United States of America, 108, 2504–2509.
26. Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annual Review of Entomology, 60, 17–34.
27. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620.
28. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567.
29. Feau N, Lauron-Moreau A, Piou D, Marçais B, Dutech C, Desprez-Loustau M-L (2012) Niche partitioning of the genetic lineages of the oak powdery mildew complex. Fungal Ecology, 5, 154–162.
30. Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecological Entomology, 36, 533–543.
31. Forester BR, Jones MR, Joost S, Landguth EL, Lasky JR (2016) Detecting spatial genetic signatures of local adaptation in heterogeneous landscapes. Molecular Ecology, 25, 104–120.
32. Frago E, Dicke M, Godfray HCJ (2012) Insect symbionts as hidden players in insect-plant interactions. Trends in Ecology and Evolution, 27, 705–711.
33. Gause GF (1934) The Struggle for Existence. Williams & Wilkins, Baltimore, Maryland. 192 p.
34. Godefroid M, Rasplus J-Y, Rossi J-P (2016) Is phylogeography helpful for invasive species risk assessment? The case study of the bark beetle genus Dendroctonus. Ecography, 39, 001–013.
35. Goodsman DW, Erbilgin N, Lieffers VJ (2012) The impact of phloem nutrients on overwintering mountain pine beetles and their fungal symbionts. Environmental Entomology, 41, 478–486.
36. Hijmans RJ (2016) raster: Geographic Data Analysis and Modeling. R package version 2.5-8. https://CRAN.R-project.org/package=raster.
37. James PMA, Coltman DW, Murray BW, Hamelin RC, Sperling FAH (2011) Spatial genetic structure of a symbiotic beetle-fungal system: toward multi-taxa integrated landscape genetics. PLoS One, 6, e25359.
38. Kamvar ZN, Brooks JC, Grünwald NJ (2015) Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Frontiers in Genetics, 6, 208.
39. Khadempour L, Massoumi Alamouti S, Hamelin R, Bohlmann J, Breuil C (2010) Target-specific PCR primers can detect and differentiate ophiostomatoid fungi from microbial communities associated with the mountain pine beetle Dendroctonus ponderosae. Fungal Biology, 114, 825–833.
40. Krokene P, Solheim H (1996) Fungal associates of five bark beetle species colonizing Norway spruce. Canadian Journal of Forest Research, 26, 2115–2122.
41. Kurz WA, Dymond CC, Stinson G et al. (2008) Mountain pine beetle and forest carbon feedback to climate change. Nature, 452, 987–990.
42. Lee S, Kim JJ, Breuil C (2006a) Diversity of fungi associated with the mountain pine beetle, Dendroctonus ponderosae and infested lodgepole pines in British Columbia. Fungal Diversity, 22, 91–105.
43. Lee S, Kim J, Breuil C (2006b) Pathogenicity of Leptographium longiclavatum associated with Dendroctonus ponderosae to Pinus contorta. Canadian Journal of Forest Research, 36, 2864–2872.
44. Legendre P, Lapointe F (2004) Assessing congruence among distance matrices: single-malt Scotch whiskies revisited. Australian and New Zealand Journal of Statistics, 46, 615–629.
45. MacArthur RH (1958) Population ecology of some warblers of northeastern coniferous forests. Ecology, 39, 599–619.
46. Maynard-Smith J, Smith NH, O'Rourke M, Spratt BG (1993) How clonal are bacteria? Proceedings of the National Academy of Sciences of the United States of America, 90, 4384–4388.
47. Moore ML, Six DL (2015) Effects of temperature on growth, sporulation, and competition of mountain pine beetle fungal symbionts. Microbial Ecology, 70, 336–347.
48. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583–590.
49. 2 and nitrogen fixation by an endosymbiotic spirochete of a termite-gut cellulolytic protist. Proceedings of the National Academy of Sciences of the United States of America, 112, 10224–10230.
50. Ojeda DI, Dhillon B, Tsui CKM, Hamelin RC (2013) Single-nucleotide polymorphism discovery in Leptographium longiclavatum, a mountain pine beetle-associated symbiotic fungus, using whole-genome resequencing. Molecular Ecology Resources, 14, 401–410.
51. Oksanen J, Blanchet FG, Friendly M et al. (2016) vegan: Community Ecology Package. R package version 2.4-1. https://CRAN.R-project.org/package=vegan.
52. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289–290.
53. Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295.
54. Pirondi A, Pérez-García A, Battistini G, Muzzi E, Brunelli A, Collina M (2015) Seasonal variations in the occurrence of Golovinomyces orontii and Podosphaera xanthii, causal agents of cucurbit powdery mildew in Northern Italy. Annals of Applied Biology, 167, 298–313.
55. Popa V, Deziel E, Lavallee R, Bauce E, Guertic C (2012) The complex symbiotic relationships of bark beetles with microorganisms: a potential practical approach for biological control in forestry. Pest Management Science, 68, 963–975.
56. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.
57. Raffa KF, Smalley EB (1995) Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle-fungal complexes. Oecologia, 102, 285–295.
58. Reid RW, Whitney HS, Watson JA (1967) Reactions of lodgepole pine to attack by Dendroctonus ponderosae Hopkins and blue stain fungi. Canadian Journal of Botany, 45, 1115–1126.
59. Rice AV, Langor DW (2009) Mountain pine beetle-associated blue-stain fungi in lodgepole × jack pine hybrids near Grande Prairie, Alberta (Canada). Forest Pathology, 39, 323–334.
60. Rice AV, Thormann MN, Langor DW (2008) Mountain pine beetle-associated blue-stain fungi are differentially adapted to boreal temperatures. Forest Pathology, 38, 113–123.
61. Roe AD, James P, Rice AV, Cooke JEK, Sperling FAH (2011a) Spatial community structure of mountain pine beetle fungal symbionts across a latitudinal gradient. Microbial Ecology, 62, 347–360.
62. Roe AD, Rice AV, Coltman DW, Cooke JEK, Sperling FAH (2011b) Comparative phylogeography, genetic differentiation and contrasting reproductive models in three fungal symbionts of a multipartite bark beetle symbiosis. Molecular Ecology, 20, 584–600.
63. Six DL (2003) A comparison of mycangial and phoretic fungi of individual mountain pine beetles. Canadian Journal of Forest Research, 33, 1331–1334.
64. Six DL (2012) Ecological and evolutionary determinants of bark beetles-fungus symbiosis. Insects, 3, 339–366.
65. Six DL (2013) The bark beetle holobiont: why microbes matter. Journal of Chemical Ecology, 39, 989–1002.
66. Six DL, Bentz BJ (2007) Temperature determines symbiont abundance in a multipartite bark beetle-fungus ectosymbiosis. Microbial Ecology, 54, 112–118.
67. Six DL, Paine T (1998) Effects of mycangial fungi and host tree species on progeny survival and emergence of Dendroctonus ponderosae (Coleoptera: Scolytidae). Environmental Entomology, 27, 1393–1401.
68. Six DL, Paine T (1999) Allozyme diversity and gene flow in Ophiostoma clavigerum (Ophiostomatales: Ophiostomataceae), the mycangial fungus of Jeffrey pine beetle. Dendroctonus jeffreyi (Coleoptera: Scolytidae). Canadian Journal of Forest Research, 29, 324–331.
69. Six DL, Wingfield MJ (2011) The role of phytopathogenicity in bark beetle–fungus symbioses: a challenge to the classic paradigm. Annual Review of Entomology, 56, 255–272.
70. Solheim H, Krokene P (1998) Growth and virulence of mountain pine beetle associated blue-stain fungi, Ophiostoma clavigerum and Ophiostoma montium. Canadian Journal of Botany, 76, 561–566.
71. Taylor DL, Hollingsworth TN, McFarland JK, Lennon NJ, Nusbaum C, Ruess RW (2014) A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitioning. Ecological Monographs, 84, 3–20.
72. Thorpe AS, Aschehoug ET, Atwater DZ, Callaway RM (2011) Interactions among plants and evolution. Journal of Ecology, 99, 729–740.
73. Tsui CK-M, Roe AD, El-kassaby YA et al. (2012) Population structure and migration pattern of a conifer pathogen, Grosmannia clavigera, as influenced by its symbiont, the mountain pine beetle. Molecular Ecology, 21, 71–86.
74. Tsui CK-M, DiGuistini S, Wang Y et al. (2013) Unequal recombination and evolution of the mating-type (MAT) Loci in the pathogenic fungus Grosmannia clavigera and relatives. G3: Genes Genomes Genetics, 3, 465–480.
75. Tsui CK-M, Farfan L, Roe AD et al. (2014) Population structure of mountain pine beetle symbiont Leptographium longiclavatum and the implication on the multipartite beetle-fungi relationships. PLoS One, 9, e105455.
76. st at two spatial scales. Heredity, 95, 466–475.
77. Wadke N, Kandasamy D, Vogel H et al. (2016) The bark-beetle-associated fungus, Endoconidiophora polonica, utilizes the phenolic defense compounds of its host as a carbon source. Plant Physiology, 171, 914–931.
78. Wang Y, Lim L, DiGuistini S et al. (2013) A specialized ABC efflux transporter GcABC-G1 confers monoterpene resistance to Grosmannia clavigera, a bark beetle-associated fungal pathogen of pine trees. New Phytologist, 197, 886–898.
79. Wang Y, Lim L, Madilao L, Lah L, Bohlmann J, Breuil C (2014) Gene discovery for enzymes involved in limonene modification or utilization by the mountain pine beetle-associated pathogen Grosmannia clavigera. Applied Environmental Microbiology, 80, 4566–4576.
80. Whitney HS, Farris SH (1970) Maxillary mycangium in the mountain pine beetle. Science, 167, 54–55.
81. Yamaoka Y, Swanson RH, Hiratsuka Y (1990) Inoculation of lodgepole pine with four blue-stain fungi associated with mountain pine beetle, monitored by a heat pulse velocity (HPV) instrument. Canadian Journal of Forest Research, 20, 31–31.
82. Yamaoka Y, Hiratsuka Y, Maruyama PJ (1995) The ability of Ophiostoma clavigerum to kill mature lodgepole-pine trees. European Journal of Forest Pathology, 25, 401–404.