An inordinate fondness for Fusarium: Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts

Matthew T. Kasson, Kerry O'Donnell, Alejandro P. Rooney, Stacy Sink, Randy C. Ploetz, Jill N. Ploetz, Joshua L. Konkol, Daniel Carrillo, Stanley Freeman, Zvi Mendel, Jason A. Smith, Adam W. Black, Jiri Hulcr, Craig Bateman, Kristyna Stefkova, Paul R. Campbell, Andrew D.W. Geering, Elizabeth K. Dann, Akif Eskalen, Keerthi MohottiDylan P.G. Short, Takayuki Aoki, Kristi A. Fenstermacher, Donald D. Davis, David M. Geiser

Research output: Contribution to journalArticle

76 Citations (Scopus)

Abstract

Ambrosia beetle fungiculture represents one of the most ecologically and evolutionarily successful symbioses, as evidenced by the 11 independent origins and 3500 species of ambrosia beetles. Here we document the evolution of a clade within Fusarium associated with ambrosia beetles in the genus Euwallacea (Coleoptera: Scolytinae). Ambrosia Fusarium Clade (AFC) symbionts are unusual in that some are plant pathogens that cause significant damage in naïve natural and cultivated ecosystems, and currently threaten avocado production in the United States, Israel and Australia. Most AFC fusaria produce unusual clavate macroconidia that serve as a putative food source for their insect mutualists. AFC symbionts were abundant in the heads of four Euwallacea spp., which suggests that they are transported within and from the natal gallery in mandibular mycangia. In a four-locus phylogenetic analysis, the AFC was resolved in a strongly supported monophyletic group within the previously described Clade 3 of the Fusarium solani species complex (FSSC). Divergence-time estimates place the origin of the AFC in the early Miocene ~21.2. Mya, which coincides with the hypothesized adaptive radiation of the Xyleborini. Two strongly supported clades within the AFC (Clades A and B) were identified that include nine species lineages associated with ambrosia beetles, eight with Euwallacea spp. and one reportedly with Xyleborus ferrugineus, and two lineages with no known beetle association. More derived lineages within the AFC showed fixation of the clavate (club-shaped) macroconidial trait, while basal lineages showed a mix of clavate and more typical fusiform macroconidia. AFC lineages consisted mostly of genetically identical individuals associated with specific insect hosts in defined geographic locations, with at least three interspecific hybridization events inferred based on discordant placement in individual gene genealogies and detection of recombinant loci. Overall, these data are consistent with a strong evolutionary trend toward obligate symbiosis coupled with secondary contact and interspecific hybridization.

Original languageEnglish (US)
Pages (from-to)147-157
Number of pages11
JournalFungal Genetics and Biology
Volume56
DOIs
StatePublished - Jul 1 2013

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Persea
Ambrosia
Beetles
Fusarium
Symbiosis
Insects
Mya
Genealogy and Heraldry
Geographic Locations
Israel
Ecosystem

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Genetics

Cite this

Kasson, Matthew T. ; O'Donnell, Kerry ; Rooney, Alejandro P. ; Sink, Stacy ; Ploetz, Randy C. ; Ploetz, Jill N. ; Konkol, Joshua L. ; Carrillo, Daniel ; Freeman, Stanley ; Mendel, Zvi ; Smith, Jason A. ; Black, Adam W. ; Hulcr, Jiri ; Bateman, Craig ; Stefkova, Kristyna ; Campbell, Paul R. ; Geering, Andrew D.W. ; Dann, Elizabeth K. ; Eskalen, Akif ; Mohotti, Keerthi ; Short, Dylan P.G. ; Aoki, Takayuki ; Fenstermacher, Kristi A. ; Davis, Donald D. ; Geiser, David M. / An inordinate fondness for Fusarium : Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts. In: Fungal Genetics and Biology. 2013 ; Vol. 56. pp. 147-157.
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abstract = "Ambrosia beetle fungiculture represents one of the most ecologically and evolutionarily successful symbioses, as evidenced by the 11 independent origins and 3500 species of ambrosia beetles. Here we document the evolution of a clade within Fusarium associated with ambrosia beetles in the genus Euwallacea (Coleoptera: Scolytinae). Ambrosia Fusarium Clade (AFC) symbionts are unusual in that some are plant pathogens that cause significant damage in na{\"i}ve natural and cultivated ecosystems, and currently threaten avocado production in the United States, Israel and Australia. Most AFC fusaria produce unusual clavate macroconidia that serve as a putative food source for their insect mutualists. AFC symbionts were abundant in the heads of four Euwallacea spp., which suggests that they are transported within and from the natal gallery in mandibular mycangia. In a four-locus phylogenetic analysis, the AFC was resolved in a strongly supported monophyletic group within the previously described Clade 3 of the Fusarium solani species complex (FSSC). Divergence-time estimates place the origin of the AFC in the early Miocene ~21.2. Mya, which coincides with the hypothesized adaptive radiation of the Xyleborini. Two strongly supported clades within the AFC (Clades A and B) were identified that include nine species lineages associated with ambrosia beetles, eight with Euwallacea spp. and one reportedly with Xyleborus ferrugineus, and two lineages with no known beetle association. More derived lineages within the AFC showed fixation of the clavate (club-shaped) macroconidial trait, while basal lineages showed a mix of clavate and more typical fusiform macroconidia. AFC lineages consisted mostly of genetically identical individuals associated with specific insect hosts in defined geographic locations, with at least three interspecific hybridization events inferred based on discordant placement in individual gene genealogies and detection of recombinant loci. Overall, these data are consistent with a strong evolutionary trend toward obligate symbiosis coupled with secondary contact and interspecific hybridization.",
author = "Kasson, {Matthew T.} and Kerry O'Donnell and Rooney, {Alejandro P.} and Stacy Sink and Ploetz, {Randy C.} and Ploetz, {Jill N.} and Konkol, {Joshua L.} and Daniel Carrillo and Stanley Freeman and Zvi Mendel and Smith, {Jason A.} and Black, {Adam W.} and Jiri Hulcr and Craig Bateman and Kristyna Stefkova and Campbell, {Paul R.} and Geering, {Andrew D.W.} and Dann, {Elizabeth K.} and Akif Eskalen and Keerthi Mohotti and Short, {Dylan P.G.} and Takayuki Aoki and Fenstermacher, {Kristi A.} and Davis, {Donald D.} and Geiser, {David M.}",
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Kasson, MT, O'Donnell, K, Rooney, AP, Sink, S, Ploetz, RC, Ploetz, JN, Konkol, JL, Carrillo, D, Freeman, S, Mendel, Z, Smith, JA, Black, AW, Hulcr, J, Bateman, C, Stefkova, K, Campbell, PR, Geering, ADW, Dann, EK, Eskalen, A, Mohotti, K, Short, DPG, Aoki, T, Fenstermacher, KA, Davis, DD & Geiser, DM 2013, 'An inordinate fondness for Fusarium: Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts', Fungal Genetics and Biology, vol. 56, pp. 147-157. https://doi.org/10.1016/j.fgb.2013.04.004

An inordinate fondness for Fusarium : Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts. / Kasson, Matthew T.; O'Donnell, Kerry; Rooney, Alejandro P.; Sink, Stacy; Ploetz, Randy C.; Ploetz, Jill N.; Konkol, Joshua L.; Carrillo, Daniel; Freeman, Stanley; Mendel, Zvi; Smith, Jason A.; Black, Adam W.; Hulcr, Jiri; Bateman, Craig; Stefkova, Kristyna; Campbell, Paul R.; Geering, Andrew D.W.; Dann, Elizabeth K.; Eskalen, Akif; Mohotti, Keerthi; Short, Dylan P.G.; Aoki, Takayuki; Fenstermacher, Kristi A.; Davis, Donald D.; Geiser, David M.

In: Fungal Genetics and Biology, Vol. 56, 01.07.2013, p. 147-157.

Research output: Contribution to journalArticle

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T1 - An inordinate fondness for Fusarium

T2 - Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts

AU - Kasson, Matthew T.

AU - O'Donnell, Kerry

AU - Rooney, Alejandro P.

AU - Sink, Stacy

AU - Ploetz, Randy C.

AU - Ploetz, Jill N.

AU - Konkol, Joshua L.

AU - Carrillo, Daniel

AU - Freeman, Stanley

AU - Mendel, Zvi

AU - Smith, Jason A.

AU - Black, Adam W.

AU - Hulcr, Jiri

AU - Bateman, Craig

AU - Stefkova, Kristyna

AU - Campbell, Paul R.

AU - Geering, Andrew D.W.

AU - Dann, Elizabeth K.

AU - Eskalen, Akif

AU - Mohotti, Keerthi

AU - Short, Dylan P.G.

AU - Aoki, Takayuki

AU - Fenstermacher, Kristi A.

AU - Davis, Donald D.

AU - Geiser, David M.

PY - 2013/7/1

Y1 - 2013/7/1

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