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Phylogenomics clarifies repeated evolutionary origins of inbreeding and fungus farming in bark beetles (Curculionidae, Scolytinae)

Published on Oct 1, 2018in Molecular Phylogenetics and Evolution3.99
· DOI :10.1016/j.ympev.2018.05.028
Andrew J. Johnson2
Estimated H-index: 2
(UF: University of Florida),
Duane D. McKenna15
Estimated H-index: 15
(U of M: University of Memphis)
+ 5 AuthorsJiri Hulcr25
Estimated H-index: 25
(UF: University of Florida)
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Abstract
Abstract Bark and ambrosia beetles (Curculionidae, Scolytinae) display a conspicuous diversity of unusual genetic and ecological attributes and behaviors. Reconstructing the evolution of Scolytinae, particularly the large and ecologically significant tribe Cryphalini (pygmy borers), has long been problematic. These challenges have not adequately been addressed using morphological characters, and previous research has used only DNA sequence data from small numbers of genes. Through a combination of anchored hybrid enrichment, low-coverage draft genomes, and transcriptomes, we addressed these challenges by amassing a large molecular phylogenetic dataset for bark and ambrosia beetles. The resulting DNA sequence data from 251 protein coding genes (114,276 bp of nucleotide sequence data) support inference of the first robust phylogeny of Scolytinae, with a special focus on the species rich tribe Cryphalini and its close relatives. Key strategies, including inbreeding mating systems and fungus farming, evolved repeatedly across Scolytinae. We confirm 12 of 16 hypothesized origins of fungus farming, 6 of 8 origins of inbreeding polygyny and at least 11 independent origins of a super-generalist host range. These three innovations are statistically correlated, but their appearance within lineages was not necessarily simultaneous. Additionally, the evolution of extreme host plant generalism often preceded, rather than succeeded, fungus farming. Of the high-diversity tribes of Scolytinae, only Xyleborini is monophyletic, Corthylini is paraphyletic and Cryphalini is highly polyphyletic. Cryphalini sensu stricto is part of a clade containing the genera Hypothenemus , Cryphalus and Trypophloeus , and the tribe Xyloterini. Stegomerus and Cryptocarenus (Cryphalini) are part of a clade otherwise containing all Corthylini. Several other genera, including Ernoporus and Scolytogenes (Cryphalini), make up a distantly related clade. Several of the genera of Cryphalini are also intermixed. For example, Cryphalus and Hypocryphalus are intermingled, as well as Ernoporicus , Ptilopodius and Scolytogenes . Our data are consistent with widespread polyphyly and paraphyly across Scolytinae and within Cryphalini, and provides new insights into the evolution of inbreeding mating systems and fungus farming in the species rich and ecologically significant weevil subfamily Scolytinae.
  • References (68)
  • Citations (5)
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References68
Newest
Published on Oct 1, 2018in Microbial Ecology3.61
James Skelton7
Estimated H-index: 7
(UF: University of Florida),
Michelle A. Jusino5
Estimated H-index: 5
+ 5 AuthorsJiri Hulcr25
Estimated H-index: 25
(UF: University of Florida)
Separating symbioses from incidental associations is a major obstacle in symbiosis research. In this survey of fungi associated with Asian bark and ambrosia beetles, we used quantitative culture and DNA barcode identification to characterize fungal communities associated with co-infesting beetle species in pines (Pinus) of China and Vietnam. To quantitatively discern likely symbioses from coincidental associations, we used multivariate analysis and multilevel pattern analysis (a type of indicato...
Published on Apr 1, 2018in Molecular Biology and Evolution14.80
Seunggwan Shin6
Estimated H-index: 6
(U of M: University of Memphis),
Dave J. Clarke3
Estimated H-index: 3
(U of M: University of Memphis)
+ 7 AuthorsDuane D. McKenna15
Estimated H-index: 15
(U of M: University of Memphis)
Published on Apr 1, 2018in Systematic Entomology3.73
Dario Pistone2
Estimated H-index: 2
(University of Bergen),
Jostein Gohli5
Estimated H-index: 5
(University of Bergen),
Bjarte H. Jordal21
Estimated H-index: 21
(University of Bergen)
The Scolytinae phylogeny was reconstructed using a large molecular dataset consisting of 182 species and 18 gene fragments totalling more than 10 kb of nucleotides. The phylogenetic resolution at deeper nodes increased only moderately; 15 tribes were monophyletic, whereas the remaining ones (11) were para‐ or polyphyletic. Recent relationships showed higher resolution and had stronger support. A revision of Scolytinae is clearly required. The use of additional molecular data and morphological ch...
Published on Feb 1, 2018in Current opinion in insect science3.78
Duane D. McKenna15
Estimated H-index: 15
(U of M: University of Memphis)
The order Coleoptera (beetles) is arguably the most species-rich lineage of animals. Beetles exhibit an extraordinary variety of life histories and occupy most terrestrial environments. Whole genome sequences are available for 11 beetle species, only six of which have been published. Studies of beetle genomes have revealed remarkable new insights into the genomic basis and evolution of beetle life histories and other aspects of beetle biodiversity, including the genes underlying chemoperception,...
Published on Jan 1, 2018in Systematic Entomology3.73
Stephanie Haddad4
Estimated H-index: 4
(U of M: University of Memphis),
Seunggwan Shin6
Estimated H-index: 6
(U of M: University of Memphis)
+ 6 AuthorsDuane D. McKenna15
Estimated H-index: 15
(U of M: University of Memphis)
Cerambycidae is a species-rich family of mostly wood-feeding (xylophagous) beetles containing nearly 35 000 known species. The higher-level phylogeny of Cerambycidae has never been robustly reconstructed using molecular phylogenetic data or a comprehensive sample of higher taxa, and its internal relationships and evolutionary history remain the subjects of ongoing debate. We reconstructed the higher-level phylogeny of Cerambycidae using phylogenomic data from 522 single copy nuclear genes, gener...
Published on Dec 1, 2017in Ecology and Evolution2.42
Caroline Storer4
Estimated H-index: 4
(UF: University of Florida),
Adam C. Payton5
Estimated H-index: 5
(UF: University of Florida)
+ 2 AuthorsJiri Hulcr25
Estimated H-index: 25
(UF: University of Florida)
Each year new exotic species are transported across the world through global commerce, causing considerable economic and ecological damage. An important component of managing invasion pathways is to identify source populations. Some of the most widespread exotic species are haplodiploid ambrosia beetles. The ability to mate with siblings (inbreed) and their transportable food source (symbiotic fungus) have enabled them to colonize most of the world and become pests of plant nurseries, lumber, an...
Published on May 1, 2017in Evolution3.57
Jostein Gohli5
Estimated H-index: 5
(University of Bergen),
Lawrence R. Kirkendall21
Estimated H-index: 21
(University of Bergen)
+ 3 AuthorsBjarte H. Jordal21
Estimated H-index: 21
(University of Bergen)
The study of species diversification can identify the processes that shape patterns of species richness across the tree of life. Here we perform comparative analyses of species diversification using a large dataset of bark beetles. Three examined covariates – permanent inbreeding (sibling mating), fungus farming, and major host type – represent a range of factors that may be important for speciation. We studied the association of these covariates with species diversification while controlling fo...
Published on Jan 31, 2017in Annual Review of Entomology11.80
Jiri Hulcr25
Estimated H-index: 25
,
Lukasz L. Stelinski36
Estimated H-index: 36
The ambrosia beetle–fungus farming symbiosis is more heterogeneous than previously thought. There is not one but many ambrosia symbioses. Beetle-fungus specificity is clade dependent and ranges from strict to promiscuous. Each new origin has evolved a new mycangium. The most common relationship with host trees is colonization of freshly dead tissues, but there are also parasites of living trees, vectors of pathogenic fungi, and beetles living in rotten trees with a wood-decay symbiont. Most of t...
Published on Jan 12, 2017in Molecular Biology and Evolution14.80
Dan L. Warren17
Estimated H-index: 17
(Macquarie University),
Anthony J. Geneva11
Estimated H-index: 11
(Harvard University),
Robert Lanfear29
Estimated H-index: 29
(Macquarie University)
Bayesian inference using Markov chain Monte Carlo (MCMC) has become one of the primary methods used to infer phylogenies from sequence data. Assessing convergence is a crucial component of these analyses, as it establishes the reliability of the posterior distribution estimates of the tree topology and model parameters sampled from the MCMC. Numerous tests and visualizations have been developed for this purpose, but many of the most popular methods are implemented in ways that make them inconven...
Published on Nov 29, 2016in Zootaxa0.99
Andrew J. Johnson2
Estimated H-index: 2
(UF: University of Florida),
Thomas H. Atkinson4
Estimated H-index: 4
(University of Texas at Austin),
Jiri Hulcr25
Estimated H-index: 25
(UF: University of Florida)
Two new Hypothenemus species found in southern and southeastern USA are described: Hypothenemus piaparolinae sp. n. and Hypothenemus subterrestris sp. n. The distribution and habits suggest these species are native and widely distributed, but elusive, and not recently arrived exotics. Both appear to have unusual biology: H. subterrestris appears to live in material on or in the ground, and H. piaparolinae has only been collected from the xylem of extensively rotten, fungus-filled twigs.
Cited By5
Newest
Published on Jun 21, 2019in Coleopterists Bulletin0.70
Michail Yu Mandelshtam1
Estimated H-index: 1
,
Alexander V. Petrov2
Estimated H-index: 2
+ 1 AuthorsAnthony I. Cognato22
Estimated H-index: 22
(MSU: Michigan State University)
Xyleborine ambrosia beetles bore galleries into wood to cultivate symbiotic fungi for larval and adult food. This habit and their haplodiploid mating system have contributed to their diversification in forest habitats throughout the world. There are ∼1,200 species divided in 37 genera that have been recently revised in a phylogenetic framework. To continue to equate genera with monophyletic groups, we investigated the validity of Heteroborips Reitter, 1913, a genus first erected for the Palearct...
Published on Dec 22, 2018in Life
Jazmín Blaz , Josué Barrera-Redondo2
Estimated H-index: 2
+ 11 AuthorsAlexandro Alonso-Sánchez2
Estimated H-index: 2
Mutualistic symbiosis and eusociality have developed through gradual evolutionary processes at different times in specific lineages. Like some species of termites and ants, ambrosia beetles have independently evolved a mutualistic nutritional symbiosis with fungi, which has been associated with the evolution of complex social behaviors in some members of this group. We sequenced the transcriptomes of two ambrosia complexes (Euwallacea sp. near fornicatus–Fusarium euwallaceae and Xyleborus glabra...
Published on Dec 20, 2018in Diversity
Dave J. Clarke3
Estimated H-index: 3
,
Ajay Limaye1
Estimated H-index: 1
+ 1 AuthorsRolf G. Oberprieler11
Estimated H-index: 11
Only a few weevils have been described from Burmese amber, and although most have been misclassified, they show unusual and specialised characters unknown in extant weevils. In this paper, we present the results of a study of a much larger and more diverse selection of Burmese amber weevils. We prepared all amber blocks to maximise visibility of structures and examined these with high-magnification light microscopy as well as CT scanning (selected specimens). We redescribe most previously descri...
Published on Sep 1, 2018in Journal of Insect Science1.45
You Li3
Estimated H-index: 3
(UF: University of Florida),
Yong‐Ying Ruan1
Estimated H-index: 1
(SZPT: Shenzhen Polytechnic)
+ 5 AuthorsJiri Hulcr25
Estimated H-index: 25
(UF: University of Florida)
Published on Jul 18, 2018in Diversity
Duane D. McKenna15
Estimated H-index: 15
(U of M: University of Memphis),
Duane D. McKenna3
Estimated H-index: 3
(U of M: University of Memphis)
+ 22 AuthorsBruno Augusto Souza de Medeiros3
Estimated H-index: 3
(Harvard University)
The 2016 International Weevil Meeting was held immediately after the International Congress of Entomology (ICE). It built on the topics and content of the 2016 ICE weevil symposium Phylogeny and Evolution of Weevils (Coleoptera: Curculionoidea): A Symposium in Honor of Dr. Guillermo "Willy” Kuschel. Beyond catalyzing research and collaboration, the meeting was intended to serve as a forum for identifying priorities and goals for those who study weevils. The meeting consisted of 46 invited and co...
View next paperGenetics of Bark Beetles and Associated Microorganisms: Third Workshop Proceedings