Genome-scale data reveal the role of hybridization in lichen-forming fungi.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
30 01 2020
30 01 2020
Historique:
received:
17
07
2019
accepted:
19
12
2019
entrez:
1
2
2020
pubmed:
1
2
2020
medline:
18
11
2020
Statut:
epublish
Résumé
Advancements in molecular genetics have revealed that hybridization may be common among plants, animals, and fungi, playing a role in evolutionary dynamics and speciation. While hybridization has been well-documented in pathogenic fungi, the effects of these processes on speciation in fungal lineages with different life histories and ecological niches are largely unexplored. Here we investigated the potential influence of hybridization on the emergence of morphologically and reproductively distinct asexual lichens. We focused on vagrant forms (growing obligately unattached to substrates) within a clade of rock-dwelling, sexually reproducing species in the Rhizoplaca melanophthalma (Lecanoraceae, Ascomycota) species complex. We used phylogenomic data from both mitochondrial and nuclear genomes to infer evolutionary relationships and potential patterns of introgression. We observed multiple instances of discordance between the mitochondrial and nuclear trees, including the clade comprising the asexual vagrant species R. arbuscula, R. haydenii, R. idahoensis, and a closely related rock-dwelling lineage. Despite well-supported phylogenies, we recovered strong evidence of a reticulated evolutionary history using a network approach that incorporates both incomplete lineage sorting and hybridization. These data suggest that the rock-dwelling western North American subalpine endemic R. shushanii is potentially the result of a hybrid speciation event, and introgression may have also played a role in other taxa, including vagrant species R. arbuscula, R. haydenii and R. idahoensis. We discuss the potential roles of hybridization in terms of generating asexuality and novel morphological traits in lichens. Furthermore, our results highlight the need for additional study of reticulate phylogenies when investigating species boundaries and evolutionary history, even in cases with well-supported topologies inferred from genome-scale data.
Identifiants
pubmed: 32001749
doi: 10.1038/s41598-020-58279-x
pii: 10.1038/s41598-020-58279-x
pmc: PMC6992703
doi:
Substances chimiques
DNA, Fungal
0
DNA, Mitochondrial
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1497Références
Chan, K. M. A. & Levin, S. A. Leaky prezygotic isolation and porous genomes: Rapid introgression of maternally inherited DNA. Evolution 59, 720–729 (2005).
doi: 10.1111/j.0014-3820.2005.tb01748.x
Mallet, J. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237, https://doi.org/10.1016/j.tree.2005.02.010 (2005).
doi: 10.1016/j.tree.2005.02.010
pubmed: 16701374
Stukenbrock, E. H. The Role of Hybridization in the Evolution and Emergence of New Fungal Plant Pathogens. Phytopathology 106, 104–112, https://doi.org/10.1094/phyto-08-15-0184-rvw (2016).
doi: 10.1094/phyto-08-15-0184-rvw
pubmed: 26824768
Hedrick, P. W. Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol. Ecol. 22, 4606–4618, https://doi.org/10.1111/mec.12415 (2013).
doi: 10.1111/mec.12415
pubmed: 23906376
Hill, G. E. The mitonuclear compatibility species concept. Auk 134, 393–409, https://doi.org/10.1642/auk-16-201.1 (2017).
doi: 10.1642/auk-16-201.1
Huang, J. P. Parapatric genetic introgression and phenotypic assimilation: testing conditions for introgression between Hercules beetles (Dynastes, Dynastinae). Mol. Ecol. 25, 5513–5526, https://doi.org/10.1111/mec.13849 (2016).
doi: 10.1111/mec.13849
pubmed: 27661063
Feliner, G. N. et al. Is homoploid hybrid speciation that rare? An empiricist’s view. Heredity 118, 513–516, https://doi.org/10.1038/hdy.2017.7 (2017).
doi: 10.1038/hdy.2017.7
Schumer, M., Rosenthal, G. G. & Andolfatto, P. How common is homoploid hybrid speciation? Evolution 68, 1553–1560, https://doi.org/10.1111/evo.12399 (2014).
doi: 10.1111/evo.12399
pubmed: 24620775
Abbott, R. et al. Hybridization and speciation. J. Evolut. Biol. 26, 229–246, https://doi.org/10.1111/j.1420-9101.2012.02599.x (2013).
doi: 10.1111/j.1420-9101.2012.02599.x
Chapman, M. A. & Burke, J. M. Genetic divergence and hybrid speciation. Evolution 61, 1773–1780, https://doi.org/10.1111/j.1558-5646.2007.00134.x (2007).
doi: 10.1111/j.1558-5646.2007.00134.x
pubmed: 17598755
Tigano, A. & Friesen, V. L. Genomics of local adaptation with gene flow. Mol. Ecol. 25, 2144–2164, https://doi.org/10.1111/mec.13606 (2016).
doi: 10.1111/mec.13606
pubmed: 26946320
Rieseberg, L. H. et al. Major ecological transitions in wild sunflowers facilitated by hybridization. Sci. 301, 1211–1216, https://doi.org/10.1126/science.1086949 (2003).
doi: 10.1126/science.1086949
Gladieux, P. et al. Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes. Mol. Ecol. 23, 753–773, https://doi.org/10.1111/mec.12631 (2014).
doi: 10.1111/mec.12631
pubmed: 24341913
Dasmahapatra, K. K. et al. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nat. 487, 94–98, https://doi.org/10.1038/nature11041 (2012).
doi: 10.1038/nature11041
Lamichhaney, S. et al. Rapid hybrid speciation in Darwin’s finches. Sci. 359, 224–227, https://doi.org/10.1126/science.aao4593 (2018).
doi: 10.1126/science.aao4593
Stankowski, S. & Streisfeld, M. A. Introgressive hybridization facilitates adaptive divergence in a recent radiation of monkeyflowers. Proc Biol Sci 282, https://doi.org/10.1098/rspb.2015.1666 (2015).
doi: 10.1098/rspb.2015.1666
Fishman, L. & Sweigart, A. L. When Two Rights Make a Wrong: The Evolutionary Genetics of Plant Hybrid Incompatibilities, Vol. 69 Annual Review of Plant Biology (ed S. S. Merchant) 707–731 (2018).
Mack, K. L. & Nachman, M. W. Gene regulation and speciation. Trends Genet. 33, 68–80, https://doi.org/10.1016/j.tig.2016.11.003 (2017).
doi: 10.1016/j.tig.2016.11.003
pubmed: 27914620
Bonnet, T., Leblois, R., Rousset, F. & Crochet, P. A. A reassessment of explanations for discordant introgressions of mitochondrial and nuclear genomes. Evolution 71, 2140–2158, https://doi.org/10.1111/evo.13296 (2017).
doi: 10.1111/evo.13296
pubmed: 28703292
Burton, R. S. & Barreto, F. S. A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities? Mol. Ecol. 21, 4942–4957, https://doi.org/10.1111/mec.12006 (2012).
doi: 10.1111/mec.12006
pubmed: 22994153
Lee, H. Y. et al. Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135, 1065–1073, https://doi.org/10.1016/j.cell.2008.10.047 (2008).
doi: 10.1016/j.cell.2008.10.047
pubmed: 19070577
Sloan, D. B., Havird, J. C. & Sharbrough, J. The on-again, off-again relationship between mitochondrial genomes and species boundaries. Mol. Ecol. 26, 2212–2236, https://doi.org/10.1111/mec.13959 (2017).
doi: 10.1111/mec.13959
pubmed: 27997046
pmcid: 6534505
Toews, D. P. & Brelsford, A. The biogeography of mitochondrial and nuclear discordance in animals. Mol. Ecol. 21, 3907–3930, https://doi.org/10.1111/j.1365-294X.2012.05664.x (2012).
doi: 10.1111/j.1365-294X.2012.05664.x
pubmed: 22738314
Ivanov, V., Lee, K. M. & Mutanen, M. Mitonuclear discordance in wolf spiders: Genomic evidence for species integrity and introgression. Mol. Ecol. 27, 1681–1695, https://doi.org/10.1111/mec.14564 (2018).
doi: 10.1111/mec.14564
pubmed: 29575366
Giordano, L., Sillo, F., Garbelotto, M. & Gonthier, P. Mitonuclear interactions may contribute to fitness of fungal hybrids. Sci. Rep. 8, 1706, https://doi.org/10.1038/s41598-018-19922-w (2018).
doi: 10.1038/s41598-018-19922-w
pubmed: 29374209
pmcid: 5786003
Greig, D., Louis, E. J., Borts, R. H. & Travisano, M. Hybrid speciation in experimental populations of yeast. Sci. 298, 1773–1775, https://doi.org/10.1126/science.1076374 (2002).
doi: 10.1126/science.1076374
Anderson, J. B. et al. Mode of selection and experimental evolution of antifungal drug resistance in Saccharomyces cerevisiae. Genet. 163, 1287–1298 (2003).
Stukenbrock, E. H., Christiansen, F. B., Hansen, T. T., Dutheil, J. Y. & Schierup, M. H. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. Proc. Natl Acad. Sci. USA 109, 10954–10959, https://doi.org/10.1073/pnas.1201403109 (2012).
doi: 10.1073/pnas.1201403109
pubmed: 22711811
Greenspan, S. E. et al. Hybrids of amphibian chytrid show high virulence in native hosts. Sci. Rep. 8, 9600, https://doi.org/10.1038/s41598-018-27828-w (2018).
doi: 10.1038/s41598-018-27828-w
pubmed: 29941894
pmcid: 6018099
Silva, D. N., Varzea, V., Paulo, O. S. & Batista, D. Population genomic footprints of host adaptation, introgression and recombination in coffee leaf rust. Mol. Plant. Pathol. 19, 1742–1753, https://doi.org/10.1111/mpp.12657 (2018).
doi: 10.1111/mpp.12657
pubmed: 29328532
pmcid: 6638104
Anderson, E. & Rudolph, E. D. An analysis of variation in a variable population of Cladonia. Evolution 10, 147–156 (1956).
doi: 10.1111/j.1558-5646.1956.tb02841.x
Culberson, C. F., Culberson, W. L. & Johnson, A. Gene Flow in Lichens. Am. J. Botany 75, 1135–1139 (1988).
doi: 10.1002/j.1537-2197.1988.tb08826.x
O’Brien, H., Miadlikowska, J. & Lutzoni, F. Assessing Reproductive Isolation in Highly Diverse Communities of the Lichen-Forming Fungal Genus Peltigera. Evolution 63, 2076–2086 (2009).
doi: 10.1111/j.1558-5646.2009.00685.x
Zoller, S., Lutzoni, F. & Scheidegger, C. Genet. Var. Popul. threatened lichen Lobaria pulmonaria Switz. Implic. its conservation. 8, 2049–2059 (1999).
Magain, N., Sérusiaux, E., Zhurbenko, M. P., Lutzoni, F. & Miadlikowska, J. Disentangling the Peltigera polydactylon Species Complex by Recognizing Two New Taxa, P. polydactylon subsp. udeghe and P. seneca. Herzogia 29, 514–528, https://doi.org/10.13158/heia.29.2.2016.514 (2016).
doi: 10.13158/heia.29.2.2016.514
Steenkamp, E. T., Wingfield, M. J., McTaggart, A. R. & Wingfield, B. D. Fungal species and their boundaries matter - Definitions, mechanisms and practical implications. Fungal Biol. Rev. 32, 104–116, https://doi.org/10.1016/j.fbr.2017.11.002 (2018).
doi: 10.1016/j.fbr.2017.11.002
Prieto, M. & Wedin, M. Dating the diversification of the major lineages of Ascomycota (Fungi). Plos One 8, https://doi.org/10.1371/journal.pone.0065576 (2013).
doi: 10.1371/journal.pone.0065576
Lucking, R., Huhndorf, S., Pfister, D. H., Plata, E. R. & Lumbsch, H. T. Fungi evolved right on track. Mycologia 101, 810–822, https://doi.org/10.3852/09-016 (2009).
doi: 10.3852/09-016
pubmed: 19927746
Lumbsch, H. T. & Leavitt, S. D. Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi. Fungal Diversity 50, 59–72, https://doi.org/10.1007/s13225-011-0123-z (2011).
doi: 10.1007/s13225-011-0123-z
Culberson, C. F. & Hale, M. E. Chemical and morphological evolution in Parmelia sect. Hypotrachyna: Product of ancient hybridization? Brittonia 25, 162–173, https://doi.org/10.2307/2805934 (1973).
doi: 10.2307/2805934
Ertz, D. et al. Towards a new classification of the Arthoniales (Ascomycota) based on a three-gene phylogeny focussing on the genus Opegrapha. Mycol. Res. 113, 141–152, https://doi.org/10.1016/j.mycres.2008.09.002 (2009).
doi: 10.1016/j.mycres.2008.09.002
pubmed: 18929650
Ekman, S. & Fröberg, L. Taxonomical problems in Aspicilia contorta and A. hoffmannii - an effect of hybridization? Int. J. Mycology Lichenology 3, 215–226 (1988).
Widhelm, T. J. et al. Multiple historical processes obscure phylogenetic relationships in a taxonomically difficult group (Lobariaceae, Ascomycota). Sci. Rep. 9, 8968, https://doi.org/10.1038/s41598-019-45455-x (2019).
doi: 10.1038/s41598-019-45455-x
pubmed: 31222061
pmcid: 6586878
Tripp, E. A. & Lendemer, J. C. Twenty-seven modes of reproduction in the obligate lichen symbiosis. Brittonia 70, 1–14, https://doi.org/10.1007/s12228-017-9500-6 (2017).
doi: 10.1007/s12228-017-9500-6
Murtagh, G. J., Dyer, P. S. & Crittenden, P. D. Reproductive systems: Sex and the single lichen. Nat. 404, 564 (2000).
doi: 10.1038/35007142
Billiard, S., Lopez-Villavicencio, M., Hood, M. E. & Giraud, T. Sex, outcrossing and mating types: unsolved questions in fungi and beyond. J. Evol. Biol. 25, 1020–1038, https://doi.org/10.1111/j.1420-9101.2012.02495.x (2012).
doi: 10.1111/j.1420-9101.2012.02495.x
pubmed: 22515640
Taylor, J. W., Jacobson, D. J. & Fisher, M. C. The Evolution of Asexual Fungi: Reproduction, Speciation and Classification. Annu. Rev. Phytopathol. 37, 197–246 (1999).
doi: 10.1146/annurev.phyto.37.1.197
Wilson, A. M. et al. Homothallism: an umbrella term for describing diverse sexual behaviours. IMA Fungus 6, 207–214, https://doi.org/10.5598/imafungus.2015.06.01.13 (2015).
doi: 10.5598/imafungus.2015.06.01.13
pubmed: 26203424
pmcid: 4500084
Schardl, C. L. & Craven, K. D. Interspecific hybridization in plant-associated fungi and oomycetes: a review. Mol. Ecol. 12, 2861–2873, https://doi.org/10.1046/j.1365-294X.2003.01965.x (2003).
doi: 10.1046/j.1365-294X.2003.01965.x
pubmed: 14629368
Leavitt, S. et al. DNA barcode identification of lichen-forming fungal species in the Rhizoplaca melanophthalma species-complex (Lecanorales, Lecanoraceae), including five new species. MycoKeys 7, 1–22, https://doi.org/10.3897/mycokeys.7.4508 (2013).
doi: 10.3897/mycokeys.7.4508
Leavitt, S. D. et al. Complex patterns of speciation in cosmopolitan “rock posy” lichens–discovering and delimiting cryptic fungal species in the lichen-forming Rhizoplaca melanophthalma species-complex (Lecanoraceae, Ascomycota). Mol. Phylogenet Evol. 59, 587–602, https://doi.org/10.1016/j.ympev.2011.03.020 (2011).
doi: 10.1016/j.ympev.2011.03.020
pubmed: 21443956
Leavitt, S. D. et al. Local representation of global diversity in a cosmopolitan lichen-forming fungal species complex (Rhizoplaca, Ascomycota). J. Biogeography 40, 1792–1806, https://doi.org/10.1111/jbi.12118 (2013).
doi: 10.1111/jbi.12118
Rosentreter, R. Vagrant Lichens in North America. Bryologist 96, 333–338 (1993).
doi: 10.2307/3243861
Feurtey, A. & Stukenbrock, E. H. Interspecific Gene Exchange as a Driver of Adaptive Evolution in Fungi. Annu. Rev. Microbiol. 72, 377–398, https://doi.org/10.1146/annurev-micro-090817-062753 (2018).
doi: 10.1146/annurev-micro-090817-062753
pubmed: 29927707
Leavitt, S. D. et al. Resolving evolutionary relationships in lichen-forming fungi using diverse phylogenomic datasets and analytical approaches. Sci. Rep. 6, 22262, https://doi.org/10.1038/srep22262 (2016).
doi: 10.1038/srep22262
pubmed: 26915968
pmcid: 4768097
Leavitt, S. D. et al. DNA barcode Identif. lichen-forming fungal species Rhizoplaca melanophthalma species-complex, including five N. species MycoKeys 7, 1–22, https://doi.org/10.3897/mycokeys.7.4508 (2013).
doi: 10.3897/mycokeys.7.4508
Leavitt, D. H., Keuler, R., Newberry, C. C., Rosentreter, R. & St. Clair, L. Shotgun sequencing decades-old lichen specimens to resolve phylogenomic placement of type specimens. Plant and Fungal Systematics 64, 237–247, https://doi.org/10.2478/pfs-2019-0020 (2019).
doi: 10.2478/pfs-2019-0020
Grewe, F., Huang, J. P., Leavitt, S. D. & Lumbsch, H. T. Reference-based RADseq resolves robust relationships among closely related species of lichen-forming fungi using metagenomic DNA. Sci. Rep. 7, 9884, https://doi.org/10.1038/s41598-017-09906-7 (2017).
doi: 10.1038/s41598-017-09906-7
pubmed: 28852019
pmcid: 5575168
McCune, B. & Rosentreter, R. Biotic Soil Crust Lichens of the Columbia Basin. Vol. 39 (Northwest Lichenologists, 2007).
Leavitt, S. D. et al. Cryptic diversity and symbiont interactions in rock-posy lichens. Mol. Phylogenet Evol. 99, 261–274, https://doi.org/10.1016/j.ympev.2016.03.030 (2016).
doi: 10.1016/j.ympev.2016.03.030
pubmed: 27033947
Schoch, C. L. et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl Acad. Sci. USA 109, 6241–6246, https://doi.org/10.1073/pnas.1117018109 (2012).
doi: 10.1073/pnas.1117018109
pubmed: 22454494
Simao, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinforma. 31, 3210–3212, https://doi.org/10.1093/bioinformatics/btv351 (2015).
doi: 10.1093/bioinformatics/btv351
Bertels, F., Silander, O. K., Pachkov, M., Rainey, P. B. & van Nimwegen, E. Automated reconstruction of whole-genome phylogenies from short-sequence reads. Mol. Biol. Evol. 31, 1077–1088, https://doi.org/10.1093/molbev/msu088 (2014).
doi: 10.1093/molbev/msu088
pubmed: 24600054
pmcid: 3995342
Zeng, Q. et al. Comparative genomics of Spiraeoideae-infecting Erwinia amylovora strains provides novel insight to genetic diversity and identifies the genetic basis of a low-virulence strain. Mol. Plant. Pathol. 19, 1652–1666, https://doi.org/10.1111/mpp.12647 (2018).
doi: 10.1111/mpp.12647
pubmed: 29178620
pmcid: 6638132
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359, https://doi.org/10.1038/nmeth.1923 (2012).
doi: 10.1038/nmeth.1923
pubmed: 22388286
pmcid: 22388286
Stanke, M., Steinkamp, R., Waack, S. & Morgenstern, B. AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res. 32, W309–312, https://doi.org/10.1093/nar/gkh379 (2004).
doi: 10.1093/nar/gkh379
pubmed: 15215400
pmcid: 441517
Merchant, N. et al. The iPlant Collaborative: cyberinfrastructure for enabling data to discovery for the life sciences. Plos Biology 14, https://doi.org/10.1371/journal.pbio.1002342 (2016).
doi: 10.1371/journal.pbio.1002342
Goff, S. A. et al. The iPlant Collaborative: Cyberinfrastructure for Plant Biology. Front. Plant. Sci. 2, 34, https://doi.org/10.3389/fpls.2011.00034 (2011).
doi: 10.3389/fpls.2011.00034
pubmed: 22645531
pmcid: 3355756
Misof, B. et al. Selecting informative subsets of sparse supermatrices increases the chance to find correct trees. BMC Bioinforma. 14, 348, https://doi.org/10.1186/1471-2105-14-348 (2013).
doi: 10.1186/1471-2105-14-348
Parra, G., Bradnam, K. & Korf, I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinforma. 23, 1061–1067, https://doi.org/10.1093/bioinformatics/btm071 (2007).
doi: 10.1093/bioinformatics/btm071
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797, https://doi.org/10.1093/nar/gkh340 (2004).
doi: 10.1093/nar/gkh340
pubmed: 15034147
pmcid: 390337
Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477, https://doi.org/10.1089/cmb.2012.0021 (2012).
doi: 10.1089/cmb.2012.0021
pubmed: 22506599
pmcid: 3342519
Wyman, S. K., Jansen, R. K. & Boore, J. L. Automatic annotation of organellar genomes with DOGMA. Bioinforma. 20, 3252–3255, https://doi.org/10.1093/bioinformatics/bth352 (2004).
doi: 10.1093/bioinformatics/bth352
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780, https://doi.org/10.1093/molbev/mst010 (2013).
doi: 10.1093/molbev/mst010
pubmed: 23329690
pmcid: 3603318
Tonini, J., Moore, A., Stern, D., Shcheglovitova, M. & Orti, G. Concatenation and species tree methods exhibit statistically indistinguishable accuracy under a range of simulated conditions. PLoS Curr 7, https://doi.org/10.1371/currents.tol.34260cc27551a527b124ec5f6334b6be (2015).
Zhang, C., Rabiee, M., Sayyari, E. & Mirarab, S. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinforma. 19, 153, https://doi.org/10.1186/s12859-018-2129-y (2018).
doi: 10.1186/s12859-018-2129-y
Chifman, J. & Kubatko, L. Quartet inference from SNP data under the coalescent model. Bioinforma. 30, 3317–3324, https://doi.org/10.1093/bioinformatics/btu530 (2014).
doi: 10.1093/bioinformatics/btu530
Solis-Lemus, C. & Ane, C. Inferring phylogenetic networks with maximum pseudolikelihood under incomplete lineage sorting. PLoS Genet. 12, e1005896, https://doi.org/10.1371/journal.pgen.1005896 (2016).
doi: 10.1371/journal.pgen.1005896
pubmed: 26950302
pmcid: 4780787
Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274, https://doi.org/10.1093/molbev/msu300 (2015).
doi: 10.1093/molbev/msu300
pubmed: 25371430
Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol. Biol. Evol. 35, 518–522, https://doi.org/10.1093/molbev/msx281 (2018).
doi: 10.1093/molbev/msx281
pubmed: 29077904
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589, https://doi.org/10.1038/nmeth.4285 (2017).
doi: 10.1038/nmeth.4285
pubmed: 28481363
pmcid: 5453245
Edwards, S. V. Is a new and general theory of molecular systematics emerging? Evolution 63, 1–19, https://doi.org/10.1111/j.1558-5646.2008.00549.x (2009).
doi: 10.1111/j.1558-5646.2008.00549.x
pubmed: 19146594
Chou, J. et al. A comparative study of SVDquartets and other coalescent-based species tree estimation methods. BMC Genomics 16 (2015).
doi: 10.1186/1471-2164-16-S10-S2
Sayyari, E. & Mirarab, S. Fast coalescent-based computation of local branch support from quartet frequencies. Mol. Biol. Evolution 33, 1654–1668, https://doi.org/10.1093/molbev/msw079 (2016).
doi: 10.1093/molbev/msw079
Swofford, D. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0b10. Vol. Version 4.0 (2002).
Salichos, L., Stamatakis, A. & Rokas, A. Novel information theory-based measures for quantifying incongruence among phylogenetic trees. Mol. Biol. Evol. 31, 1261–1271, https://doi.org/10.1093/molbev/msu061 (2014).
doi: 10.1093/molbev/msu061
pubmed: 24509691
Burbrink, F. T. & Gehara, M. The Biogeography of Deep Time Phylogenetic Reticulation. Syst. Biol. 67, 743–744, https://doi.org/10.1093/sysbio/syy019 (2018).
doi: 10.1093/sysbio/syy019
pubmed: 29534232
Yu, Y. & Nakhleh, L. A maximum pseudo-likelihood approach for phylogenetic networks. Bmc Genomics 16, https://doi.org/10.1186/1471-2164-16-s10-s10 (2015).
Wen, D. Q., Yu, Y., Zhu, J. F. & Nakhleh, L. Inferring phylogenetic networks using PhyloNet. Syst. Biol. 67, 735–740, https://doi.org/10.1093/sysbio/syy015 (2018).
doi: 10.1093/sysbio/syy015
pubmed: 29514307
pmcid: 6005058
Sullivan, J. & Joyce, P. Model Selection in Phylogenetics. Annu. Rev. Ecology, Evolution, Syst. 36, 445–466, https://doi.org/10.1146/annurev.ecolsys.36.102003.152633 (2005).
doi: 10.1146/annurev.ecolsys.36.102003.152633
Akaike, H. In Selected Papers of Hirotugu Akaike (eds Emanuel Parzen, Kunio Tanabe, & Genshiro Kitagawa) 199–213 (Springer New York, 1998).
Blischak, P. D., Chifman, J., Wolfe, A. D. & Kubatko, L. S. HyDe: A Python Package for Genome-Scale Hybridization Detection. Syst. Biol. 67, 821–829, https://doi.org/10.1093/sysbio/syy023 (2018).
doi: 10.1093/sysbio/syy023
pubmed: 29562307
pmcid: 6454532
Green, R. E. et al. A Draft Sequence of the Neandertal Genome. Sci. 328, 710–722, https://doi.org/10.1126/science.1188021 (2010).
doi: 10.1126/science.1188021
Eaton, D. A. R. & Ree, R. H. Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae). Syst. Biol. 62, 689–706, https://doi.org/10.1093/sysbio/syt032 (2013).
doi: 10.1093/sysbio/syt032
pubmed: 23652346
pmcid: 3739883
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinforma. 30, 1312–1313, https://doi.org/10.1093/bioinformatics/btu033 (2014).
doi: 10.1093/bioinformatics/btu033
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772, https://doi.org/10.1038/nmeth.2109 (2012).
doi: 10.1038/nmeth.2109
pubmed: 22847109
pmcid: 4594756
Marques, D. A., Meier, J. I. & Seehausen, O. A combinatorial view on speciation and adaptive radiation. Trends Ecol Evol, https://doi.org/10.1016/j.tree.2019.02.008 (2019).
doi: 10.1016/j.tree.2019.02.008
Lewontin, R. C. Hybridization as a new source of variation for adaptation to new environments. Evolution 20, 315–336 (1966).
doi: 10.1111/j.1558-5646.1966.tb03369.x
Soltis, D. E. et al. Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biol. J. Linn. Soc. 82, 485–501 (2004).
doi: 10.1111/j.1095-8312.2004.00335.x
Wallbank, R. W. et al. Evolutionary novelty in a butterfly wing pattern through enhancer shuffling. PLoS Biol. 14, e1002353, https://doi.org/10.1371/journal.pbio.1002353 (2016).
doi: 10.1371/journal.pbio.1002353
pubmed: 26771987
pmcid: 4714872
Bell, C. D. et al. Rapid diversification of Tragopogon and ecological associates in Eurasia. J. Evol. Biol. 25, 2470–2480, https://doi.org/10.1111/j.1420-9101.2012.02616.x (2012).
doi: 10.1111/j.1420-9101.2012.02616.x
pubmed: 23163328
Bassham, S., Catchen, J., Lescak, E., von Hippel, F. A. & Cresko, W. A. Repeated Selection of Alternatively Adapted Haplotypes Creates Sweeping Genomic Remodeling in Stickleback. Genet. 209, 921–939, https://doi.org/10.1534/genetics.117.300610 (2018).
doi: 10.1534/genetics.117.300610
Pogoda, C. S. et al. Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria. Ecol. Evol. 9, 4245–4263, https://doi.org/10.1002/ece3.5056 (2019).
doi: 10.1002/ece3.5056
pubmed: 31016002
pmcid: 6467859
Aguileta, G. et al. High variability of mitochondrial gene order among fungi. Genome Biol. Evol. 6, 451–465, https://doi.org/10.1093/gbe/evu028 (2014).
doi: 10.1093/gbe/evu028
pubmed: 24504088
pmcid: 3942027
Blair, C. & Ane, C. Phylogenetic trees and networks can serve as powerful and complementary approaches for analysis of genomic data. Syst Biol, https://doi.org/10.1093/sysbio/syz056 (2019).
Kohn, L. M. Mechanisms of fungal speciation. Annu. Rev. Phytopathol. 43, 279–308, https://doi.org/10.1146/annurev.phyto.43.040204.135958 (2005).
doi: 10.1146/annurev.phyto.43.040204.135958
pubmed: 16078886
Lodé, T. Adaptive Significance and Long-Term Survival of Asexual Lineages. Evolut. Biol. 40, 450–460, https://doi.org/10.1007/s11692-012-9219-y (2012).
doi: 10.1007/s11692-012-9219-y
Janko, K. et al. Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation. Mol. Ecol. 27, 248–263, https://doi.org/10.1111/mec.14377 (2018).
doi: 10.1111/mec.14377
pubmed: 28987005
Pizarro, D. et al. Whole-Genome Sequence Data Uncover Widespread Heterothallism in the Largest Group of Lichen-Forming Fungi. Genome Biol. Evol. 11, 721–730, https://doi.org/10.1093/gbe/evz027 (2019).
doi: 10.1093/gbe/evz027
pubmed: 30715356
pmcid: 6414310
Kroken, S. & Taylor, J. W. Outcrossing and recombination in the lichenized fungus Letharia. Fungal Genet. Biol. 34, 83–92, https://doi.org/10.1006/fgbi.2001.1291 (2001).
doi: 10.1006/fgbi.2001.1291
pubmed: 11686674
Buschbom, J. & Mueller, G. M. Testing “species pair” hypotheses: evolutionary processes in the lichen-forming species complex Porpidia flavocoerulescens and Porpidia melinodes. Mol. Biol. Evol. 23, 574–586, https://doi.org/10.1093/molbev/msj063 (2006).
doi: 10.1093/molbev/msj063
pubmed: 16306384
Honegger, R. & Zippler, U. Mating systems in representatives of Parmeliaceae, Ramalinaceae and Physciaceae (Lecanoromycetes, lichen-forming ascomycetes). Mycol. Res. 111, 424–432, https://doi.org/10.1016/j.mycres.2007.02.005 (2007).
doi: 10.1016/j.mycres.2007.02.005
pubmed: 17512182
Tripp, E. A. Is asexual reproduction an evolutionary dead end in lichens? Lichenologist 48, 559–580, https://doi.org/10.1017/s0024282916000335 (2016).
doi: 10.1017/s0024282916000335
Roper, M., Ellison, C., Taylor, J. W. & Glass, N. L. Nuclear and genome dynamics in multinucleate ascomycete fungi. Curr. Biol. 21, R786–793, https://doi.org/10.1016/j.cub.2011.06.042 (2011).
doi: 10.1016/j.cub.2011.06.042
pubmed: 21959169
pmcid: 3184236
Clutterbuck, A. J. Parasexual recombination in fungi. Indian. Acad. Sci. 75, 281–286 (1996).
Ertz, D., Guzow-Krzeminska, B., Thor, G., Lubek, A. & Kukwa, M. Photobiont switching causes changes in the reproduction strategy and phenotypic dimorphism in the Arthoniomycetes. Sci. Rep. 8, 4952, https://doi.org/10.1038/s41598-018-23219-3 (2018).
doi: 10.1038/s41598-018-23219-3
pubmed: 29563606
pmcid: 5862901
Spribille, T. Relative symbiont input and the lichen symbiotic outcome. Curr. Opin. Plant. Biol. 44, 57–63, https://doi.org/10.1016/j.pbi.2018.02.007 (2018).
doi: 10.1016/j.pbi.2018.02.007
pubmed: 29529531