in

Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism

  • 1.

    Taylor, S. A. & Larson, E. L. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nat. Ecol. Evol. 3, 170–177 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  • 2.

    Payseur, B. A. & Rieseberg, L. H. A genomic perspective on hybridization and speciation. Mol. Ecol. 25, 2337–2360 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 3.

    Arnold, M. L. & Kunte, K. Adaptive genetic exchange: a tangled history of admixture and evolutionary innovation. Trends Ecol. Evol. 32, 601–611 (2017).

    PubMed  Article  Google Scholar 

  • 4.

    Mallet, J. Hybrid speciation. Nature 446, 279–283 (2007).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 5.

    Abbott, R. et al. Hybridization and speciation. J. Evol. Biol. 26, 229–246 (2013).

    CAS  PubMed  Article  Google Scholar 

  • 6.

    Gross, B. L. & Rieseberg, L. H. The ecological genetics of homoploid hybrid speciation. J. Hered. 96, 241–252 (2005).

    CAS  PubMed  Article  Google Scholar 

  • 7.

    Schumer, M., Rosenthal, G. G. & Andolfatto, P. How common is homoploid hybrid speciation? Evolution 68, 1553–1560 (2014).

    PubMed  Article  Google Scholar 

  • 8.

    Grant, V. Pollination systems as isolating mechanisms in angiosperms. Evolution 3, 82–97 (1949).

    CAS  PubMed  Article  Google Scholar 

  • 9.

    Kay, K. M. & Sargent, R. D. The role of animal pollination in plant speciation: Integrating ecology, geography, and genetics. Annu. Rev. Ecol. Evol. Syst. 40, 637–656 (2009).

    Article  Google Scholar 

  • 10.

    Serrano-Serrano, M. L., Rolland, J., Clark, J. L., Salamin, N. & Perret, M. Hummingbird pollination and the diversification of angiosperms: an old and successful association in Gesneriaceae. Proc. R. Soc. B Biol. Sci. 284, https://doi.org/10.1098/rspb.2016.2816 (2017).

  • 11.

    Thompson, J. N. Specific hypotheses on the geographic mosaic of coevolution. Am. Nat. 153, S1–S14 (1999).

    Article  Google Scholar 

  • 12.

    Van der Niet, T., Peakall, R. & Johnson, S. D. Pollinator-driven ecological speciation in plants: new evidence and future perspectives. Ann. Bot. 113, 199–211 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  • 13.

    Armbruster, W. S. The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Funct. Ecol. 31, 88–100 (2017).

    Article  Google Scholar 

  • 14.

    Ayasse, M., Stokl, J. & Francke, W. Chemical ecology and pollinator-driven speciation in sexually deceptive orchids. Phytochemistry 72, 1667–1677 (2011).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 15.

    Machado, C. A., Robbins, N., Gilbert, M. T. P. & Herre, E. A. Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proc. Natl Acad. Sci. USA 102, 6558–6565 (2005).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 16.

    Kawakita, A. Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae). Plant Species Biol. 25, 3–19 (2010).

    Article  Google Scholar 

  • 17.

    Ramirez, W. Host specificity of fig wasps (Agaonidae). Evolution 24, 680–691 (1970).

    Article  Google Scholar 

  • 18.

    Schiestl, F. P. & Schluter, P. M. Floral isolation, specialized pollination, and pollinator behavior in orchids. Annu. Rev. Entomol. 54, 425–446 (2009).

    CAS  PubMed  Article  Google Scholar 

  • 19.

    Ramirez, S. R. et al. Asynchronous diversification in a specialized plant-pollinator mutualism. Science 333, 1742–1746 (2011).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 20.

    Cruaud, A. et al. An extreme case of plant-insect co-diversification: figs and fig-pollinating wasps. Syst. Biol. 61, 1029–1047 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  • 21.

    Berg, C. C. & Corner, E. J. H. in Flora Malesiana Series I -Seed Plants Vol. 17 (ed. Nooteboom, H. P.) 1–702 (Nationaal Herbarium, Nederland, 2005).

  • 22.

    Wang, G., Cannon, C. H. & Chen, J. Pollinator sharing and gene flow among closely related sympatric dioecious fig taxa. Proc. R. Soc. B Biol. Sci. 283, https://doi.org/10.1098/rspb.2015.2963 (2016).

  • 23.

    Machado, C. A., Jousselin, E., Kjellberg, F., Compton, S. G. & Herre, E. A. Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating wasps. Proc. R. Soc. B Biol. Sci. 268, 685–694 (2001).

    CAS  Article  Google Scholar 

  • 24.

    Harrison, R. D. Figs and the diversity of tropical rainforests. Bioscience 55, 1053–1064 (2005).

    Article  Google Scholar 

  • 25.

    Grison-Pigé, L., Bessière, J. M. & Hossaert-McKey, M. Specific attraction of fig-pollinating wasps: Role of volatile compounds released by tropical figs. J. Chem. Ecol. 28, 283–295 (2002).

    PubMed  Article  PubMed Central  Google Scholar 

  • 26.

    Herre, E. A. et al. Molecular phylogenies of figs and their pollinator wasps. J. Biogeogr. 23, 521–530 (1996).

    Article  Google Scholar 

  • 27.

    Molbo, D., Machado, C. A., Sevenster, J. G., Keller, L. & Herre, E. A. Cryptic species of fig-pollinating wasps: Implications for the evolution of the fig-wasp mutualism, sex allocation, and precision of adaptation. Proc. Natl Acad. Sci. USA 100, 5867–5872 (2003).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 28.

    Rasplus, J. Y. in The Biodiversity of African Plants (eds van der Maesen, L. J. G. et al.) 639–649 (Springer, 1996).

  • 29.

    Yang, L.-Y. et al. The incidence and pattern of co-pollinator diversification in dioecious and monoecious figs. Evolution 69, 294–304 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  • 30.

    Cornille, A. et al. Floral volatiles, pollinator sharing and diversification in the fig-wasp mutualism: insights from Ficus natalensis, and its two wasp pollinators (South Africa). Proc. R. Soc. B Biol. Sci. 279, 1731–1739 (2012).

    CAS  Article  Google Scholar 

  • 31.

    Compton, S. G. A collapse of host specificity in some African fig wasps. S. Afr. J. Sci. 86, 39–40 (1990).

    Google Scholar 

  • 32.

    Renoult, J. P., Kjellberg, F., Grout, C., Santoni, S. & Khadari, B. Cyto-nuclear discordance in the phylogeny of Ficus section Galoglychia and host shifts in plant-pollinator associations. BMC Evol. Biol. 9, 248 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 33.

    Satler, J. D. et al. Inferring processes of coevolutionary diversification in a community of Panamanian strangler figs and associated pollinating wasps. Evolution 73, 2295–2311 (2019).

  • 34.

    Jackson, A. P., Machado, C. A., Robbins, N. & Herre, E. A. Multi-locus phylogenetic analysis of neotropical figs does not support co-speciation with the pollinators: the importance of systematic scale in fig/wasp cophylogenetic studies. Symbiosis 45, 57–72 (2008).

    CAS  Google Scholar 

  • 35.

    Parrish, T. L., Koelewijn, H. P., van Dijk, P. J. & Kruijt, M. Genetic evidence for natural hybridization between species of dioecious Ficus on island populations. Biotropica 35, 333–343 (2003).

    Article  Google Scholar 

  • 36.

    Ramirez, W. Hybridization of Ficus religiosa with F. septica and F. aurea (Moraceae). Rev. Biol. Trop. 42, 339–342 (1994).

    Google Scholar 

  • 37.

    Wei, Z. D., Kobmoo, N., Cruaud, A. & Kjellberg, F. Genetic structure and hybridization in the species group of Ficus auriculata: can closely related sympatric Ficus species retain their genetic identity while sharing pollinators? Mol. Ecol. 23, 3538–3550 (2014).

    PubMed  Article  PubMed Central  Google Scholar 

  • 38.

    Bruun-Lund, S., Clement, W. L., Kjellberg, F. & Rønsted, N. First plastid phylogenomic study reveals potential cyto-nuclear discordance in the evolutionary history of Ficus L. (Moraceae). Mol. Phylogenet. Evol. 109, 93–104 (2017).

    PubMed  Article  Google Scholar 

  • 39.

    Zhang, X. et al. Genomes of the Banyan tree and pollinator wasp provide insights into fig-wasp coevolution. Cell 183, 875–889 (2020).

    CAS  PubMed  Article  Google Scholar 

  • 40.

    Mirarab, S. & Warnow, T. ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, 44–52 (2015).

    Article  CAS  Google Scholar 

  • 41.

    Rønsted, N., Weiblen, G. D., Clement, W. L., Zerega, N. J. C. & Savolainen, V. Reconstructing the phylogeny of figs (Ficus, Moraceae) to reveal the history of the fig pollination mutualism. Symbiosis 45, 45–55 (2008).

    Google Scholar 

  • 42.

    Ane, C., Larget, B., Baum, D. A., Smith, S. D. & Rokas, A. Bayesian estimation of concordance among gene trees. Mol. Biol. Evol. 24, 412–426 (2007).

    CAS  PubMed  Article  Google Scholar 

  • 43.

    Larget, B. R., Kotha, S. K., Dewey, C. N. & Ane, C. BUCKy: Gene tree/species tree reconciliation with Bayesian concordance analysis. Bioinformatics 26, 2910–2911 (2010).

    CAS  PubMed  Article  Google Scholar 

  • 44.

    Baum, D. A. Concordance trees, concordance factors, and the exploration of reticulate genealogy. Taxon 56, 417–426 (2007).

    Article  Google Scholar 

  • 45.

    Solis-Lemus, C., Bastide, P. & Ane, C. PhyloNetworks: a package for phylogenetic networks. Mol. Biol. Evol. 34, 3292–3298 (2017).

    CAS  PubMed  Article  Google Scholar 

  • 46.

    Soraggi, S., Wiuf, C. & Albrechtsen, A. Powerful inference with the D-statistic on low-coverage whole-genome data. G3 (Bethesda) 8, 551–566 (2018).

  • 47.

    Durand, E. Y., Patterson, N., Reich, D. & Slatkin, M. Testing for ancient admixture between closely related populations. Mol. Biol. Evol. 28, 2239–2252 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 48.

    Degnan, J. H. & Rosenberg, N. A. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol. Evol. 24, 332–340 (2009).

    PubMed  Article  Google Scholar 

  • 49.

    Conow, C., Fielder, D., Ovadia, Y. & Libeskind-Hadas, R. Jane: a new tool for the cophylogeny reconstruction problem. Algorithms Mol. Biol. 5, https://doi.org/10.1186/1748-7188-5-16 (2010).

  • 50.

    Ramsey, A. J. & Mandel, J. R. When one genome is not enough: organellar heteroplasmy in plants. Annual Plant Reviews 2, 619–658 (2019).

    Article  Google Scholar 

  • 51.

    Zhang, Q. & Liu, Y. & Sodmergen. Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant Cell Physiol. 44, 941–951 (2003).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 52.

    Hu, Y. C., Zhang, Q. & Rao, G. Y. & Sodmergen. Occurrence of plastids in the sperm cells of Caprifoliaceae: Biparental plastid inheritance in angiosperms is unilaterally derived from maternal inheritance. Plant Cell Physiol. 49, 958–968 (2008).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 53.

    Mayr, E. Animal Species and Evolution 1–811 (Belknap Press, 1963).

  • 54.

    Wu, C. I. The genic view of the process of speciation. J. Evol. Biol. 14, 851–865 (2001).

    Article  Google Scholar 

  • 55.

    Sun, M. et al. Deep phylogenetic incongruence in the angiosperm clade Rosidae. Mol. Phylogenet. Evol. 83, 156–166 (2015).

    PubMed  Article  PubMed Central  Google Scholar 

  • 56.

    Folk, R. A., Soltis, P. S., Soltis, D. E. & Guralnick, R. New prospects in the detection and comparative analysis of hybridization in the tree of life. Am. J. Bot. 105, 364–375 (2018).

    PubMed  Article  PubMed Central  Google Scholar 

  • 57.

    Jiao, X., Flouri, T., Rannala, B. & Yang, Z. The impact of cross-species gene flow on species tree estimation. Syst. Biol. 69, 830–847 (2020).

  • 58.

    Jousselin, E. et al. One fig to bind them all: host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and nonpollinating fig wasps. Evolution 62, 1777–1797 (2008).

    PubMed  Article  PubMed Central  Google Scholar 

  • 59.

    Moe, A. M. & Weiblen, G. D. Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae). Evolution 66, 3710–3721 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  • 60.

    Wang, G., Compton, S. G. & Chen, J. The mechanism of pollinator specificity between two sympatric fig varieties: a combination of olfactory signals and contact cues. Ann. Bot. 111, 173–181 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 61.

    Bronstein, J. L. Maintenance of species-specificity in a neotropical fig – pollinator wasp mutualism. Oikos 48, 39–46 (1987).

    Article  Google Scholar 

  • 62.

    Ware, A., Kaye, P., Compton, S. & Noort, S. Fig volatiles: their role in attracting pollinators and maintaining pollinator specificity. Plant Syst. Evol. 186, 147–156 (1993).

    Article  Google Scholar 

  • 63.

    Soler, C. C. L., Proffit, M., Bessière, J. M., Hossaert-McKey, M. & Schatz, B. Evidence for intersexual chemical mimicry in a dioecious plant. Ecol. Lett. 15, 978–985 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  • 64.

    Hossaert-McKey, M., Soler, C., Schatz, B. & Proffit, M. Floral scents: their roles in nursery pollination mutualisms. Chemoecology 20, 75–88 (2010).

    Article  Google Scholar 

  • 65.

    Knudsen, J. T., Eriksson, R., Gershenzon, J. & Stahl, B. Diversity and distribution of floral scent. Bot. Rev. 72, 1–120 (2006).

    Article  Google Scholar 

  • 66.

    Herre, E. A., Jander, K. C. & Machado, C. A. Evolutionary ecology of figs and their associates: Recent progress and outstanding puzzles. Annu. Rev. Ecol. Evol. Syst. 39, 439–458 (2008).

    Article  Google Scholar 

  • 67.

    Kiester, A. R., Lande, R. & Schemske, D. W. Models of coevolution and speciation in plants and their pollinators. Am. Nat. 124, 220–243 (1984).

    Article  Google Scholar 

  • 68.

    Vereecken, N. J., Cozzolino, S. & Schiestl, F. P. Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids. BMC Evol. Biol. 10, 103 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 69.

    Rønsted, N. et al. 60 million years of co-divergence in the fig-wasp symbiosis. Proc. R. Soc. B Biol. Sci. 272, 0962–8452 (2005). 2593-2599.

    Google Scholar 

  • 70.

    Wiebes, J. T. Co-evolution of figs and their insect pollinators. Annu. Rev. Ecol. Syst. 10, 1–12 (1979).

    Article  Google Scholar 

  • 71.

    Zhu, H. et al. Native Seed Plants in Xishuangbanna of Yunnan (eds Zhu, H. & Yan, L.) 1–565 (Science Press, 2012).

  • 72.

    Yang, J. B., Li, D. Z. & Li, H. T. Highly effective sequencing whole chloroplast genomes of angiosperms by nine novel universal primer pairs. Mol. Ecol. Resour. 14, 1024–1031 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 73.

    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 74.

    Andrews, S. FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2010).

  • 75.

    Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589–595 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 76.

    Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 77.

    McKenna, A. et al. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 78.

    Jin, J.-J. et al. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 21, 31 (2020).

    Article  Google Scholar 

  • 79.

    Wick, R. R., Schultz, M. B., Zobel, J. & Holt, K. E. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31, 3350–3352 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 80.

    Weiß, C. L., Pais, M., Cano, L. M., Kamoun, S. & Burbano, H. A. nQuire: a statistical framework for ploidy estimation using next generation sequencing. BMC Bioinformatics 19, 122 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 81.

    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 82.

    Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  • 83.

    Yang, Z. H. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

    CAS  PubMed  Article  Google Scholar 

  • 84.

    Zhu, T. Q., Dos Reis, M. & Yang, Z. H. Characterization of the uncertainty of divergence time estimation under relaxed molecular clock models using multiple loci. Syst. Biol. 64, 267–280 (2015).

    CAS  PubMed  Article  Google Scholar 

  • 85.

    Gardner, E. M., Sarraf, P., Williams, E. W. & Zerega, N. J. C. Phylogeny and biogeography of Maclura (Moraceae) and the origin of an anachronistic fruit. Mol. Phylogenet. Evol. 117, 49–59 (2017).

    PubMed  Article  Google Scholar 

  • 86.

    dos Reis, M. & Yang, Z. Approximate likelihood calculation on a phylogeny for bayesian estimation of divergence times. Mol. Biol. Evol. 28, 2161–2172 (2011).

    PubMed  Article  CAS  Google Scholar 

  • 87.

    Yang, Z. & Rannala, B. Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol. Biol. Evol. 23, 212–226 (2006).

    CAS  PubMed  Article  Google Scholar 

  • 88.

    Matzke, N. J. Model selection in historical biogeography reveals that founder-event speciation is a crucial process in Island Clades. Syst. Biol. 63, 951–970 (2014).

    PubMed  Article  Google Scholar 

  • 89.

    Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 90.

    Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772–772 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 91.

    Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

  • 92.

    Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: analysis of next generation sequencing data. BMC Bioinformatics 15, 1–13 (2014).

    Article  Google Scholar 

  • 93.

    Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 94.

    Wang, G. et al. Data from: Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism. Dryad, Dataset https://doi.org/10.5061/dryad.zcrjdfn7m (2020).

  • 95.

    Zhang, T. & Zhang, S. C. Code from: Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism. Github https://doi.org/10.5281/zenodo.4308886 (2020).


  • Source: Ecology - nature.com

    Geologists produce new timeline of Earth’s Paleozoic climate changes

    Sludge amendment accelerating reclamation process of reconstructed mining substrates