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Phylogenomics reveals the origin of mammal lice out of Afrotheria

Nature Ecology & Evolution volume 6, pages 1205–1210 (2022)Cite this article

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Abstract

Mammals host a wide diversity of parasites. Lice, comprising more than 5,000 species, are one group of ectoparasites whose major lineages have a somewhat patchwork distribution across the major groups of mammals. Here we explored patterns in the diversification of mammalian lice by reconstructing a higher-level phylogeny of these lice, leveraging whole genome sequence reads to assemble single-copy orthologue genes across the genome. The evolutionary tree of lice indicated that three of the major lineages of placental mammal lice had a single common ancestor. Comparisons of this parasite phylogeny with that for their mammalian hosts indicated that the common ancestor of elephants, elephant shrews and hyraxes (that is, Afrotheria) was the ancestral host of this group of lice. Other groups of placental mammals obtained their lice via host-switching out of these Afrotherian ancestors. In addition, reconstructions of the ancestral host group (bird versus mammal) for all parasitic lice supported an avian ancestral host, indicating that the ancestor of Afrotheria acquired these parasites via host-switching from an ancient avian host. These results shed new light on the long-standing question of why the major groups of parasitic lice are not uniformly distributed across mammals and reveal the origins of mammalian lice.

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Fig. 1: Phylogenetic tree from maximum likelihood analysis of the concatenated alignment of 3,921,975 bp from 2,395 single-copy target nuclear gene orthologues.
Fig. 2: Cophylogenetic comparison of dated mammal (left) and mammal louse (right) phylogenies.

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Data availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Information. Phylogenomic data generated in this study are available at figshare (https://doi.org/10.6084/m9.figshare.18737423).

References

  1. Wilson, D. E., Mittermeier, R. A. & Cavallini, P. Handbook of the Mammals of the World Vol. 1 (Lynx Edicions, 2009).

  2. Meredith, R. W. et al. Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334, 521–524 (2011).

    Article  CAS  Google Scholar 

  3. dos Reis, M. et al. Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proc. R. Soc. B 279, 3491–3500 (2012).

    Article  Google Scholar 

  4. O’Leary, M. A. et al. The placental mammal ancestor and the post-K–Pg radiation of placentals. Science 339, 662–667 (2013).

    Article  Google Scholar 

  5. Upham, N. S., Esselstyn, J. A. & Jetz, W. Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biol. 17, e3000494 (2019).

    Article  CAS  Google Scholar 

  6. Murphy, W. J., Foley, N. M., Bredemeyer, K. R., Gatesy, J. & Springer, M. S. Phylogenomics and the genetic architecture of the placental mammal radiation. Annu. Rev. Anim. Biosci. 9, 29–53 (2021).

    Article  CAS  Google Scholar 

  7. Álvarez-Carretero, S. et al. A species-level timeline of mammal evolution integrating phylogenomic data. Nature 602, 263–267 (2022).

    Article  Google Scholar 

  8. Kim, K. C. Coevolution of Parasitic Arthropods and Mammals (Wiley, 1986).

  9. Johnson, K. P. et al. Simultaneous radiation of bird and mammal lice following the K–Pg boundary. Biol. Lett. 14, 20180141 (2018).

    Article  Google Scholar 

  10. Hafner, M. S. & Nadler, S. A. Phylogenetic trees support the coevolution of parasites and their hosts. Nature 332, 258–259 (1988).

    Article  CAS  Google Scholar 

  11. Huelsenbeck, J. P. & Rannala, B. Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276, 227–232 (1997).

    Article  CAS  Google Scholar 

  12. Page, R. D. M. & Charleston, M. A. Trees within trees: phylogeny and historical associations. Trends Ecol. Evol. 13, 356–359 (1998).

    Article  CAS  Google Scholar 

  13. Nieberding, C. M. & Olivieri, I. Parasites: proxies for host genealogy and ecology? Trends Ecol. Evol. 22, 156–165 (2007).

    Article  Google Scholar 

  14. Allen, J. M., Worman, C. O., Light, J. E. & Reed D. L. in Developments in Primatology: Progress and Prospects Vol. 38 (eds Brinkworth, J. & Pechenkina, K.) 161–186 (Springer, 2013).

  15. Clayton, D. H., Bush, S. E. & Johnson, K. P. Coevolution of Life on Hosts: Integrating Ecology and History (Univ. Chicago Press, 2015).

  16. Althoff, D. M., Segraves, K. A. & Johnson, M. T. J. Testing for coevolutionary diversification: linking pattern with process. Trends Ecol. Evol. 29, 82–89 (2014).

    Article  Google Scholar 

  17. Hayward, A., Poulin, R. & Nakagawa, S. A broadscale analysis of host-symbiont cophylogeny reveals the drivers of phylogenetic congruence. Ecol. Lett. 24, 1681–1696 (2021).

  18. Price, R. D., Hellenthal, R. A., Palma, R. L., Johnson, K. P. & Clayton, D. H. The Chewing Lice: World Checklist and Biological Overview (Illinois Natural History Survey, 2003).

  19. Durden, L. A. & Musser, G. G. The Sucking Lice (Insecta, Anoplura) of the World: A Taxonomic Checklist with Records of Mammalian Hosts and Geographical Distributions (American Museum of Natural History, 1994).

  20. de Moya, R. S. et al. Phylogenomics of parasitic and non-parasitic lice (Insecta: Psocodea): combining sequence data and exploring compositional bias solutions in next generation datasets. Syst. Biol. 70, 719–738 (2021).

    Article  Google Scholar 

  21. Reed, D. L., Light, J. E., Allen, J. M. & Kirchman, J. J. Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice. BMC Biol. 5, 7 (2007).

    Article  Google Scholar 

  22. Light, J. E., Smith, V. S., Allen, J. M., Durden, L. A. & Reed, D. L. Evolutionary history of mammalian sucking lice (Phthiraptera: Anoplura). BMC Evol. Biol. 10, 292 (2010).

    Article  Google Scholar 

  23. Balbuena, J. A., Míguez-Lozano, R. & Blasco-Costa, I. PACo: a novel Procrustes application to cophylogenetic analysis. PLoS ONE 8, e61048 (2013).

    Article  CAS  Google Scholar 

  24. Santichaivekin, S. et al. eMPRess: a systematic cophylogeny reconciliation tool. Bioinformatics https://doi.org/10.1093/bioinformatics/btaa978 (2020).

  25. Boyd, B. M. et al. Long-distance dispersal of pigeons and doves generated new ecological opportunities for host-switching and adaptive radiation by their parasites. Proc. R. Soc. B https://doi.org/10.1098/rspb.2022.0042 (2022).

  26. Catanach, T. A. & Johnson, K. P. Independent origins of the feather lice (Insecta: Degeeriella) of raptors. Biol. J. Linn. Soc. 114, 837–847 (2015).

    Article  Google Scholar 

  27. de Moya, R. S. et al. Extensive host-switching of avian feather lice following the Cretaceous–Paleogene mass extinction event. Commun. Biol. 2, 445 (2019).

    Article  Google Scholar 

  28. Hafner, M. S. et al. Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265, 1087–1090 (1994).

    Article  CAS  Google Scholar 

  29. Page, R. D. M. (ed.) Tangled Trees: Phylogeny, Cospeciation, and Coevolution (Univ. Chicago Press, 2003).

  30. Allen, J. M., LaFrance, R., Folk, R. A., Johnson, K. P. & Guralnick, R. P. aTRAM 2.0: an improved, flexible locus assembler for NGS data. Evol. Bioinform. 14, 1176934318774546 (2018).

    Article  Google Scholar 

  31. Johnson, K. P., Weckstein, J. D., Herrera, S. V. & Doña, J. The interplay between host biogeography and phylogeny in structuring diversification of the feather louse genus Penenirmus. Mol. Phylogenet. Evol. 165, 107297 (2021).

  32. Slater, G. S. C. & Birney, E. Automated generation of heuristics for biological sequence comparison. BMC Bioinform. 6, 31 (2005).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  34. Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).

    Article  Google Scholar 

  35. Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  37. Zhang, C., Rabiee, M., Sayyari, E. & Mirarab, S. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinform. 19, 153 (2018).

    Article  Google Scholar 

  38. Ronquist, F., Lartillot, N. & Phillips, M. J. Closing the gap between rocks and clocks using total-evidence dating. Phil. Trans. R. Soc. B 371, 20150136 (2016).

    Article  Google Scholar 

  39. Legendre, P., Desdevises, Y. & Bazin, E. A statistical test for host–parasite coevolution. Syst. Biol. 51, 217–234 (2002).

    Article  Google Scholar 

  40. Smith, V. S. et al. Multiple lineages of lice pass through the K–Pg boundary. Biol. Lett. 7, 782–785 (2011).

    Article  Google Scholar 

  41. Johnson, K. P. et al. Phylogenomics and the evolution of hemipteroid insects. Proc. Natl Acad. Sci. USA 115, 12775–12780 (2018).

    Article  CAS  Google Scholar 

  42. Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2018).

    Article  Google Scholar 

Download references

Acknowledgements

We thank J. Allen, K. C. Bell, I. Beveridge, S. Bush, T. Chesser, D. Clayton, C. Floyd, R. Furness, T. D. Galloway, S. Goodman, P. James, R. E. Junge, A. Lawrence, S. Leonardi, J. Malenke, S. Matthee, K. McCracken, M. Meyer, L. Mugisha, T. Nyman, B. O’Shea, E. Osnas, R. Palma, J. Scherer, V. Smith, T. Spradling, O. Sychra, W. Veronesi, D. Verrier, J. Weckstein and R. Wilson for assistance in obtaining specimens for this study. Funding was provided by US NSF DEB-1239788, DEB-1925487 and DEB-1926919 grant awards to K.P.J, and European Commission grant H2020-MSCA-IF-2019 (INTROSYM:886532) to J.D. We thank R. de Moya, S. Virrueta Herrera and K. K. O. Walden for assistance with DNA extraction. We thank A. Hernandez and the Roy J. Carver Biotechnology Center at the University of Illinois for assistance with genome sequencing. We thank K. K. O. Walden for assistance with submission of data to NCBI. Images copyright Lynx Edicions originally illustrated by H. Burn, F. Jutglar, T. Llobet, F. Peacock, L. Sanz, L. Solé and I. Velikov. We thank L. J. Revell for assistance with Fig. 2. We thank CSIRC personnel (Universidad de Granada, Spain) for assistance and providing computational resources (Alhambra supercomputer).

Author information

Authors and Affiliations

  1. Illinois Natural History Survey, Prairie Research Institute, University of Illinois, Champaign, IL, USA

    Kevin P. Johnson & Jorge Doña

  2. Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa

    Conrad Matthee

  3. Departamento de Biología Animal, Universidad de Granada, Granada, Spain

    Jorge Doña

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  1. Kevin P. Johnson
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Contributions

K.P.J. designed the study, obtained funding and wrote the manuscript draft. C.M. provided critical samples and edited the manuscript. J.D. designed the study, conducted the analyses, prepared figures and edited the manuscript.

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Correspondence to Kevin P. Johnson or Jorge Doña.

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Nature Ecology & Evolution thanks the anonymous reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Summary of cophylogenetic reconstruction of optimal MPRs from eMPRess comparison (cost scheme duplication: 1, sorting: 1, and host-switching: 2) of the louse (concatenated) tree with the mammal host tree.

Arrows indicate direction of host-switches. Numbers associated with events are the percentage of MPRs with that event.

Extended Data Fig. 2 Summary of cophylogenetic reconstruction of optimal MPRs from eMPRess comparison (cost scheme duplication: 1, sorting: 1, and host-switching: 2) of the louse (coalescent) tree with the mammal host tree.

Arrows indicate direction of host-switches. Numbers associated with events are the percentage of MPRs with that event.

Extended Data Fig. 3 Jack-knifed squared residuals (bars) and upper 95% confidence interval (error bars) associated with each mammal-louse association (link).

Dashed line indicates the overall median squared residual value (n = 33 biologically independent samples).

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Johnson, K.P., Matthee, C. & Doña, J. Phylogenomics reveals the origin of mammal lice out of Afrotheria. Nat Ecol Evol 6, 1205–1210 (2022). https://doi.org/10.1038/s41559-022-01803-1

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