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Phylogenomics reveals the origin of mammal lice out of Afrotheria

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.

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).

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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

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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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The authors declare no competing interests.

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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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