Extensive host-switching of avian feather lice following the Cretaceous-Paleogene mass extinction event

Abstract

Nearly all lineages of birds host parasitic feather lice. Based on recent phylogenomic studies, the three major lineages of modern birds diverged from each other before the Cretaceous-Paleogene (K-Pg) mass extinction event. In contrast, studies of the phylogeny of feather lice on birds, indicate that these parasites diversified largely after this event. However, these studies were unable to reconstruct the ancestral avian host lineage for feather lice. Here we use genome sequences of a broad diversity of lice to reconstruct a phylogeny based on 1,075 genes. By comparing this louse evolutionary tree to the avian host tree, we show that feather lice began diversifying on the common ancestor of waterfowl and landfowl, then radiated onto other avian lineages by extensive host-switching. Dating analyses and cophylogenetic comparisons revealed that two of three lineages of birds that diverged before the K-Pg boundary acquired their feather lice after this event via host-switching.

Keywords: Coevolution; Phylogenetics.

Fig. 1

Phylogeny of feather lice and outgroups based on a partitioned maximum likelihood search with 3rd codon positions removed. Summary support for other analyses are provided on nodes. The first value is the bootstrap support from the maximum likelihood analysis of the data with 3rd positions removed. The second value is bootstrap support based on maximum likelihood analysis of all nucleotide sites. The third value is the local posterior probability from the Astral gene tree analysis. Note: Two exceptionally long branches are broken for the purposes of graphical display. Images are obtained from phylopic.org (Cuculidae: Lip Kee Yap; Struthio: Matt Martyniuk and T. Michael Keesey; Rhea: Darren Naish and T. Michael Keesey; Falco: Liftarn; Tauraco: Lisa M. “Pixxl”, John E. McCormack, Michael G. Harvey, Brant C. Faircloth, Nicholas G. Crawford, Travis C. Glenn, Robb T. Brumfield and T. Michael Keesey; Podiceps: Doug Backlund, John E. McCormack, Michael G. Harvey, Brant C. Faircloth, Nicholas G. Crawford, Travis C. Glenn, Robb T. Brumfield and T. Michael Keesey; Phalacrocoracidae: L. Shymal; Fulmarus: Bennet McComish and Avenue; Aptenodytes: Neil Kelley; Columbidae: Dori and Nevit Delmin; Sciurus: Anthony Caravaggi; Cavioidea: Zimices; Macropodiformes: T. Michael Keesey and Tony Hisgett; all images are modified under license: https://creativecommons.org/licenses/by-sa/3.0/legalcode) (Hoatzin: Warren H. and T. Michael Keesey; Tinamus: Darren Naish and T. Michael Keesey; Buteo: Shyamal; Laridae: Rebecca Groom; Ardea: Rebecca Groom; Coliidae: Joseph Wetsy, John E. McCormack, Michael G. Harvey, Brant C. Faircloth, Nicholas G. Crawford, Travis C. Glenn, Robb T. Brumfield and T. Michael Keesey; Gavia: John E. McCormack, Michael G. Harvey, Brant C. Faircloth, Nicholas G. Crawford, Travis C. Glenn, Robb T. Brumfield and T. Michael Keesey; Connochaetes: Jan A. Venter, Herbert H. T. Prins, David A. Balfour, Rob Slotow and T. Michael Keesey; Pan: T. Michael Keesey and Tony Hisgett; Dromaius: Darren Naish and T. Michael Keesey; all images are modified under license: https://creativecommons.org/licenses/by/3.0/legalcode).

Fig. 2

Cophylogenetic comparison of feather lice (b) with their avian hosts (a). Colors of branches in the feather louse phylogeny corresponds to the colors of the branch of major groups of their avian hosts. The feather louse tree is based upon the partitioned maximum likelihood analysis of the concatenated matrix with 3rd codon positions removed (Fig. 1). Timescale corresponds to results from dating analyses of the feather louse tree performed in MCMCtree. The bird host tree is based on Prum et al. Dashed arrows indicate reconstructed host-switches from other avian groups to Palaeognathae as indicated by the Jane cophylogenetic analyses. Colored circles identify cospeciation events between birds and feather lice as indicated by the Jane analysis.