AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (6.4 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Bird species (Charadriiformes) does not impact endosymbiotic bacteria (Gammaproteobacteria) of their ectoparasites (Insecta: Phthiraptera: Ischnocera)

Alexandra A. GrossiaMin Zhanga,b( )Fasheng ZouaDaniel R. Gustafssona
Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Library of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, 510260, China
Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China
Show Author Information

Abstract

Endosymbiotic bacteria of insects can facilitate host expansion into novel niches by providing their host with a fitness benefit such as vitamins or amino acids that are otherwise lacking in their hosts' diet. This close association can lead to cospeciation between insects and their symbionts; however, the symbionts’ small genome size leaves it susceptible to genome derogation which can result in symbiont replacement. Here, we screen chewing lice infesting shorebirds and terns to see what endosymbiotic bacteria are present, and build a summary phylogeny that includes louse endosymbiont sequences from this study as well as those from other louse genera, insects and bacteria strains from GenBank. We found a Sodalis-allied endosymbiont in Carduiceps, Lunaceps, Quadraceps, and Saemundssonia, as well as symbionts belonging to the family Enterobacteriaceae in Lunaceps, and Quadraceps. No louse species were host to both endosymbionts; however, the birds Kentish Plover (Charadrius alexandrinus) and Greater Crested Tern (Thalasseus bergii) were host to two genera of lice, each of which was infested with a different group of endosymbionts. In the summary phylogeny the endosymbionts from shorebirds, and tern lice did not form a monophyletic group, and therefore likely acquired their bacterial endosymbionts multiple times.

References

 

Alickovic, L., Johnson, K.P., Boyd, B.M., 2021. The reduced genome of a heritable symbiont from an ectoparasitic feather feeding louse. BMC Ecol. Evol. 21, 108.

 
Arlott, N., 2017. Birds of South-East Asia. Collins Field Guide. Harper Collins, London.
 

Brooke, M.D.L., 2010. Vertical transmission of feather lice between adult blackbirds Turdus merula and their nestlings: a lousy perspective. J. Parasitol. 96, 1076–1080.

 

Clayton, D.H., Tompkins, D.M., 1994. Ectoparasite virulence is linked to mode of transmission. Proc. R. Soc. B 256, 211–217.

 
Clements, J.F., Schulenberg, T.S., Iliff, M.J., Fredericks, T.A., Gerbracht, J.A., Lepage, D., et al., 2022. The eBird/Clements checklist of Birds of the World: v2022. https://www.birds.cornell.edu/clementschecklist/download/. (Accessed 2 January 2023).
 

Dale, C., Maudlin, I., 1999. Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int. J. Syst. Bacteriol. 49, 267–275.

 
D’Alessio, L.M., 2023. Cophylogenetics of the Brueelia-Complex (Phthiraptera: Ischnocera) with avian hosts and bacterial endosymbionts. University of Illinois, Urbana-Champaign, Urbana, Illinois. Master’s Thesis.
 

Danforth, B.N., Ji, S., 1998. Elongation factor-1 alpha occurs as two copies in bees: implications for phylogenetic analysis of EF-1 alpha sequences in insects. Mol. Biol. Evol. 15, 225–235.

 

de Moya, R.S., Allen, J.M., Sweet, A.D., Walden, K.K.O., Palma, R.L., Smith, V.S., et al., 2019. Extensive host-switching of avian feather lice following the Cretaceous-Paleogene mass extinction event. Commun. Biol. 2, 445.

 

Douglas, A.E., 2009. The microbial dimension in insect nutritional ecology. Funct. Ecol. 23, 38–47.

 

Edgar, R.C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797.

 

Fujisawa, T., Barraclough, T.G., 2013. Delimiting species using single-locus data and the generalized mixed yule coalescent approach: a revised method and evaluation on simulated data sets. Syst. Biol. 62, 707–724.

 

Fukatsu, T., Koga, R., Smith, W.A., Tanaka, K., Nikoh, N., Sasaki-Fukatsu, K., et al., 2007. Bacterial endosymbiont of the slender pigeon louse, Columbicola columbae, allied to endosymbionts of grain weevils and tsetse flies. Appl. Environ. Microbiol. 73, 6660–6668.

 

Grossi, A.A., Tian, C., Ren, M., Zou, F., Gustafsson, D.R., 2024. Co-phylogeny of a hyper-symbiotic system: endosymbiotic bacteria (Gammaproteobacteria), chewing lice (Insecta: Phthiraptera) and birds (Passeriformes). Mol. Phylogenet. Evol. 190, 107957.

 

Grossi, A.A., Lee, M.B., Tian, C., Zou, F., Choi, C.Y., Gustafsson, D.R., 2023. Host migration and size do not influence the prevalence of most chewing lice (Phthiraptera: amblycera and Ischnocera) on shorebirds (Aves: Charadriiformes) across the world. Diversity 15, 200.

 

Gustafsson, D.R., Lei, L., Luo, K., Chu, X., Zhao, X., Zhang, Q., et al., 2019. Chewing lice from high-altitude and migrating birds in Yunnan, China, with descriptions of two new species of Guimaraesiella. Med. Vet. Entomol. 33, 407–419.

 

Gustafsson, D.R., Olsson, U., 2012. The “very thankless task”: revision of Lunaceps Clay and Meinertzhagen, 1939 (Insecta: Phthiraptera: Ischnocera: Philopteridae), with descriptions of six new species and one new subspecies. Zootaxa 3377, 1–85.

 

Gustafsson, D.R., Olsson, U., 2017. Unexpected distribution patterns of Carduiceps feather lice (Phthiraptera: Ischnocera: Philopteridae) on sandpipers (Aves: Charadriiformes: Scolopacidae). Syst. Entomol. 42, 509–522.

 

Hafner, M.S., Sudman, P.D., Villablanca, F.X., Spradling, T.A., Demastes, J.W., Nadler, S.A., 1994. Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265, 1087–1090.

 

Hillgarth, N., 1996. Ectoparasite transfer during mating in ringed-necked pheasants Phasianus colchicus. J. Avian Biol. 27, 260–262.

 

Hopkins, G.H.E., Timmermann, G., 1954. A revision of the species of Quadraceps (Mallophaga) parasitic on Tringinae. Trans. R. Ent. Soc. Lond. 105, 131–150.

 

Husník, F., Chrudimský, T., Hypša, V., 2011. Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches. BMC Biol. 9, 87.

 

Husnik, F., McCutcheon, J.P., 2016. Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. Proc. Natl. Acad. Sci. U.S.A. 113, E5416–E5424.

 

Johnson, K.P., Shreve, S.M., Smith, V.S., 2012. Repeated adaptive divergence of microhabitat specialization in avian feather lice. BMC Biol. 10, 52.

 

Joseph, V.R., Vakayil, A., 2022. SPlit: an optimal method for data splitting. Technometrics 64, 166–176.

 

Kumar, S., Stecher, G., Tamura, K., 2021. MEGA11: molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38, 3022–3027.

 

Lee, L.I., Tan, D.J.X., Obona, J., Gustafsson, D.R., Ang, Y., Meier, R., 2022. Hitchhiking into the future on a fly: toward a better understanding of phoresy and avian louse evolution (Phthiraptera) by screening bird carcasses for phoretic lice on hippoboscid flies (Diptera). Syst. Entomol. 47, 420–429.

 

Lee, P.L.M., Clayton, D.H., 1995. Population biology of swift (Apus apus) ectoparasites in relation to host reproductive success. Ecol. Entomol. 20, 43–50.

 

MacKinnon, J., Phillipps, K., 2000. A Field Guide to the Birds of China. Oxford University Press, Oxford.

 

Marshall, A., 1981. The Ecology of Ectoparasitic Insects. Academic Press, London.

 

McCutcheon, J.P., Moran, N.A., 2012. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10, 13–26.

 

Michalik, A., Franco, D.C., Kobiałka, M., Szklarzewicz, T., Stroinski, A., Łukasik, P., 2021. Alternative transmission patterns in independently acquired nutritional cosymbionts of Dictyopharidae planthoppers. mBio 12, e0122821.

 

Nováková, E., Hypša, V., 2007. A new Sodalis lineage from bloodsucking fly Craterina melbae (Diptera, Hippoboscoidea) originated independently of the tsetse flies symbiont Sodalis glossinidius. FEMS Microbiol. Lett. 269, 131–135.

 
R Core Team, 2018. R: A Language and Environment for statistical computing. Foundation for Statistical Computing. https://www.r-project.org/.
 

Rambaut, A., Drummond, A.J., Xie, D., Baele, G., Suchard, M.A., 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901–904.

 

Ries, E., 1931. Die symbiose der läuse und federlinge. Z. Morph. Okol. Tiere 20, 233–367.

 

Rubin, B.E.R., Sanders, J.G., Turner, K.M., Pierce, N.E., Kocher, S.D., 2018. Social behaviour in bees influences the abundance of Sodalis (Enterobacteriaceae) symbionts. R. Soc. Open Sci. 5, 180369.

 

Santos-Garcia, D., Silva, F.J., Morin, S., Dettner, K., Kuechler, S.M., 2017. The all-rounder Sodalis: a new bacteriome-associated endosymbiont of the Lygaeoid Bug Henestaris halophilus (Heteroptera: Henestarinae) and a critical examination of its evolution. Genome Biol. Evol. 9, 2893–2910.

 

Saridaki, A., Bourtzis, K., 2010. Wolbachia: more than just a bug in insects genitals. Curr. Opin. Microbiol. 13, 67–72.

 

Smith, W.A., Oakeson, K.F., Johnson, K.P., Reed, D.L., Carter, T., Smith, K.L., et al., 2013. Phylogenetic analysis of symbionts in feather-feeding lice of the genus Columbicola: evidence for repeated symbiont replacements. BMC Evol. Biol. 13, 109.

 

Šochová, E., Husník, F., Nováková, E., Halajian, A., Hypša, V., 2017. Arsenophonus and Sodalis replacements shape evolution of symbiosis in louse flies. PeerJ 5, e4099.

 

Suchard, M.A., Lemey, P., Baele, G., Ayres, D.L., Drummond, A.J., Rambaut, A., 2018. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4, vey016.

 

Sweet, A.D., Browne, D.R., Hernandez, A.G., Johnson, K.P., Cameron, S.L., 2023. Draft genome assemblies of the avian louse Brueelia nebulosa and its associates using long-read sequencing from an individual specimen. G3 Gen. Genom. Genet. 13, jkad030.

 

Timmermann, G., 1950. Saemundssonia meridiana n. sp., eine bemerkenswerte neue Mallophagenart von Sterna anaethetus Scopoli. Parasitol. News 1, 1–4.

 

Timmermann, G., 1952. Revision der bei Seeschwalben schmarotzenden Kletterfederlinge der Gattung Quadraceps. Zool. Anz. 148, 71–87.

 

Timmermann, G., 1954. A revision of the genus Carduiceps Clay & meinertzhagen, 1939 (mallophaga). Ann. Mag. Nat. Hist. 12, 40–48.

 

Toju, H., Tanabe, A.S., Notsu, Y., Sota, T., Fukatsu, T., 2013. Diversification of endosymbiosis: replacements, co-speciation and promiscuity of bacteriocyte symbionts in weevils. ISME J. 7, 1378–1390.

 

Wernegreen, J.J., 2015. Endosymbiont evolution: predictions from theory and surprises from genomes. Ann. N. Y. Acad. Sci. 1360, 16–35.

 

Werren, J.H., Baldo, L., Clark, M.E., 2008. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6, 741–751.

 

Wilson, A.C.C., Ashton, P.D., Calevro, F., Charles, H., Colella, S., Febvay, G., et al., 2010. Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol. Biol. 19, 249–258.

Avian Research
Article number: 100206

{{item.num}}

Comments on this article

Go to comment

< Back to all reports

Review Status: {{reviewData.commendedNum}} Commended , {{reviewData.revisionRequiredNum}} Revision Required , {{reviewData.notCommendedNum}} Not Commended Under Peer Review

Review Comment

Close
Close
Cite this article:
Grossi AA, Zhang M, Zou F, et al. Bird species (Charadriiformes) does not impact endosymbiotic bacteria (Gammaproteobacteria) of their ectoparasites (Insecta: Phthiraptera: Ischnocera). Avian Research, 2024, 15(4): 100206. https://doi.org/10.1016/j.avrs.2024.100206

114

Views

2

Downloads

0

Crossref

0

Web of Science

0

Scopus

0

CSCD

Altmetrics

Received: 29 November 2023
Revised: 25 August 2024
Accepted: 26 August 2024
Published: 30 August 2024
© 2024 The Authors.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).