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Avian Haemosporidian (Plasmodium and Haemoproteus) Status in Two Bird Groups (Old-World Flycatchers and Thrushes) of India and Their Phylogenetic Relationships with Other Lineages of the World

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Abstract

Purpose

Avian haemosporidian may affect the host from body damage to the extinction of a population. Knowledge of their status may help in future avifauna conservation plans. Hence, their status in two bird groups of India and their phylogenetic relationships with other known lineages of the world were examined.

Methods

Cytochrome b gene sequences (479 bp) generated from India and available at MalAvi database were used to study the avian haemosporidian prevalence and phylogenetic analysis of lineages at local and world levels.

Results

One common (COLL2) and only once in the study (CYOPOL01, CHD01, CYORUB01, EUMTHA01, GEOCIT01) haemosporidian lineages were discovered. 5.88% prevalence of haemosporidian infection was found in 102 samples belonging to 6 host species. Haemoproteus prevalence was 4.90% across five host species (Phylloscopus trochiloides, Cyornis poliogenys, C. hainanus dialilaemus, C. rubeculoides, Eumiyas thalassinus) and Plasmodium prevalence was 0.98% in Geokichla citrina. Spatial phylogeny at the global level showed that COLL2 lineage, found in C. poliogenys in India, was genetically identical to H. pallidus lineages (COLL2) in parts of Africa, Europe, North America, Malaysia, and the Philippines. The Plasmodium lineage (GEOCIT01) was related to PADOM16 in Egypt, but the sequences were only 93.89% alike.

Conclusions

Four new lineages of Haemoproteus and one of Plasmodium were reported. COLL2 similarity with other H. pallidus lineages may suggest their hosts as possible infection sources.

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Data Availability

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

References

  1. Atkinson CT, Van RC (1991) Pathogenicity and epizootiology of avian haematozoa. Plasmodium, Leucocytozoon, and Haemoproteus. In: Loye JE, Zuk M (eds) Bird-parasite interactions ecology, evolution, and behaviour. Oxford University Press, Oxford, pp 19–48

    Google Scholar 

  2. Valkiunas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton Florida, p 932

    Google Scholar 

  3. Ilgunas M, Bukauskaite D, Palinauskas V, Iezhova T, Fragner K, Platonova E, Weissenböck H, Valki unas G (2019) Patterns of Plasmodium homocircumflexum virulence in experimentally infected passerine birds. Malar J 18:174

    Article  PubMed  PubMed Central  Google Scholar 

  4. Muriel J, Marzal A, Magallanes S, García-Longoria L, Suarez-Rubio M, Bates PJJ, Lin HH, Soe AN, Oo KS, Aye AA et al (2021) Prevalence and diversity of avian haemosporidians may vary with anthropogenic disturbance. Diversity 13:111

    Article  Google Scholar 

  5. Valkiunas G, Atkinson CT (2020) Introduction to life cycles, taxonomy, distribution, and basic research techniques. In: Santiago-Alarcon D, Marzal A (eds) avian malaria and related parasites in the tropics. Springer International Publishing, Cham, Switzerland, pp 45–80

    Chapter  Google Scholar 

  6. Asghar M, Hasselquist D, Hansson B, Zehtindjiev P, Westerdahl H, Bensch S (2015) Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347:436–438

    Article  CAS  PubMed  Google Scholar 

  7. Martínez-de la Puente J, Merino S, Tomás G, Moreno J, Morales J, Lobato E, García-Fraile S, Belda EJ (2010) The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment. Biol Lett 6:663–665

    Article  Google Scholar 

  8. Marzal A, Balbontín J, Reviriego M, García-Longoria L, Relinque C, Hermosell IG, Magallanes S, López-Calderón C, De Lope F, Møller AP (2016) A longitudinal study of age-related changes in Haemoproteus infection in a passerine bird. Oikos 125:1092–1099

    Article  Google Scholar 

  9. Marzal A, De Lope F, Navarro C, Møller AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142:541–545

    Article  PubMed  Google Scholar 

  10. Merino S, Moreno J, Sanz JJ, Arriero E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc R Soc B Biol Sci 267:2507–2510

    Article  CAS  Google Scholar 

  11. Marzal A, Bensch S, Reviriego M, Balbontin J, De Lope F (2008) Effects of malaria double infection in birds: one plus one is not two. J Evol Biol 21:979–987

    Article  CAS  PubMed  Google Scholar 

  12. Palinauskas V, Valkiunas G, Bolshakov CV, Bensch S (2008) Plasmodium relictum (lineage P-SGS1): Effects on experimentally infected passerine birds. Exp Parasitol 120:372–380

    Article  PubMed  Google Scholar 

  13. Lapointe DA, Atkinson CT, Samuel MD (2012) Ecology and conservation biology of avian malaria. Ann N Y Acad Sci 1249:211–226

    Article  PubMed  Google Scholar 

  14. Marzal A, Garcia-Longoria L (2020) The role of malaria parasites in invasion biology. Avian malaria and related parasites in the tropics. Springer International Publishing Cham, Switzerland, pp 487–512

    Chapter  Google Scholar 

  15. Rahmana A R Bird diversity of India. http://bnhsenvis.nic.in/files/Bird_Diversity_Popular_Lecture.pdf

  16. Farah I (2017) Exploring host and geographical shifts in transmission of haemosporidians in a Palaearctic passerine wintering in India. J Ornithol 158:869–874. https://doi.org/10.1007/s10336-017-1444-9

    Article  Google Scholar 

  17. Gupta P, Vishnudas CK, Ramakrishnan U, Robin VV, Dharmarajan G (2019) Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical skyisland archipelago. Proc R Soc B 286:20190439. https://doi.org/10.1098/rspb.0439

    Article  PubMed  PubMed Central  Google Scholar 

  18. Bensch S, Hellgren O, Perez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358. https://doi.org/10.1111/j.1755-0998.2009.02692.x

    Article  PubMed  Google Scholar 

  19. Ricklefs RE, Fallon SM (2002) Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London. Series B Biological Sciences 269: 885–892

  20. Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce M, Thane AK, Carter PAT, Robert FC (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol 13:3829–3844

    Article  PubMed  Google Scholar 

  21. Marzal A, Ricklefs RE, Valkiunas G, Albayrak T, Arriero E, Bonneaud C, Czirják GA, Ewen J, Hellgren O, Hořáková D, Iezhova TA, Jensen H, Križanauskienė A, Lima MR, de Lope F, Magnussen E, Martin LB, Møller AP, Palinauskas V, Pap PL, Pérez-Tris J, Sehgal RNM, Soler M, Szöllősi E, Westerdahl H, Zetindjiev P, Bensch S (2011) Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS ONE 6(7):e21905. https://doi.org/10.1371/journal.pone.0021905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Jia T, Huang X, Valkiūnas G, Yang M, Zheng C, Tianchun Pu, Yanyun Zhang Lu, Dong XS, Zhang C (2018) Malaria parasites and related haemosporidians cause mortality in cranes: a study on the parasites diversity, prevalence and distribution in Beijing Zoo. Malar J 17:234. https://doi.org/10.1186/s12936-018-2385-3

    Article  PubMed  PubMed Central  Google Scholar 

  23. Gil-Vargas DL, Sedano-Cruz RE (2019) Genetic variation of avian malaria in the tropical Andes: a relationship with the spatial distribution of hosts. Malar J 18:129. https://doi.org/10.1186/s12936-019-2699-9

    Article  PubMed  PubMed Central  Google Scholar 

  24. Bensch S, Stjernman M, Ostman HDO, Hansson B, Westerdahl H, Pinheiro RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc London B Biol Sci 267:1583–1589

    Article  CAS  Google Scholar 

  25. http://creagrus.home.montereybay.com/muscicapids.html

  26. https://en.wikipedia.org/wiki/Thrush_(bird);

  27. Winkler DW, Billerman SM, Lovette IJ (2020) Old World Flycatchers (Muscicapidae), version 10. In: Billerman SM, Keeney BK, Rodewald PG, Schulenberg TS (eds) Birds of the World. Cornell Lab of Ornithology, Ithaca

    Google Scholar 

  28. Levin II, Colborn RE, Kim D, Perlut NG, Renfrew RB, Parker PG (2016) Local parasite lineage sharing in temperate grassland birds provides clues about potential origins of Galapagos avian Plasmodium. Ecol Evol 6:716–726

    Article  PubMed  PubMed Central  Google Scholar 

  29. Singh A, Gupta SK, Alström P, Mohan D, Hooper DM, Kumar RS, Bhatt D, Singh P, Price TD (2019) Taxonomy of cryptic species in the Cyornis rubeculoides complex in the Indian subcontinent. Ibis 162(3):924–935. https://doi.org/10.1111/ibi.12735

    Article  Google Scholar 

  30. Singh A, Kumar A, Kumar RS, Bhatt D, Gupta SK (2017) Amplification of mtDNA control region in opportunistically collected bird samples belonging to nine families of the order Passeriformes. Mitochondrial DNA Part B 2(1):99–100. https://doi.org/10.1080/23802359.2017.1289342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hellgren O, Krizanauskiene A, Valkiunas G, Bensch S (2017) Diversity and phylogeny of mitochondrial cytochrome b lineages from six morphospecies of avian Haemoproteus (Haemosporida, Haemoproteidae). J Parasitol 93:889–896

    Article  Google Scholar 

  32. Tan T, M C, Nelson J S, H C Ng, R C Y Ting, and U A K Kara, (1997) Direct PCR amplification and sequence analysis of extra chromosomal Plasmodium DNA from dried blood spots. Acta Trop 68:105–114

    Article  CAS  PubMed  Google Scholar 

  33. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  34. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214

    Article  CAS  PubMed  Google Scholar 

  35. Hellgren O (2005) The occurrence of haemosporidian parasites in the Fennoscandian bluethroat (Luscinia svecica) population. J Ornithol 146:55–60

    Article  Google Scholar 

  36. Chagas CRF, Valkiūnas G, de Oliveira GL, Monteiro EF, Guida FJV, Simões RF, Rodrigues PT, de Albuquerque Luna EJ, Kirchgatter K (2017) Diversity and distribution of avian malaria and related haemosporidian parasites in captive birds from a Brazilian megalopolis. Malar J 16:83

    Article  PubMed  PubMed Central  Google Scholar 

  37. Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, Heled J, Jones G, Kühnert D, De Maio N, Matschiner M, Fábio K, Mendes Nicola F, Müller Huw A, Ogilvie L, du Plessis A, Popinga AR, Rasmussen D, Siveroni I, Suchard MA, Chieh-Hsi W, Xie D, Zhang C, Stadler T, Drummond AJ (2019) BEAST 25 An advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 15(4):e1006650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 17. Syst Biol. https://doi.org/10.1093/sysbio/syy032

    Article  PubMed  PubMed Central  Google Scholar 

  39. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Rambaut A (2018) FigTree v1.4.4, A Graphical Viewer of Phylogenetic Trees. Available from 〈http://tree.bio.ed.ac.uk/software/figtree/〉.

  41. Bouckaert R (2016) Phylogeography by diffusion on a sphere: whole world phylogeography. PeerJ 4:e2406. https://doi.org/10.7717/peerj.2406

    Article  PubMed  PubMed Central  Google Scholar 

  42. Filip B, Guy B, Bram V, Suchard Marc A, Andrew R, Philippe L (2016) SpreaD3: interactive visualisation of spatiotemporal history and trait evolutionary processes. Mol Biol Evol 33(8):2167–2169. https://doi.org/10.1093/molbev/msw082

    Article  CAS  Google Scholar 

  43. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. BirdLife International (2017) Cyornis rubeculoides (amended version of 2016 assessment) The IUCN Red List of Threatened Species 2017: e.T103761873A111163294. https://doi.org/10.2305/IUCN.UK.2017-1.RLTS.T103761873A111163294.en. Downloaded on 25 July 2020

  45. BirdLife International. Cyornis poliogenys (2018) The IUCN Red List of Threatened Species. e.T22709527A131953768. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22709527A131953768.en. Downloaded on 25 July 2020

  46. Aparup D, Anvikara AR, Catorb LJ, Dhimana RC, Eapenc A, Mishraa N, Nagpala BN, Nandaa N, Raghavendraa K, Readd AF, Sharmae SK, Singha OP, Singha V, Sinnisf P, Srivastavag HC, Sullivanh SA, Suttonh PL, Thomasb MB, Carltonh JM, Valecha N (2012) Malaria in India: the center for the study of complex malaria in India. Acta Trop 121(3):267–273. https://doi.org/10.1016/j.actatropica.2011.11.008

    Article  Google Scholar 

  47. Foster WA, Walker ED (2002) MOSQUITOES (Culicidae) (Eds). Gary mullen, lance durden medical and veterinary entomology. Academic Press, Cambridge, pp 203–262

    Chapter  Google Scholar 

  48. Pigeault R, Vézilier J, Cornet S, Zélé F, Nicot A, Perret P, Gandon S (2015) Rivero A (2014) avian malaria: a new lease of life for an old experimental model to study the evolutionary ecology of Plasmodium. Phil Trans R Soc B 370:20140300. https://doi.org/10.1098/rstb.2014.0300

    Article  PubMed  PubMed Central  Google Scholar 

  49. Adie MRS and Adie JR (1912) Note of an inquiry into malaria and mosquitoes in the Kashmir valley. The Indian Medical Gazette 1913 Page 341

  50. Dar TH (2018) Faunistic studies on the diversity and distribution of mosquitoes of the high altitude Himalayan Region Jammu and Kashmir. A Ph. D thesis submitted to the Pondicherry University. URI: http://hdl.handle.net/10603/284347

  51. Puteri R, Abd AM, Coleman GT, Irwin PJ, Traub RJ (2011) Hippobosca longipennis-a potential intermediate host of a species of Acanthocheilonema in dogs in northern India. Parasit Vectors 4:143

    Article  Google Scholar 

  52. Sikha G, Uttaran M, Abhijit M, Chaudhuri Prasanta K (2008) Biting flies of the genus Homohelea of India (Diptera: Ceratopogonidae) 2009. Folia Heyrovskyana series A 16(4):91–106 (ed March 31 2009 ISSN 1801-7142)

    Google Scholar 

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Acknowledgements

The current study was part of the project under UGC-Dr. D.S. Kothari Postdoctoral Fellowship Scheme, UGC awarded to the first author (BL/16-17/0151) from March 2017 to March 2020. We acknowledge the Director and Dean, WII for their support. We thank the National Institute of Malaria Research, Dwarka, New Delhi, for sparing the positive Plasmodium DNA sample for the standardization work and the Director, Indian Institute of Integrative Medicine, CSIR, Jammu, for allowing us to carry out the standardization work of this project. We sincerely thank Professor Trevor Price, the University of Chicago, for his generous support. We thank the Forest department of Union Territory of Jammu and Kashmir, Himachal Pradesh, Uttarakhand, Sikkim, Arunachal Pradesh, Mizoram, Andhra Pradesh, and Meghalaya for granting permission for sample collection.

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11686_2022_626_MOESM1_ESM.jpg

Supplementary file1 Cytochrome b gene (479 bp) [24] sequence comparison for the lineages from MalAvi database (COLL2 and PFC1) and from the current study (COLL2 (LM10), CYOPOL01 (LM6), GEOCIT01 (LM16), CHD01 (AS 86), CYORUB01 (AS91) and EUMTHA01 ( AS102)). Dots represent the common nucleotides. (JPG 529 KB)

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Vipin, Singh, A., Sharma, V. et al. Avian Haemosporidian (Plasmodium and Haemoproteus) Status in Two Bird Groups (Old-World Flycatchers and Thrushes) of India and Their Phylogenetic Relationships with Other Lineages of the World. Acta Parasit. 67, 1756–1766 (2022). https://doi.org/10.1007/s11686-022-00626-1

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