Skip to main content
Top
Published in: Malaria Journal 1/2021

Open Access 01-12-2021 | Malaria | Research

Low MSP-1 haplotype diversity in the West Palearctic population of the avian malaria parasite Plasmodium relictum

Authors: Olof Hellgren, Victor Kelbskopf, Vincenzo A. Ellis, Arif Ciloglu, Mélanie Duc, Xi Huang, Ricardo J. Lopes, Vanessa A. Mata, Sargis A. Aghayan, Abdullah Inci, Sergei V. Drovetski

Published in: Malaria Journal | Issue 1/2021

Login to get access

Abstract

Background

Although avian Plasmodium species are widespread and common across the globe, limited data exist on how genetically variable their populations are. Here, the hypothesis that the avian blood parasite Plasmodium relictum exhibits very low genetic diversity in its Western Palearctic transmission area (from Morocco to Sweden in the north and Transcaucasia in the east) was tested.

Methods

The genetic diversity of Plasmodium relictum was investigated by sequencing a portion (block 14) of the fast-evolving merozoite surface protein 1 (MSP1) gene in 75 different P. relictum infections from 36 host species. Furthermore, the full-length MSP1 sequences representing the common block 14 allele was sequenced in order to investigate if additional variation could be found outside block 14.

Results

The majority (72 of 75) of the sequenced infections shared the same MSP1 allele. This common allele has previously been found to be the dominant allele transmitted in Europe.

Conclusion

The results corroborate earlier findings derived from a limited dataset that the globally transmitted malaria parasite P. relictum exhibits very low genetic diversity in its Western Palearctic transmission area. This is likely the result of a recent introduction event or a selective sweep.
Literature
1.
go back to reference Drummond AJ, Rambaut A, Shapiro B, Pybus OG. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol. 2005;22:1185–92.CrossRef Drummond AJ, Rambaut A, Shapiro B, Pybus OG. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol. 2005;22:1185–92.CrossRef
2.
go back to reference Heled J, Drummond AJ. Bayesian inference of population size history from multiple loci. Bmc Evol Biol. 2008;8:289.CrossRef Heled J, Drummond AJ. Bayesian inference of population size history from multiple loci. Bmc Evol Biol. 2008;8:289.CrossRef
3.
go back to reference Miao M, Yang Z, Patch H, Huang Y, Escalante AA, Cui L. Plasmodium vivax populations revisited: mitochondrial genomes of temperate strains in Asia suggest ancient population expansion. BMC Evol Biol. 2012;12:22.CrossRef Miao M, Yang Z, Patch H, Huang Y, Escalante AA, Cui L. Plasmodium vivax populations revisited: mitochondrial genomes of temperate strains in Asia suggest ancient population expansion. BMC Evol Biol. 2012;12:22.CrossRef
4.
go back to reference Rachowicz LJ, Hero J, Alford RA, Taylor JW, Morgan JAT, Vredenburg VT, et al. The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conserv Biol. 2005;19:1441–8.CrossRef Rachowicz LJ, Hero J, Alford RA, Taylor JW, Morgan JAT, Vredenburg VT, et al. The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conserv Biol. 2005;19:1441–8.CrossRef
5.
go back to reference Moya A, Holmes EC, González-Candelas F. The population genetics and evolutionary epidemiology of RNA viruses. Nat Rev Microbiol. 2004;2:279–88.CrossRef Moya A, Holmes EC, González-Candelas F. The population genetics and evolutionary epidemiology of RNA viruses. Nat Rev Microbiol. 2004;2:279–88.CrossRef
6.
go back to reference Morgan JAT, Vredenburg VT, Rachowicz LJ, Knapp RA, Stice MJ, Tunstall T, et al. Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proc Natl Acad Sci USA. 2007;104:13845–50.CrossRef Morgan JAT, Vredenburg VT, Rachowicz LJ, Knapp RA, Stice MJ, Tunstall T, et al. Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proc Natl Acad Sci USA. 2007;104:13845–50.CrossRef
7.
go back to reference Bensch S, Perez-Tris J, Waldenstrom J, Hellgren O. Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution. 2004;58:1617–21.CrossRef Bensch S, Perez-Tris J, Waldenstrom J, Hellgren O. Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution. 2004;58:1617–21.CrossRef
8.
go back to reference Valkiunas G. Avian malaria parasites and other haemosporidia. New York: CRC; 2005. Valkiunas G. Avian malaria parasites and other haemosporidia. New York: CRC; 2005.
9.
go back to reference Bensch S, Hellgren O, Pérez-Tris J. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour. 2009;9:1353–8.CrossRef Bensch S, Hellgren O, Pérez-Tris J. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour. 2009;9:1353–8.CrossRef
10.
go back to reference Stephens R, Culleton RL, Lamb TJ. The contribution of Plasmodium chabaudi to our understanding of malaria. Trends Parasitol. 2012;28:73–82.CrossRef Stephens R, Culleton RL, Lamb TJ. The contribution of Plasmodium chabaudi to our understanding of malaria. Trends Parasitol. 2012;28:73–82.CrossRef
11.
go back to reference Rivero A, Gandon S. Evolutionary ecology of avian malaria: past to present. Trends Parasitol. 2018;34:712–26.CrossRef Rivero A, Gandon S. Evolutionary ecology of avian malaria: past to present. Trends Parasitol. 2018;34:712–26.CrossRef
12.
go back to reference Pigeault R, Vézilier J, Cornet S, Zélé F, Nicot A, Perret P, et al. Avian malaria: a new lease of life for an old experimental model to study the evolutionary ecology of Plasmodium. Philos Trans R Soc Lond B Biol Sci. 2015;370:20140300.CrossRef Pigeault R, Vézilier J, Cornet S, Zélé F, Nicot A, Perret P, et al. Avian malaria: a new lease of life for an old experimental model to study the evolutionary ecology of Plasmodium. Philos Trans R Soc Lond B Biol Sci. 2015;370:20140300.CrossRef
13.
go back to reference Videvall E. Genomic advances in avian malaria research. Trends Parasitol. 2019;35:254–66.CrossRef Videvall E. Genomic advances in avian malaria research. Trends Parasitol. 2019;35:254–66.CrossRef
14.
go back to reference Videvall E, Cornwallis CK, Ahren D, Palinauskas V, Valkiūnas G, Hellgren O. The transcriptome of the avian malaria parasite Plasmodium ashfordi displays host-specific gene expression. Mol Ecol. 2017;26:2939–58.CrossRef Videvall E, Cornwallis CK, Ahren D, Palinauskas V, Valkiūnas G, Hellgren O. The transcriptome of the avian malaria parasite Plasmodium ashfordi displays host-specific gene expression. Mol Ecol. 2017;26:2939–58.CrossRef
15.
go back to reference Böhme U, Otto TD, Cotton JA, Steinbiss S, Sanders M, Oyola SO, et al. Complete avian malaria parasite genomes reveal features associated with lineage-specific evolution in birds and mammals. Genome Res. 2018;28:547–60.CrossRef Böhme U, Otto TD, Cotton JA, Steinbiss S, Sanders M, Oyola SO, et al. Complete avian malaria parasite genomes reveal features associated with lineage-specific evolution in birds and mammals. Genome Res. 2018;28:547–60.CrossRef
16.
go back to reference Garcia-Longoria L, Palinauskas V, Ilgūnas M, Valkiūnas G, Hellgren O. Differential gene expression of Plasmodium homocircumflexum (lineage pCOLL4) across two experimentally infected passerine bird species. Genomics. 2020;112:2857–65.CrossRef Garcia-Longoria L, Palinauskas V, Ilgūnas M, Valkiūnas G, Hellgren O. Differential gene expression of Plasmodium homocircumflexum (lineage pCOLL4) across two experimentally infected passerine bird species. Genomics. 2020;112:2857–65.CrossRef
17.
go back to reference Barrow LN, Allen JM, Huang X, Bensch S, Witt CC. Genomic sequence capture of haemosporidian parasites: methods and prospects for enhanced study of host-parasite evolution. Mol Ecol Resour. 2018;19:400–10.CrossRef Barrow LN, Allen JM, Huang X, Bensch S, Witt CC. Genomic sequence capture of haemosporidian parasites: methods and prospects for enhanced study of host-parasite evolution. Mol Ecol Resour. 2018;19:400–10.CrossRef
18.
go back to reference Huang X, Hansson R, Palinauskas V, Valkiūnas G, Hellgren O, Bensch S. The success of sequence capture in relation to phylogenetic distance from a reference genome: a case study of avian haemosporidian parasites. Int J Parasitol. 2018;48:947–54.CrossRef Huang X, Hansson R, Palinauskas V, Valkiūnas G, Hellgren O, Bensch S. The success of sequence capture in relation to phylogenetic distance from a reference genome: a case study of avian haemosporidian parasites. Int J Parasitol. 2018;48:947–54.CrossRef
19.
go back to reference Valkiūnas G, Ilgunas M, Bukauskaite D, Fragner K, Weissenböck H, Atkinson CT, et al. Characterization of Plasmodium relictum, a cosmopolitan agent of avian malaria. Malar J. 2018;17:184.CrossRef Valkiūnas G, Ilgunas M, Bukauskaite D, Fragner K, Weissenböck H, Atkinson CT, et al. Characterization of Plasmodium relictum, a cosmopolitan agent of avian malaria. Malar J. 2018;17:184.CrossRef
20.
go back to reference Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, et al. Global phylogeographic limits of Hawaii’s avian malaria. Proc Biol Sci. 2006;273:2935–44.PubMedPubMedCentral Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, et al. Global phylogeographic limits of Hawaii’s avian malaria. Proc Biol Sci. 2006;273:2935–44.PubMedPubMedCentral
21.
go back to reference Hellgren O, Atkinson CT, Bensch S, Albayrak T, Dimitrov D, Ewen JG, et al. Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography. 2015;38:842–50.CrossRef Hellgren O, Atkinson CT, Bensch S, Albayrak T, Dimitrov D, Ewen JG, et al. Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography. 2015;38:842–50.CrossRef
22.
go back to reference Vanriper C, Vanriper SG, Goff ML, Laird M. The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr. 1986;56:327–44.CrossRef Vanriper C, Vanriper SG, Goff ML, Laird M. The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr. 1986;56:327–44.CrossRef
23.
go back to reference Bueno MG, Lopez RPG, Menezes RMT, Costa-Nascimento M, Lima G, Araújo RA, et al. Identification of Plasmodium relictum causing mortality in penguins (Spheniscus magellanicus) from São Paulo Zoo Brazil. Vet Parasitol. 2010;173:123–7.CrossRef Bueno MG, Lopez RPG, Menezes RMT, Costa-Nascimento M, Lima G, Araújo RA, et al. Identification of Plasmodium relictum causing mortality in penguins (Spheniscus magellanicus) from São Paulo Zoo Brazil. Vet Parasitol. 2010;173:123–7.CrossRef
24.
go back to reference Hellgren O, Kutzer M, Bensch S, Valkiūnas G, Palinauskas V. Identification and characterization of the merozoite surface protein 1 (msp1) gene in a host-generalist avian malaria parasite, Plasmodium relictum (lineages SGS1 and GRW4) with the use of blood transcriptome. Malar J. 2013;12:381.CrossRef Hellgren O, Kutzer M, Bensch S, Valkiūnas G, Palinauskas V. Identification and characterization of the merozoite surface protein 1 (msp1) gene in a host-generalist avian malaria parasite, Plasmodium relictum (lineages SGS1 and GRW4) with the use of blood transcriptome. Malar J. 2013;12:381.CrossRef
25.
go back to reference Kadekoppala M, Holder AA. Merozoite surface proteins of the malaria parasite: the MSP1 complex and the MSP7 family. Int J Parasitol. 2010;40:1155–61.CrossRef Kadekoppala M, Holder AA. Merozoite surface proteins of the malaria parasite: the MSP1 complex and the MSP7 family. Int J Parasitol. 2010;40:1155–61.CrossRef
26.
go back to reference Tanabe K, Sakihama N, Rooth I, Björkman A, Färnert A. High frequency of recombination-driven allelic diversity and temporal variation of Plasmodium falciparum msp1 in Tanzania. Am J Trop Med Hyg. 2007;76:1037–45.CrossRef Tanabe K, Sakihama N, Rooth I, Björkman A, Färnert A. High frequency of recombination-driven allelic diversity and temporal variation of Plasmodium falciparum msp1 in Tanzania. Am J Trop Med Hyg. 2007;76:1037–45.CrossRef
27.
go back to reference Bensch S, Hellgren O. The Use of Molecular Methods in Studies of Avian Haemosporidians. In: Santiago-Alarcon D, Marzal R, Alfonso AG, editors. Avian malaria in the tropics. In avian malaria and related parasites in the tropics, ecology, evolution and systematics. Switzerland: Springer; 2020. p. 113–35.CrossRef Bensch S, Hellgren O. The Use of Molecular Methods in Studies of Avian Haemosporidians. In: Santiago-Alarcon D, Marzal R, Alfonso AG, editors. Avian malaria in the tropics. In avian malaria and related parasites in the tropics, ecology, evolution and systematics. Switzerland: Springer; 2020. p. 113–35.CrossRef
28.
go back to reference Mata VA, da Silva LP, Lopes RJ, Drovetski SV. The Strait of Gibraltar poses an effective barrier to host-specialised but not to host-generalised lineages of avian Haemosporidia. Int J Parasitol. 2015;45:711–9.CrossRef Mata VA, da Silva LP, Lopes RJ, Drovetski SV. The Strait of Gibraltar poses an effective barrier to host-specialised but not to host-generalised lineages of avian Haemosporidia. Int J Parasitol. 2015;45:711–9.CrossRef
29.
go back to reference Drovetski SV, Aghayan SA, Mata VA, Lopes RJ, Mode NA, Harvey JA, et al. Does the niche breadth or trade-off hypothesis explain the abundance–occupancy relationship in avian Haemosporidia? Mol Ecol. 2014;23:3322–9.CrossRef Drovetski SV, Aghayan SA, Mata VA, Lopes RJ, Mode NA, Harvey JA, et al. Does the niche breadth or trade-off hypothesis explain the abundance–occupancy relationship in avian Haemosporidia? Mol Ecol. 2014;23:3322–9.CrossRef
30.
go back to reference Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.CrossRef Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.CrossRef
31.
go back to reference Leigh JW, Bryant D. popart: full-feature software for haplotype network construction. Methods Ecol Evol. 2015;6:1110–6.CrossRef Leigh JW, Bryant D. popart: full-feature software for haplotype network construction. Methods Ecol Evol. 2015;6:1110–6.CrossRef
32.
go back to reference Clement M, Snell Q, Walke P, Posada D, Crandall K. TCS: estimating gene genealogies. In: Proceedings of 16th international parallel distributed process symposium. 2002, p 7. Clement M, Snell Q, Walke P, Posada D, Crandall K. TCS: estimating gene genealogies. In: Proceedings of 16th international parallel distributed process symposium. 2002, p 7.
33.
go back to reference Hellgren O, Waldenström J, Bensch S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol. 2004;90:797–802.CrossRef Hellgren O, Waldenström J, Bensch S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol. 2004;90:797–802.CrossRef
34.
go back to reference Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.CrossRef Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.CrossRef
35.
go back to reference Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 2009;37:D539–43.CrossRef Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 2009;37:D539–43.CrossRef
36.
go back to reference Sedlazeck FJ, Rescheneder P, von Haeseler A. NextGenMap: fast and accurate read mapping in highly polymorphic genomes. Bioinformatics. 2013;29:2790–1.CrossRef Sedlazeck FJ, Rescheneder P, von Haeseler A. NextGenMap: fast and accurate read mapping in highly polymorphic genomes. Bioinformatics. 2013;29:2790–1.CrossRef
37.
go back to reference Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–9.CrossRef Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–9.CrossRef
38.
go back to reference Videvall E, Palinauskas V, Valkiūnas G, Hellgren O. Host transcriptional responses to high- and low-virulent avian malaria parasites. Am Nat. 2020;195:1070–84.CrossRef Videvall E, Palinauskas V, Valkiūnas G, Hellgren O. Host transcriptional responses to high- and low-virulent avian malaria parasites. Am Nat. 2020;195:1070–84.CrossRef
39.
go back to reference Dimitrov D, Palinauskas V, Iezhova TA, Bernotienė R, Ilgunas M, Bukauskaite D, et al. Plasmodium spp.: an experimental study on vertebrate host susceptibility to avian malaria. Exp Parasitol. 2015;148:1–16.CrossRef Dimitrov D, Palinauskas V, Iezhova TA, Bernotienė R, Ilgunas M, Bukauskaite D, et al. Plasmodium spp.: an experimental study on vertebrate host susceptibility to avian malaria. Exp Parasitol. 2015;148:1–16.CrossRef
40.
go back to reference Garcia-Longoria L, Hellgren O, Bensch S, Lope FD, Marzal A. Detecting transmission areas of malaria parasites in a migratory bird species. Parasitology. 2015;142:1215–20.CrossRef Garcia-Longoria L, Hellgren O, Bensch S, Lope FD, Marzal A. Detecting transmission areas of malaria parasites in a migratory bird species. Parasitology. 2015;142:1215–20.CrossRef
Metadata
Title
Low MSP-1 haplotype diversity in the West Palearctic population of the avian malaria parasite Plasmodium relictum
Authors
Olof Hellgren
Victor Kelbskopf
Vincenzo A. Ellis
Arif Ciloglu
Mélanie Duc
Xi Huang
Ricardo J. Lopes
Vanessa A. Mata
Sargis A. Aghayan
Abdullah Inci
Sergei V. Drovetski
Publication date
01-12-2021
Publisher
BioMed Central
Keywords
Malaria
Plasmodia
Published in
Malaria Journal / Issue 1/2021
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-021-03799-8

Other articles of this Issue 1/2021

Malaria Journal 1/2021 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.