Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity

Abstract

Knowing the genetic variation that occurs in pathogen populations and how it is distributed across geographical areas is essential to understand parasite epidemiology, local patterns of virulence, and evolution of host‐resistance. In addition, it is important to identify populations of pathogens that are evolutionarily independent and thus ‘free’ to adapt to hosts and environments. Here, we investigated genetic variation in the globally distributed, highly invasive avian malaria parasite Plasmodium relictum, which has several distinctive mitochondrial haplotyps (cyt b lineages, SGS1, GRW11 and GRW4). The phylogeography of P. relictum was accessed using the highly variable nuclear gene merozoite surface protein 1 (MSP1), a gene linked to the invasion biology of the parasite. We show that the lineage GRW4 is evolutionarily independent of GRW11 and SGS1 whereas GRW11 and SGS1 share MSP1 alleles and thus suggesting the presence of two distinct species (GRW4 versus SGS1 and GRW11). Further, there were significant differences in the global distribution of MSP1 alleles with differences between GRW4 alleles in the New and the Old World. For SGS1, a lineage formerly believed to have both tropical and temperate transmission, there were clear differences in MSP1 alleles transmitted in tropical Africa compared to the temperate regions of Europe and Asia. Further, we highlight the occurrence of multiple MSP1 alleles in GRW4 isolates from the Hawaiian Islands, where the parasite has contributed to declines and extinctions of endemic forest birds since it was introduced. This study stresses the importance of multiple independent loci for understanding patterns of transmission and evolutionary independence across avian malaria parasites.

Detecting transmission areas of malaria parasites in a migratory bird species

“…1. * and § represent confirmed active transmission in Africa and Europe, respectively (Hellgren et al 2015). parasites. * and § represent confirmed active transmission in Africa and Europe, respectively (Hellgren et al 2015). parasites.…”

“…The data on the distribution of nuclear MSP1 alleles across the cyt b lineages may facilitate the investigation on the distribution of these malaria parasites across geographical regions (Hellgren et al 2013(Hellgren et al , 2015. A recent study has explored the global phylogeography of the P. relictum based on MSP1 allelic diversity, showing several different MSP1 alleles within the cyt b lineages of SGS1 and GRW4.…”

“…The merozoite surface protein 1 (MSP1) is a gene which shows a high variability (Miller et al 1993) and encodes a protein involved in the attachment of the malaria parasite to the red blood cell (Gerold et al 1996). For example, the SGS1 lineage transmitted in tropical Africa has a different set of MSP1 alleles compared with those transmitted in Europe, suggesting the existence of separate SGS1 populations along the European-African migratory flyways (Hellgren et al 2015). For example, the SGS1 lineage transmitted in tropical Africa has a different set of MSP1 alleles compared with those transmitted in Europe, suggesting the existence of separate SGS1 populations along the European-African migratory flyways (Hellgren et al 2015).…”

Genomic sequence capture of haemosporidian parasites: Methods and prospects for enhanced study of host–parasite evolution

“…First, the species limits of haemosporidian parasites are difficult to define. Some lineages differing by a single nucleotide in the cytb barcode region are considered to be reproductively isolated, biological species (Nilsson et al, ), while others are considered to represent intraspecific variants (Hellgren et al, ; Outlaw & Ricklefs, ). Galen, Nunes, et al () used seven nuclear loci to show that both phenomena occur in Leucocytozoon , confirming the poor resolution of mtDNA for inferring species limits.…”

The malaria parasite Plasmodium relictum in the endemic avifauna of eastern Cuba

“…For all infections identified as P. relictum GRW4 based on mitochondrial sequence, we ran a nested polymerase chain reaction (PCR) assay that targeted a highly variable region of the P. relictum nuclear DNA: the merozoite surface protein (msp1) gene (Hellgren et al. , ). The PCR conditions for amplification of the msp1 gene are described in the Supporting Information.…”