Population structure of avian malaria parasites

Abstract

The geographic distribution of genetic diversity in malaria parasite populations (Apicomplexa: Haemosporida) presumably influences local patterns of virulence and the evolution of host-resistance, but little is known about population genetic structure in these parasites. We assess the distribution of genetic diversity in the partial Domain I of apical membrane antigen 1 (AMA1) in three mtDNA-defined lineages of avian Plasmodium to determine spatial population structure and host-parasite genetic relationships. We find that one parasite lineage is genetically differentiated in association with a single host genus and among some locations, but not with respect to other hosts. Two other parasite lineages are undifferentiated with respect to host species but exhibit geographic differentiation that is inconsistent with shared geographic barriers or with isolation-by-distance. Additional differentiation within two other lineages is unassociated with host species or location; in one case, we tentatively interpret this differentiation as the result of mitochondrial introgression from one of the lineages into a second lineage. More sampling of nuclear genetic diversity within populations of avian Plasmodium is needed to rule out coinfection as a possible confounding factor. If coinfections are not responsible for these findings, further assessment is needed to determine the frequency of mitonuclear discordance and its implications for defining parasite lineages based on mitochondrial genetic variation.

Open research badges: This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at Genbank https://www.ncbi.nlm.nih.gov/genbank/, accession numbers MK965548-MK965653 and MK929797-MK930264.

Keywords: AMA1; Haemoproteus; Haemosporida; Plasmodium; avian malaria; host–parasite genetic relationship; introgression; spatial population structure.

Figure 1

Overall detections of lineages OZ01 (blue triangles), OZ04 (red diamonds), and OZ14 (green circles). OZ01 is broadly distributed in the Neotropics and Nearctic; OZ04 is primarily restricted to the West Indies with limited detection in North and South America; OZ14 is distributed in the eastern United States and locally in the Greater Antilles. All three lineages are known to co‐occur on Jamaica, Hispaniola, and in the Ozarks region of Missouri

Figure 2

Phylogenetic relationships among the lineages assessed here and other Plasmodium species, based on a maximum likelihood phylogeny of the amino acid sequences produced in Mega6. In accordance with Mega6 model selection, the amino acid substitution model LG + G (Le & Gascuel, 2008) was implemented with five gamma categories and 100 bootstrap replicates. Included in the phylogeny are representatives of nine avian and three mammalian malaria species for which AMA1 sequences were available (Genbank accessions KJ722597, KX601270, KX601271, KJ722596, KJ722593, KJ722594, KJ722595, KJ722542, KJ722547, KY905274, ACB55391, and AF352829)

Figure 3

AMA1 sampling localities depicting lineage co‐occurrences and locations of suspected introgression (crosses). Introgressed parasites were detected at seven localities where OZ01 and OZ04 are known to co‐occur and one locality where OZ01 has not been detected (Refugio Boquerón, PR)

Figure 4

Sliding window analysis of nucleotide diversity for OZ01, OZ04, OZ14, and Plasmodium falciparum from Escalante et al. (2001). Window, 30 bp; step size, 9 bp

Figure 5

Median‐joining haplotype networks of AMA1 variation for mitochondrial lineages OZ01 (A), OZ04 (B), and OZ14 (C). Circle size indicates the number of individuals with a given haplotype, color indicates host family/superfamily, and black hash marks indicate mutations. The gray oval in panel A encloses the group primarily infecting Passerina

Figure 6

Median‐joining haplotype networks of AMA1 depicting combined lineages OZ01, OZ04, and OZ14. Circle size indicates the number of individuals with a given haplotype, color indicates mitochondrial lineage designation, and black hash marks indicate mutations

Figure 7

Number of detections by location for lineages OZ01 and OZ04

Figure 8

Number of detections by host species for lineages OZ01 and OZ04

Figure 9

Median‐joining haplotype networks of AMA1 for only introgressed samples. Circle size indicates the number of individuals with a given haplotype, color indicates location, and black hash marks indicate mutations

Figure 10

Median‐joining haplotype network of 51 Plasmodium lucens AMA1 sequences depicting the main group (red) and the divergent group (blue). All samples were recovered from a population of olive sunbirds (Cyanomitra olivacea) in Cameroon (Lauron et al., 2014)