The global biogeography of avian haemosporidian parasites is characterized by local diversification and intercontinental dispersal

Abstract

The biogeographic histories of parasites and pathogens are infrequently compared with those of free-living species, including their hosts. Documenting the frequency with which parasites and pathogens disperse across geographic regions contributes to understanding not only their evolution, but also the likelihood that they may become emerging infectious diseases. Haemosporidian parasites of birds (parasite genera Plasmodium, Haemoproteus and Leucocytozoon) are globally distributed, dipteran-vectored parasites. To date, over 2000 avian haemosporidian lineages have been designated by molecular barcoding methods. To achieve their current distributions, some lineages must have dispersed long distances, often over water. Here we quantify such events using the global avian haemosporidian database MalAvi and additional records primarily from the Americas. We scored lineages as belonging to one or more global biogeographic regions based on infection records. Most lineages were restricted to a single region but some were globally distributed. We also used part of the cytochrome b gene to create genus-level parasite phylogenies and scored well-supported nodes as having descendant lineages in regional sympatry or allopatry. Descendant sister lineages of Plasmodium, Haemoproteus and Leucocytozoon were distributed in allopatry in 11, 16 and 15% of investigated nodes, respectively. Although a small but significant fraction of the molecular variance in cytochrome b of all three genera could be explained by biogeographic region, global parasite dispersal likely contributed to the majority of the unexplained variance. Our results suggest that avian haemosporidian parasites have faced few geographic barriers to dispersal over their evolutionary history.

Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago

“…For example, three specialist lineages-MONCAC03, MONFAI02, and MONMER02showed signals of co-speciation and have co-diversified with their endemic hosts Montecincla cachinnans, Montecincla fairbanki, and Montecincla meridionalis, respectively (see electronic supplementary material, figure S5). Our results further strengthen the patterns of local diversification of avian haemosporidians observed in other tropical bird communities [49,51]. Broadly, empirical data from other host-parasite systems suggest that parasites tend to be host-specialists in species-rich communities [63].…”

Avian host composition, local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds

“…At the same time, the lack of Parahaemoproteus dispersal from the Atlantic Rain Forest to Tropical and Subtropical Grassland is surprising considering their spatial connectivity, which would be expected to allow the highest number of lineage interchanges (Donoghue & Edwards, 2014). Here, we show that despite having high ecological and geographic dispersal capabilities (Ellis et al, 2015(Ellis et al, , 2019Clark et al, 2018;, Plasmodium and Parahaemoproteus differ with respect to interchange frequency across regions in South America, possibly due to differential host specificity of parasite lineages or differential mobility of avian hosts across biomes with subsequent parasite host range expansion, two hypotheses that warrant future investigation.…”

Climate variation influences host specificity in avian malaria parasites

“…; Ellis et al . ) could be interpreted as evidence that these parasites are indiscriminant host‐generalists capable of infecting an enormous diversity of host species in any given environment. We challenge this assertion by showing that multi‐host avian malaria parasites, even those that infect a high number of avian host species, generally infect phylogenetically clustered subsets of available hosts.…”

“…Many parasites and pathogens can disperse widely across geographical realms and infect distantly related host species, and avian malaria parasites are no exception (P erez-Tris & Bensch 2005;Hellgren et al 2007;Ellis et al 2015;Ricklefs et al 2017;Fecchio et al 2018a,b). Global distributions of several common and potentially invasive Plasmodium lineages Clark et al 2015;Marzal et al 2015;Ellis et al 2018) could be interpreted as evidence that these parasites are indiscriminant host-generalists capable of infecting an enormous diversity of host species in any given environment. We challenge this assertion by showing that multihost avian malaria parasites, even those that infect a high number of avian host species, generally infect phylogenetically clustered subsets of available hosts.…”