Local parasite lineage sharing in temperate grassland birds provides clues about potential origins of Galapagos avian Plasmodium

Abstract

Oceanic archipelagos are vulnerable to natural introduction of parasites via migratory birds. Our aim was to characterize the geographic origins of two Plasmodium parasite lineages detected in the Galapagos Islands and in North American breeding bobolinks (Dolichonyx oryzivorus) that regularly stop in Galapagos during migration to their South American overwintering sites. We used samples from a grassland breeding bird assemblage in Nebraska, United States, and parasite DNA sequences from the Galapagos Islands, Ecuador, to compare to global data in a DNA sequence registry. Homologous DNA sequences from parasites detected in bobolinks and more sedentary birds (e.g., brown‐headed cowbirds Molothrus ater, and other co‐occurring bird species resident on the North American breeding grounds) were compared to those recovered in previous studies from global sites. One parasite lineage that matched between Galapagos birds and the migratory bobolink, Plasmodium lineage B, was the most common lineage detected in the global MalAvi database, matching 49 sequences from unique host/site combinations, 41 of which were of South American origin. We did not detect lineage B in brown‐headed cowbirds. The other Galapagos‐bobolink match, Plasmodium lineage C, was identical to two other sequences from birds sampled in California. We detected a close variant of lineage C in brown‐headed cowbirds. Taken together, this pattern suggests that bobolinks became infected with lineage B on the South American end of their migratory range, and with lineage C on the North American breeding grounds. Overall, we detected more parasite lineages in bobolinks than in cowbirds. Galapagos Plasmodium had similar host breadth compared to the non‐Galapagos haemosporidian lineages detected in bobolinks, brown‐headed cowbirds, and other grassland species. This study highlights the utility of global haemosporidian data in the context of migratory bird–parasite connectivity. It is possible that migratory bobolinks bring parasites to the Galapagos and that these parasites originate from different biogeographic regions representing both their breeding and overwintering sites.

Avian migration and the distribution of malaria parasites in New World passerine birds

“…Each year, hundreds of species of birds leave their tropical and subtropical wintering areas for high‐latitude summer breeding grounds, returning to lower latitudes at the end of the breeding season (Alerstam et al ., ; Faaborg et al ., ). These species are exposed to different parasites in their boreal or temperate breeding areas and in their subtropical or tropical wintering areas, and they potentially could disperse parasites between these areas (Valkiūnas, ; Altizer et al ., ; Levin et al ., ; Smith & Ramey, ; Levin et al ., ), particularly because birds retain parasite infections through the annual cycle, and often for many years (e.g. Atkinson et al ., ).…”

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

“…Migrating avian hosts have also been implicated in moving haemosporidian parasites from mainland areas to islands. For example, avian Plasmodium in the Galapagos Islands likely arrived via a migrating host, the Bobolink (Dolichonyx oryzivorus), which regularly stops over in the Galapagos archipelago during its migration (Levin et al, 2013(Levin et al, , 2016.…”

Haemosporidian parasite community in migrating bobolinks on the Galapagos Islands

“…DNA from the Bobolink blood sampled in Galapagos. Two of the sequences matched the Plasmodium cathemerium lineage SEIAUR01 (GenBank accession number: AY377128 , Loiseau et al, 2013 ), which is common in Bobolinks ( Levin et al, 2013 ) and corresponds to lineage M found in those captured in North America ( Levin et al, 2016 ). The other two sequences match Plasmodium sp.…”

“…In an earlier study, we found Plasmodium parasite lineages B and C, detected in 2 Galapagos passerine species, Small ground finches ( Geospiza fuliginosa ) and Yellow warblers ( Setophaga petechia ), in the blood of Bobolinks sampled on their North American breeding grounds ( Levin et al, 2013 ). We then characterized the geographic origins of these two lineages: Plasmodium lineage B was of South American origin and Plasmodium lineage C was of North American origin, potentially California ( Levin et al, 2016 ). Although these results offer a compelling explanation as to how parasites may have arrived on the Galapagos Islands, we sought more evidence for the role of the Bobolink in Plasmodium transmission to Galapagos resident birds by sampling Bobolinks for haemosporidian parasites in the Galapagos.…”