Dynamics of avian haemosporidian assemblages through millennial time scales inferred from insular biotas of the West Indies

Abstract

Although introduced hemosporidian (malaria) parasites (Apicomplexa: Haemosporida) have hastened the extinction of endemic bird species in the Hawaiian Islands and perhaps elsewhere, little is known about the temporal dynamics of endemic malaria parasite populations. Haemosporidian parasites do not leave informative fossils, and records of population change are lacking beyond a few decades. Here, we take advantage of the isolation of West Indian land-bridge islands by rising postglacial sea levels to estimate rates of change in hemosporidian parasite assemblages over a millennial time frame. Several pairs of West Indian islands have been connected and separated by falling and rising sea levels associated with the advance and retreat of Pleistocene continental glaciers. We use island isolation following postglacial sea-level rise, ca. 2.5 ka, to characterize long-term change in insular assemblages of hemosporidian parasites. We find that assemblages on formerly connected islands are as differentiated as assemblages on islands that have never been connected, and both are more differentiated than local assemblages sampled up to two decades apart. Differentiation of parasite assemblages between formerly connected islands reflects variation in the prevalence of shared hemosporidian lineages, whereas differentiation between islands isolated by millions of years reflects replacement of hemosporidian lineages infecting similar assemblages of avian host species.avian malaria | bananaquit | beta diversity | Plasmodium | Haemoproteus I nsular biotas provide natural laboratories for characterizing change in host-parasite relationships over time (1). Haemosporidian parasites (genera Plasmodium and Haemoproteus, among others) are dipteran vector-transmitted protozoans that reproduce clonally in cells of vertebrates and cause symptoms referred to as malaria (2). The few fossils of ancient hemosporidians (3) are insufficient to analyze retrospectively the dynamics of these hostparasite interactions. We have found that hemosporidian parasite assemblages of birds present remarkable geographic heterogeneity in the West Indies, even though common avian host species are widely distributed throughout the archipelago (4). Additionally, the frequencies of individual lineages in assemblages of avian hemosporidian parasites have been observed to vary over periods as short as one decade (5-7). Here, we take advantage of the geographic history of islands in the West Indies to characterize changes in avian hemosporidian parasite assemblages over millennial time scales.During the late Quaternary glaciations, which reached their maximum extent ca. 26 ka, an increase in continental ice volume caused the global sea level to drop by as much as 120 m, exposing land connections between islands lying on shallow banks (8). During periods of sea level lows, organisms could freely disperse between some pairs of present-day islands, tending to homogenize assemblages of birds and, presumably, their pathogens (8). Deglaciation started 7.5-10 ka, and ended...

Neotropical migratory and resident birds occurring in sympatry during winter have distinct haemosporidian parasite assemblages

“…Moreover, our data indicate that host switching rarely occurs between migratory and resident species occurring in sympatry during winter, despite the close phylogenetic relationship between many of the resident and migratory bird species. These patterns are intriguing, as previously published results suggest that haemosporidian parasites switch readily, even between distantly related hosts (Ellis et al, 2015;Ricklefs & Fallon, 2002;Ricklefs et al, 2014), and an analysis of haemosporidian assemblages in the West Indies reported essentially random switching of parasite lineages between host species perceived over millennial time scales (Soares et al, 2017).…”

“…Nonetheless, the geographic and host distributions of OZ14, OZ45, MI05 and KZ01 suggest that despite host mobility between breeding and wintering regions, some lineages transmitted on North American breeding grounds have not established transmission cycles in the Caribbean. Based on descriptions of parasite assemblages in resident hosts in the Caribbean region (Fallon et al, ; Ricklefs et al, ; Soares et al, ), Ecuador (Moens & Pérez‐Tris, ; Svensson‐Coelho et al, ), Colombia (González, Lotta, García, Moncada, & Matta, ; Pulgarín‐R et al, ) and Brazil (Fecchio et al, ), resident birds of the Neotropics appear to be either incompetent or suboptimal hosts for lineages that commonly occur in North America.…”

“…This pattern was consistent across years, and the scarcity of infections among migratory hosts seems to be unlinked to any temporal changes in prevalence observed among resident hosts. For example, even though Haemosporidian parasite prevalence has been reported to vary over time Fallon et al, 2005;Soares et al, 2017), the pattern of low infection rates in over-wintering migrants persisted even in the year with the highest sampled prevalence TA B L E 2 Parameter estimates, standard errors, and p values for the linear mixed effect models testing the differences in prevalence between migratory and resident avian host species sampled in Hispaniola (2014), and even when prevalence in resident hosts varied among years. Moreover, our data indicate that host switching rarely occurs between migratory and resident species occurring in sympatry during winter, despite the close phylogenetic relationship between many of the resident and migratory bird species.…”

“…The lineage KZ01 has been detected 50 times in birds on North American breeding grounds (Ellis et al, 2015), and 14 times in migratory bird species wintering the Yucatán Peninsula, Puerto Rico, and The Bahamas (Ricklefs et al, 2014). Finally, OZ01 is the most broadly distributed lineage within this clade, having been detected in North America 253 times (Ellis et al, 2015), as well as in Ecuador (Svensson-Coelho et al, 2013), the Lesser Antilles Soares et al, 2017), the Yucatan Peninsula, and Jamaica (Ricklefs et al, 2014). Finally, our fourth hypothesis addresses the possibility of high mortality rates of infected individuals during migration.…”

“…Hence, midwinter surveys should detect transmission of parasites from resident to migratory birds within 3 months post arrival in Hispaniola. Because the prevalence of haemosporidian parasites can vary over short time scales (Bensch et al, ; Fallon, Bermingham, & Ricklefs, ; Soares, Latta, & Ricklefs, ), we compare infection prevalence between sampling years.…”