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

Abstract

Understanding why some parasites emerge in novel host communities while others do not has broad implications for human and wildlife health. In the case of haemosporidian blood parasites, epidemic wild bird mortalities on oceanic islands have been linked to Plasmodium spp., but not genera like Haemoproteus . Indeed, Haemoproteus is absent from many oceanic islands. By contrast, birds on continental islands share long coevolutionary histories with both Plasmodium and Haemoproteus , and are thus ideal model systems to elucidate eco-evolutionary endpoints associated with these parasites in oceanic islands. Here, we examine eco-evolutionary dynamics of avian haemosporidian in the Shola sky-island archipelago of the Western Ghats, India. Our analyses reveal that compared to Plasmodium , Haemoproteus lineages were highly host-specific and diversified via co-speciation with their hosts. We show that community structure of host-generalist Plasmodium was primarily driven by geographical factors (e.g. biogeographic barriers), while that of host-specialist Haemoproteus was driven by host species barriers (e.g. phylogenetic distance). Consequently, a few host species can harbour a high diversity of Plasmodium lineages which, in turn, are capable of infecting multiple host species. These two mechanisms can act in concert to increase the risk of introduction, establishment, and emergence of novel Plasmodium lineages in island systems.

Detecting turnover among complex communities using null models: A case study with sky-island haemosporidian parasites

“…These sky islands are defined by high-elevation forested habitats that are geographically isolated by low-elevation, arid habitats. Similar to archipelago systems (Ricklefs and Bermingham 2008), sky islands provide opportunities to study the factors that influence community structure, biogeographic patterns, and evolutionary diversification (Knowles 2001; McCormack et al 2008; Gupta et al 2019; Williamson et al 2019). Avian haemosporidians include the intracellular, protozoan parasites that cause avian malaria, a global disease system that has been associated with epidemics, population declines, and extinction of naïve hosts (Warner 1968; van Riper et al 1986; Atkinson and LaPointe 2009).…”

Host phylogeny matters: Examining sources of variation in infection risk by blood parasites across a tropical montane bird community in India

“…Second, we test the effect of host evolutionary history in explaining variation in avian haemosporidian infection risk not explained by host ecological factors. As mentioned earlier, several studies suggest that Plasmodium is a generalist parasite and Haemoproteus is a relatively specialist parasite [32][33][34], thus we expect that the effects of ecological factors will vary for Plasmodium and Haemoproteus in addition to their intrinsic differences in parasite biology and vector speci city. At the species-level, we expect that: (1) Species that have a lower minimum elevation will have higher Plasmodium prevalence whereas species with a higher minimum elevation will have higher Haemoproteus prevalence (Fig.…”

“…We used bird data and parasite genetic data collected as part of an earlier study, see details in Gupta et al [32]. Brie y, birds were captured using mist-nets at 52 localities across four major Sky Island groups, separated by three biogeographic barriers, spanning 600 km in the southern Western Ghats mountain range during 2011-2013 ( Fig.…”

“…Avian haemosporidians can impose strong selective pressures on bird hosts as they are known to reduce longevity [24], host tness [25,26], individual host condition [27] and have led to severe population declines [28][29][30][31]. Previous research has revealed that avian haemosporidian parasites vary widely in their host range, with Plasmodium lineages often being generalists infecting a broad range of host species and Haemoproteus lineages often being specialists infecting one or few closely related host species [32][33][34] but this pattern is not universal [35,36]. Plasmodium and Haemoproteus parasites also exhibit ecoevolutionary differences, with Plasmodium generally affected by abiotic factors such as spatial proximity and Haemoproteus, primarily affected by biotic factors such as host phylogeny and host ecology [32,37,38].…”

“…Previous research has revealed that avian haemosporidian parasites vary widely in their host range, with Plasmodium lineages often being generalists infecting a broad range of host species and Haemoproteus lineages often being specialists infecting one or few closely related host species [32][33][34] but this pattern is not universal [35,36]. Plasmodium and Haemoproteus parasites also exhibit ecoevolutionary differences, with Plasmodium generally affected by abiotic factors such as spatial proximity and Haemoproteus, primarily affected by biotic factors such as host phylogeny and host ecology [32,37,38]. Given the widespread distribution, diversity and pronounced eco-evolutionary differences between Plasmodium and Haemoproteus, variation in parasite prevalence for the two parasite genera could be affected by different ecological and evolutionary factors in multi-host communities.…”