Rerooting the evolutionary tree of malaria parasites

Abstract

Malaria parasites (Plasmodium spp.) have plagued humans for millennia. Less well known are related parasites (Haemosporida), with diverse life cycles and dipteran vectors that infect other vertebrates. Understanding the evolution of parasite life histories, including switches between hosts and vectors, depends on knowledge of evolutionary relationships among parasite lineages. In particular, inferences concerning time of origin and trait evolution require correct placement of the root of the evolutionary tree. Phylogenetic reconstructions of the diversification of malaria parasites from DNA sequences have suffered from uncertainty concerning outgroup taxa, limited taxon sampling, and selection on genes used to assess relationships. As a result, inferred relationships among the Haemosporida have been unstable, and questions concerning evolutionary diversification and host switching remain unanswered. A recent phylogeny placed mammalian malaria parasites, as well as avian/reptilian Plasmodium, in a derived position relative to the avian parasite genera Leucocytozoon and Haemoproteus, implying that the ancestral forms lacked merogony in the blood and that their vectors were non-mosquito dipterans. Bayesian, outgroup-free phylogenetic reconstruction using relaxed molecular clocks with uncorrelated rates instead suggested that mammalian and avian/reptilian Plasmodium parasites, spread by mosquito vectors, are ancestral sister taxa, from which a variety of specialized parasite lineages with modified life histories have evolved.Bayes factors | parasite diversification | Plasmodiidae M alaria parasites [broadly Apicomplexa: Haemosporida (1, 2)] have been well sampled in primates and songbirds, but are poorly known in other vertebrate groups. Recent surveys of blood parasites in vertebrate wildlife populations, using PCR to screen hosts for infections and DNA sequencing to identify parasite lineages, have revealed a rich diversity of hemosporidian parasites (3-6), possibly comparable to the number of hosts surveyed (7,8). It is important to reevaluate our interpretation of hemosporidian evolution as we expand sampling, to provide insight into shifts among hosts and vectors-often implicated in emerging infectious diseases-and to interpret the evolution of malaria parasite life cycles. Because choice of outgroup taxa critically influences the reconstruction of evolutionary relationships (9), it is also important to reassess assumptions about ancestral relationships and the monophyly of taxa. Premolecular reconstructions based on morphology and life history traits presumed that a monophyletic clade of Plasmodium parasites exhibited the most derived traits [e.g., asexual reproduction (merogony) in the circulating blood of the vertebrate host, production of hemozoin pigment from the metabolism of hemoglobin] (10, 11); accordingly, Leucocytozoon, a parasite of birds that lacks these traits, was placed in a basal position (Fig. 1A). Such a position for Leucocytozoon was indeed suggested in early molecular analyses based on the ...

The pathology and pathogenicity of a novel Haemoproteus spp. infection in wild Little Penguins (Eudyptula minor)

“…Parameters for phylogenetic analysis and rooting were based on that of Outlaw and Ricklefs (2011). A maximum likelihood phylogeny was generated using MEGA 5.0 (Tamura et al 2011) and a GTR+ gamma model of nucleotide substitution with 1,000 bootstrap iterations, and was rooted between mammalian Plasmodium and avian Plasmodium.…”

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

“…For the first set of nested PCR assays, we used the outer primer pair 3932F and DW4R (18,19) and the inner primer pair 413F and 926R (20). We also amplified and sequenced regions of the mitochondrial cyt b gene from positive samples using a variety of primer pairs and protocols (21)(22)(23). Our protocols often fail to recognize mixed infections, meaning that parasite lineage prevalence in host populations may be somewhat underestimated.…”

“…We constructed a phylogenetic tree of 132 hemosporidian lineages from North America, Central America, and the Caribbean region. We used Geneious 9.1.5 to generate an alignment of the 132 Plasmodium and Haemoproteus sequences, together with 10 Leucocytozoon sequences used as outgroup (23). We used BEAST 2.4.2 and its applications (24) to obtain a Bayesian maximum clade credibility tree using an uncorrelated relaxed lognormal clock, a GTR + I + G substitution model, and a Yule speciation prior.…”

Nematodes Associated With Mammals in the Great American Biotic Interchange (Gabi)

“…Nevertheless, determination of both the origin of host-parasite associations is possible by using indirect methods, which include the increase of taxon and geographic sampling and the calibration of molecular clocks enforcing switches in geographic distribution or association with hosts. With the use of ancillary geological evidence, it is possible to estimate the age of associations, especially in those cases that involve an evident shift in the geographic distribution that is linked to a dated geological event (Ricklefs & Outlaw 2010, Badets et al 2011, Outlaw &Ricklefs 2011. Thus, as in other organisms, the study of the evolution of parasites is possible through the analysis of their genetic structure (De Baets & Littlewood 2015), which again can be dated by correlating shifts in the distribution of parasites in their hosts or in new geographic areas.…”