Animals host an incredible diversity of parasites, here defined as organisms that live in or on another organism (the host) at some cost to the host, including microparasites (viruses, bacteria, fungi, and protozoa) and macroparasites (helminths and arthropods). Science is only just starting to understand this diversity of parasites, with the vast majority of parasites yet to be documented (Dobson et al., 2008; Poulin et al., 2016; Carlson et al., 2019). Some parasites are highly host specific, meaning that they are found only on a single host species, while others are generalists that are able to infect multiple hosts. Hence, these symbiotic associations and their transmission represent a vast web of connections that can be mapped among host species (Poulin, 2010; Gómez et al., 2013). These associations vary over time as parasites go extinct, speciate, and transmit across host species, with these processes influenced by evolutionary dynamics and geographic movements of the host species themselves (Combes, 2001). Parasites also drive coevolutionary dynamics involving reciprocal selective pressures favoring host defenses and parasite adaptations to overcome those defenses.

The factors that drive the connections between hosts and parasites are central to major research programs in ecology and evolution. These associations, and changes to them, also impact human health. In particular, parasites and pathogens can shift to human populations (a zoonosis) and adapt to humans, in some cases evolving to become specialists on humans (Wolfe et al., 2007), as seen with HIV-AIDS, measles virus, and the malaria parasite Plasmodium falciparum. Given the massive and global extent of anthropogenic change and its impacts on disease-carrying hosts (Gibb et al., 2020), such events are likely to occur increasingly often. Cross-species transmission events are also important to animal health and conservation, with parasites having negative fitness consequences for animal hosts and contributing to extinctions (De Castro and Bolker, 2004). Many of these negative outcomes result from cross-species transmissions from domesticated animals, invasive species, or humans (known as anthropozoonoses in the latter case). Finally, the loss of a host causes loss of parasites (Koh et al., 2004; Dobson et al., 2008; Dunn et al., 2009; Herrera et al., 2021). Given the important role of parasites in ecosystems, the loss of hosts can have cascading effects, with some authors proposing using naturally occurring parasites as a marker of a healthy ecosystem (Hudson et al., 2006).

A phenomenon of particular importance for global health is parasite sharing, which refers to the occurrence of a parasite in multiple host species. The distribution of parasites across hosts is influenced by three mechanisms. The first of these is co-speciation, with the diversification of the host resulting in diversification of the parasite. This scenario results in congruent host and parasite phylogenies, as found in primates and their pinworms (Hugot, 1999). Co-speciation is expected to result in parasites specializing on particular hosts (or sets of closely related hosts). A second mechanism involves opportunistic transmissions from one host species to a new species, broadly known as a host shift. Once successfully infecting a new host, the parasite lineage may specialize on it. Finally, a generalist parasite may infect multiple hosts. The majority of parasites may fall into this category, with sharing either limited to a few hosts – as is the case of Ebola virus infecting bats, great apes, and duikers – or to a wide range of hosts – as in the case of Giardia infecting many phylogenetically diverse species. In primates, for example, one study found that approximately 70% of known parasites are documented to infect more than one host (Pedersen et al., 2005).

Here, we review parasite sharing between humans and our close primate relatives for a group of protozoan parasites that cause malaria. We discuss how evolutionary and ecological perspectives can inform the origin and virulence of emerging zoonoses, as well as pathways for vaccine or therapeutic targets. Malaria parasites range from single-host specialists to wide generalists, with different malaria parasites infecting a broad range of animals, including birds, bats, primates, lizards, ungulates, and rodents (Galen et al., 2018). Host sharing of malaria parasites is driven by a mix of ecological and genetic factors, and our understanding of the process is biased by sampling of some hosts more than others (Garamszegi, 2009; Faust and Dobson, 2015). For example, among avian malaria species, previous studies revealed that malaria species tend to be generalists that infect a wide range of host species, allowing them to invade new ecosystems (Ricklefs and Fallon, 2002; Gupta et al., 2019; Ewen et al., 2012; Galen et al., 2018), though the full diversity and ecology of these species is only starting to be appreciated.

Human-infecting malaria parasites are part of the genus Plasmodium (Galen et al., 2018; Sharp et al., 2020). These protozoan parasites have an obligate Anopheles mosquito vector stage for sexual reproduction and transmission between hosts. Of the roughly 30 known primate malaria parasites, currently a handful are known to naturally infect humans regularly: P. falciparum, Plasmodium vivax, Plasmodium malariae, Plasmodium ovale wallikeri, and Plasmodium ovale curtisi, with growing evidence that Plasmodium knowlesi is also a natural parasite of humans (Singh et al., 2004; Sharp et al., 2020). Indeed, all human malaria parasites have a zoonotic origin from our nonhuman primate (NHP) relatives. Ancient host switching includes two of the most common human malaria parasites, P. falciparum and P. vivax, which are now endemic in humans, and rare in NHPs. Ongoing and emerging zoonoses include P. knowlesi, Plasmodium simium, and perhaps Plasmodium brasilianum (Antinori et al., 2021; Faust and Dobson, 2015).

Figure 1 summarizes the host-parasite relationships between the major clades of primate malaria parasites and the primates that they infect. The lack of high-quality whole-genome data for some primate malarias makes the phylogenetic relationships between certain parasites unclear and open to change (Pacheco et al., 2013; Arisue et al., 2019; Galen et al., 2018; Loy et al., 2018; Daron et al., 2020). Notably, Plasmodium is a paraphyletic genus name; P. vivax is more closely related to rodent malarias, such as Plasmodium berghei and Plasmodium chabaudi, and to Hepatocystis spp., than it is to P. falciparum (Galen et al., 2018; Sharp et al., 2020). Hence, the historical naming of Plasmodium should be supported by more taxonomically consistent subgenic taxonomic definitions based on the main clades (Figure 1). Therefore, we focus on this higher taxonomic level. The subgenus naming convention we use, along with the species within each subgenus, is listed in Figure 1. When referring to single Plasmodium species, we will use the species name, for example, P. vivax; when referring to the broader clade, we will use the term ‘relatives,’ for example, P. vivax relatives or P. vivax-related, except for Laverania, which is already widely used to describe the subgenus including P. falciparum and other parasites that infect great apes.

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We focus on primate malarias because of NHPs’ close evolutionary relationship to humans and known parasite sharing with humans that produces disease. Therefore, primate-Plasmodium relationships provide an important system to demonstrate the links between ecological and evolutionary perspectives with direct medical relevance. To better predict future zoonoses or to build interventions for ongoing zoonoses, the drivers of NHP to human host switching have been a focus of empirical and mathematical modeling studies (Abdullahi et al., 2013; Imai et al., 2014; Yakob et al., 2018, Medeiros-Sousa et al., 2021). Starting with P. knowlesi in the 1930s, controlled experimental studies have confirmed a variety of NHP malaria parasites can infect human hosts, and epidemiological and genetic studies have confirmed a subset cause infection in natural settings (Knowles and Gupta, 1932, Eyles et al., 1960; Coatney et al., 1961; Schmidt et al., 1961; Chin et al., 1968, Contacos et al., 1963; Deane et al., 1966; Coatney et al., 1966; Contacos et al., 1970). Yet, we are only beginning to understand the extent of zoonotic malaria cases, the rate of human-to-human transmission, and the ecological and evolutionary factors that underlie the origin and spread of Plasmodium across primate hosts.

To examine the ecological, evolutionary, and sampling processes that underlie the host specificity of primate malaria parasites, we collated an occurrence database of published records of the location and species involved in wild primate infections. We also collated a database of NHP Plasmodium species occurring in humans. Evidence for malaria in lemurs is limited, with no whole-genome sequences available, so we focus on Central/South American monkeys, Asian and African monkeys, and apes.

Here, we review the origin and current status of the Plasmodium parasites that regularly infect humans in natural settings, discussing the importance of transmission from NHPs to humans across timescales.

Ongoing zoonoses, with unknown human-to-human capability

In addition to the ancient zoonoses that founded modern human-infecting malaria species, multiple NHP malaria parasites are currently infecting humans, particularly in Southeast Asia and South America. Evidence of ape-to-human transmission of Laverania in Africa is rare, but has been documented (Ngoubangoye et al., 2016).

Today, zoonotic P. knowlesi is the most frequent malaria-causing agent in Malaysia and is widespread in Southeast Asia from its macaque origin (Figure 2B; Rajahram et al., 2019; WHO, 2014, WHO, 2019). Despite its high incidence, evidence for human cycles of transmission has not been clearly demonstrated, but is presumed. Genetic data suggests divergent populations of P. knowlesi circulating amongst different macaque species (Divis et al., 2015). Previously misdiagnosed as both P. vivax and P. malariae, the timing of P. knowlesi first shifting into humans is unclear (Singh et al., 2004). Though less common and well-understood, occasional natural infections of another macaque parasite, Plasmodium cynomolgi, have also been observed in Southeast Asia (Ta et al., 2014). The high rates of P. cynomolgi in the wild suggest undiagnosed current or future risk of zoonosis is possible (Zhang et al., 2016).

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South America is a newly identified hotspot for emerging zoonotic malarias, though the timeline and extent of zoonoses remain unknown because of a lack of historical or archival sampling. Early experimental studies confirmed the possibility of human infection of NHP malaria parasites P. brasilianum and P. simium (Contacos et al., 1963; Deane et al., 1966). The first natural infections in humans were only described in 2015 and 2017 for P. brasilianum and P. simium, respectively (Lalremruata et al., 2015; Brasil et al., 2017). Because of their close morphological and genetic relationships to common human-infecting malaria parasites, previous zoonotic infections of P. brasilianum and P. simium have been misclassified as P. malariae and P. vivax, respectively. Indeed because of their great genetic, morphological, and immunological similarity, it is unclear that the pairs P. brasilianum and P. malariae, or P. simium and P. vivax, should be classified as different species. Therefore, these cases may be either true zoonoses or examples of the host generalism of P. malariae relatives and P. vivax relatives.

Genomic data provides some support for differentiation between P. simium and P. vivax (Mourier et al., 2021; de Oliveira et al., 2021), but is weaker for P. brasilianum and P. malariae comparisons, which lack whole-genome data. Currently, most South American P. malariae cases are linked to international travel, but NHPs may serve as a reservoir for disease (Figure 2). Similarly, extra-Amazonian cases of P. vivax have been rising in Brazil (Brasil et al., 2017), and further testing will be required to determine if some of these are misdiagnosed zoonotic P. simium infections. Further genetic and epidemiological studies are needed to clarify the extent of natural human infection, the taxonomic relationships, and determine if their immediate origin is transmission from NHPs or from other humans. For example, widespread genotyping of malaria cases presumed to be P. vivax in humans can establish the geographic range and frequency of P. simium infection, and a combination of mathematical modeling and contact tracing or other public health surveys would inform the likelihood of human-to-human transmission versus recurrent monkey-to-human transmission. Additionally, recent identification of P. simium in other regions shows the importance of further geographic sampling to understand the origin of P. simium, including the timeline, location, and number of introductions (Rondón et al., 2019).

Malaria parasite sharing is not unidirectional; increasing human pressures on local NHP populations are reintroducing human Plasmodium species into other primates, putting often endangered species at further health and conservation risk. Additionally, these hosts may become reservoirs for human malaria, with these parasites later transmitting into human populations or other NHPs.

Because the great apes have close relatives of human-infecting Plasmodium circulating in their populations, it is hard to identify anthroponotic infections (i.e., transmission of human endemic parasites to other species). However, the presence of drug-resistant mutations can be used to predict the direction of transfer as human to ape. Using this evidence, the human P. falciparum has been found recurrently in primate populations living near humans (Ngoubangoye et al., 2016; Prugnolle et al., 2013; Loy et al., 2017). P. vivax, P. malariae, and P. ovale have also been occasionally, but rarely, described in African apes (Kaiser et al., 2010; Duval et al., 2010; Hayakawa et al., 2009; Rayner et al., 2011; Sharp et al., 2020). Further whole-genome sequencing or typing of known diagnostic regions will be able to differentiate between these close parasite relatives and inform the risk level of anthroponoses.

South American malaria parasites demonstrate the risk to humans of anthroponoses from wild NHPs. Now considered a zoonotic malaria parasite, P. simium is proposed to have originated as a human-to-howler monkey switch of P. vivax during European colonization and the Transatlantic slave trade in Brazil. An early hypothesis suggested that P. vivax come from a pre-Columbian introduction 15,000–30,000 years ago as humans first arrived. But new methodologies and a better sampling have supported a recent introduction, ~500 years ago with European colonization (Culleton et al., 2011; van Dorp et al., 2020; Taylor et al., 2013; Hupalo et al., 2016; Rodrigues et al., 2018). Historical DNA from pre-eradication Spain suggest a recent introduction and close relationship between historical Southern European P. vivax and modern South American P. vivax (van Dorp et al., 2020). This is consistent with a host switch of historical P. vivax into howler monkeys to become what is today known as P. simium, supported by the low genetic diversity of P. simium and high similarity morphologically and genetically to P. vivax (Escalante and Ayala, 1995; Lim et al., 2005; Mourier et al., 2021; de Oliveira et al., 2021). Since then, P. simium has built up a handful of genetic differences from P. vivax, perhaps through drift or adaptations to a new host (Brasil et al., 2017; Mourier et al., 2021; de Oliveira et al., 2021). Occasional cases of P. falciparum have also been reported in South American monkeys, though these cases are rare and largely unconfirmed (Duarte et al., 2008; Yamasaki et al., 2011).

The history of P. malariae/P. brasilianum in the Americas is similarly complicated by sharing across multiple primate hosts. Today, the classification of these two parasite species seems to follow the host in which they are found – P. malariae for humans and P. brasilianum for NHPs – rather than parasite characteristics (Lalremruata et al., 2015). P. malariae/brasilianum is incredibly widespread in South American monkeys and appears to circulate freely between primate and human populations and be a single anthropozoonotic species in South America. Similar to P. simium, the presence of P. malariae/P. brasilianum in American NHPs likely originated with a human-to-primate transmission associated with the Transatlantic slave trade, from African P. malariae (Collins and Jeffery, 2007; Rutledge et al., 2017; Lalremruata et al., 2015). P. malariae is now rare in humans in South America, with most cases either introduced by international travel or potentially through new zoonoses from primate reservoirs.

A variety of methods have been used to investigate the distribution of parasites among hosts. One starting point is to produce a matrix of hosts and the parasites (Cooper et al., 2012), which is known as an incidence matrix in ecology. Another approach maps the occurrence of a parasite onto a phylogeny (Cooper et al., 2012), or compares host and parasite phylogenies, aiming to identify and visualize host shifts along with parasite duplications (i.e., within host speciation) and parasite extinctions (Charleston, 1998; Huelsenbeck et al., 2000, Ricklefs and Fallon, 2002; Garamszegi, 2009). Phylogeny is often a strong predictor of parasite sharing because of shared physiological, genetic, and environmental factors. Finally, a number of authors represent host-parasite incidence data as a bipartite network (Poulin, 2010). As its name suggests, a bipartite network has two parts: one for hosts and another for parasites (Figure 1). Edges are placed between organisms in each part (but not within) based on the occurrence of a parasite in a host. One can then generate a unipartite projection of this bipartite network showing how hosts are connected through the parasites they share (or parasites are connected through the hosts that they share) (Gómez et al., 2013). A major risk in all of these approaches is that we rarely know all of the parasites in a collection of hosts, with some parasites or hosts studied better than others (Walther et al., 1995; Stephens et al., 2016). For example, terrestrial primate species are more likely to be sampled for parasites than arboreal primate species (Cooper and Nunn, 2013; Poulin et al., 2016). Thus, a variety of approaches have been developed to deal with variation in sampling effort (Nunn et al., 2003; Elmasri et al., 2020; Teitelbaum et al., 2020; Amoroso and Nunn, 2021).

The range of hosts that a parasite infects can also be quantified using measures of phylogenetic host specificity (Poulin, 2010; Cooper et al., 2012). This concept is important in the context of human and animal health because it determines the potential for cross-species transmission, with phylogenetic host specialists generally only crossing narrow phylogenetic distances, while phylogenetic host generalists can cross a wider phylogenetic range of hosts. Thus, for emerging zoonoses in humans, we should be concerned about phylogenetic host specialists arising from great apes and other NHPs and phylogenetic host generalists in other mammals. In one recent study, Park et al., 2018 used a database of >1400 parasite species and 404 mammal host species to quantify phylogenetic host specificity and its correlates. They found that arthropods and bacteria are the most generalist, viruses and helminths are intermediate in generalism, and protozoa are the most specialist of the parasites in this database. Park et al., 2018 also found that close-contact transmission is most associated with specialization on fewer hosts. These analyses also revealed a pattern consistent with a ‘leaps and creeps’ strategy by parasites, with some parasites mostly infecting closely related hosts, but occasionally taking a ‘leap’ to less related hosts, where the parasite circulates again amongst close relatives. For primate malarias, cross-species transmission, and therefore parasite sharing among hosts, is a confluence of factors in the parasite, vector, and multi-host system, and is a product of both their geography and phylogeny.

The observed patterns of Plasmodium parasite sharing among primate hosts – described above – are shaped by a variety of ecological and evolutionary factors impacting the parasite, host, and vector. Understanding the primary mechanisms behind these parasite distributions will be important for predicting parasite emergence in human populations and designing effective interventions.

For many parasites, phylogeny is a major predictor of host sharing: more closely related species are expected to harbor the same parasite because they share underlying physiology, immune defenses, behavior, and in the case of intracellular parasites such as viruses or some protozoa, these hosts share similar cellular phenotypes, such as viral or parasite entry receptors (Woolhouse, 2002; Longdon et al., 2014). This is expected to generate phylogenetic signal in host and parasite infection patterns and to influence probabilities for shifts among different hosts. The effect of phylogeny has been documented in primates, with research revealing that more closely related primate hosts have more similar parasite communities (Davies and Pedersen, 2008, Cooper et al., 2012). Similarly, a study of rabies virus among North American bat species also found support for higher probability of host shifts among more closely related species of bats (Streicker et al., 2010), while an experimental study demonstrated an effect of phylogeny on viral titers for three viruses in Drosophila (Longdon et al., 2011). This phylogenetic relationship has been observed in avian and primate malarias (Ricklefs and Fallon, 2002; Garamszegi, 2009), and we consider support for it in Section 5.

In addition to phylogenetic relatedness, geographic overlap and host phenotypic and ecological characteristics also predict parasite sharing (Clark and Clegg, 2017). Hosts that share parasites must overlap geographically with one another (or with some other host that shares a vector and acts as a reservoir to infect them both); both geographic and phylogenetic effects have been observed in primates (Davies and Pedersen, 2008; Cooper et al., 2012). Across mammals, Albery et al., 2020 found that both phylogeny and geographic overlap predicted sharing of viruses. Traits that lead to direct or indirect interactions between species, such as a shared diet, water source, or sleep site, will also facilitate parasite sharing. A variety of evidence supports these effects. In a study of primates, for example, Cooper et al., 2012 found that similarity in body mass predicted the similarity of parasite communities in pairs of species (together with effects of phylogeny and geography). In a study of bat viruses, Willoughby et al., 2017 found that cave-roosting increases parasite sharing, along with geographic overlap and phylogenetic distance. Anthropogenic change is influencing many of these processes, with likely consequences for human disease risk and primate conservation. Also important, but less well studied in natural systems, are the daily rhythms of hosts, vectors, and the different life stages of parasites (Owolabi et al., 2021; Prior et al., 2020). Here, we highlight key ecological and evolutionary factors such as these that drive the distribution of parasites across hosts for the case of primate malarias.

Parasite transmission studies are often human-centric, focusing on animal-to-human transmission. Here, we emphasize a broader perspective that between-animal transmission also has direct medical and conservation impacts, and monitoring of NHP diseases should be a priority. This is particularly timely given recent conversations about long-term creation of reservoirs of SARS-CoV-2 in new animal populations, which could then serve as a new source for future evolution and spillover into humans.

A broader perspective on the role of humans in disturbing environments, changing climates, and altering species interaction patterns will work synergistically with genetic and epidemiological research. Studies have increasingly demonstrated the importance of climatic and anthropogenic change on parasite and vector life cycles, but the ecology of the hosts is generally understudied. For example, mathematical modeling suggests that group size plays an important role in disease transmission dynamics and infection rates (Caillaud et al., 2013; Nunn et al., 2015), though these questions have generally not been explored for multi-host systems. Similarly, more attention is needed on how the timing of activity patterns of hosts, vectors, and parasites influences infection risk within and across species, including in relation to drug performance (Owolabi et al., 2021). Multi-host mathematical models can be a key tool in understanding the factors driving host sharing and infection distributions, especially with changes to local environments through climatic change and human influence. Better feedback or integration across disciplines, including mathematics, social sciences, and different fields of biology, will be an important step, and builds on similar interdisciplinarity in other areas of evolutionary medicine.

Disease burdens, as well as resources, are not equally distributed between or within countries. Within-country capacity building is particularly important for monitoring primate and zoonotic malaria. It is especially important to provide that capacity building for new genomic technologies is facilitating noninvasive sampling and field-based sequencing. Improving the ability of rapid diagnostic tests or designing capture methods to differentiate between closely related parasite species from different hosts – such as P. vivax versus P. simium or P. falciparum from other Laverania species – will be an important next step to stop human-NHP transmission pathways.

Recent studies have produced hundreds to thousands of Plasmodium genome sequences from around the world, particularly P. falciparum samples from Africa and Asia, and to a lesser extent P. vivax (Hupalo et al., 2016; Pearson et al., 2016; Amambua-Ngwa et al., 2019). Robust population-genetic methods designed to analyze the plethora of parasite samples are limited, however. Over the past few years, newer work has developed identity-by-descent and linkage-based summaries of genetic variation in Plasmodium species more suited to study recent population history (Schaffner et al., 2018; Taylor et al., 2020; de Oliveira et al., 2020; Neafsey et al., 2021). Despite these advances, a major challenge remains: the expected neutral genetic diversity in malaria parasites is unclear, limiting population-genetic inference. Plasmodium parasites undergo a complex life cycle through host and vector stages. Multiple steps involve processes expected to dramatically influence genetic variation, such as bottlenecks with transmission, rapid asexual population growth in primate hosts, and sexual recombination in vectors. The combination of these stages makes genetic variation difficult to predict or fit to common models, such as Wright–Fisher (Parobek et al., 2016; Chang and Hartl, 2015; Chang et al., 2013). In turn, common outlier approaches to detect loci of importance (e.g., for drug resistance or adaptation to new hosts), such as F_ST scans, are difficult to interpret and may produce spurious results.

A handful of studies have begun to address the challenge of understanding genetic variation by using simulation approaches, making substantial progress linking epidemiological and population-genetic models (Chang and Hartl, 2015; Chang et al., 2013; Hendry et al., 2020; Watson et al., 2021). These studies represent an important first step, but progress is needed to incorporate realistic population and genome sizes in computationally tractable ways. Beyond model building for an intuition of the population genetics of malaria infection dynamics, simulation-based studies also open the door for statistical inference of complex processes (Beaumont, 2010). With this model-based inference, we can more confidently differentiate between transmission networks or characterize regions of parasite genomes with patterns outside those expected from demography alone.

As genomic data for a wider variety of parasites becomes available, inference from population-genetic methods will instead be limited by our ecological and biological understanding of the systems. For example, more accurate estimates of mutation rates, the complexities of generation times, recombination rates, mosquito birth and death rates, and coinfection probability are needed to parameterize the models. An important next step will be to explore the phenotypic consequences and origins of the observed genetic variants hypothesized to play a role in host switching or transmission. To achieve this goal, functional tests are needed, together with population-genetic inference of adaptive versus neutral processes. Experimental studies have identified key pathways in P. falciparum that likely played a role in host switching from its putative ancestors in gorillas (Proto et al., 2019; Galaway et al., 2019). P. vivax, however, is not amenable to long-term lab culture, so functional experiments have been limited and population-genetic data will play a central role (Luo et al., 2015; Udomsangpetch et al., 2008; Noulin et al., 2013). Combining genomic information with temporally and geographically fine-scale epidemiological and ecological data will better enable scientists to link human activity to vector-borne disease prevalence and aid in predicting and prioritizing emerging zoonoses. Archived or historical samples from humans and primates are rich resources that are only beginning to be utilized (van Dorp et al., 2020). Connecting diverse information types will need to move beyond simple correlations to model-based inference and a deeper understanding of the mechanisms behind human-environment-disease interactions.

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