Vincenzo A. Ellis

Species formation by host shifting in avian malaria parasites

Significance Emerging infectious diseases pose threats to humans and livestock, but little is known about the general propensity of parasitic organisms to shift between hosts or the role of host shifting in the diversification of parasite lineages. The malaria parasites of contemporary vertebrate species descended from a common ancestor, likely after the diversification of their major host taxa, requiring rapid speciation and shifting between hosts across large host–taxonomic distances. Examination of sister lineages of avian malaria parasites in the New World suggests that such host shifting is common and often leads to the origin of new evolutionary lineages of parasites. The malaria parasites (Apicomplexa: Haemosporida) of birds are believed to have diversified across the avian host phylogeny well after the origin of most major host lineages. Although many symbionts with direct transmission codiversify with their hosts, mechanisms of species formation in vector-borne parasites, including the role of host shifting, are poorly understood. Here, we examine the hosts of sister lineages in a phylogeny of 181 putative species of malaria parasites of New World terrestrial birds to determine the role of shifts between host taxa in the formation of new parasite species. We find that host shifting, often across host genera and families, is the rule. Sympatric speciation by host shifting would require local reproductive isolation as a prerequisite to divergent selection, but this mechanism is not supported by the generalized host-biting behavior of most vectors of avian malaria parasites. Instead, the geographic distribution of individual parasite lineages in diverse hosts suggests that species formation is predominantly allopatric and involves host expansion followed by local host–pathogen coevolution and secondary sympatry, resulting in local shifting of parasite lineages across hosts.

Local host specialization, host-switching, and dispersal shape the regional distributions of avian haemosporidian parasites

Significance Within eastern North America, distributions of vector-transmitted haemosporidian blood parasites of birds, commonly known as “avian malaria parasites,” are associated with the distributions of their host species independently of direct effects of climate on potential vectors. Spatial analyses additionally indicated an absence of dispersal limitation for these parasites. Finally, host-breadth, ranging continuously from specialist to generalist, varies among parasite lineages and is dynamic within parasite assemblages over space and time. The distributions of avian haemosporidian parasites emphasize the ability of parasites to disperse across broad regions and to switch readily between hosts to become emerging infectious diseases. The drivers of regional parasite distributions are poorly understood, especially in comparison with those of free-living species. For vector-transmitted parasites, in particular, distributions might be influenced by host-switching and by parasite dispersal with primary hosts and vectors. We surveyed haemosporidian blood parasites (Plasmodium and Haemoproteus) of small land birds in eastern North America to characterize a regional parasite community. Distributions of parasite populations generally reflected distributions of their hosts across the region. However, when the interdependence between hosts and parasites was controlled statistically, local host assemblages were related to regional climatic gradients, but parasite assemblages were not. Moreover, because parasite assemblage similarity does not decrease with distance when controlling for host assemblages and climate, parasites evidently disperse readily within the distributions of their hosts. The degree of specialization on hosts varied in some parasite lineages over short periods and small geographic distances independently of the diversity of available hosts and potentially competing parasite lineages. Nonrandom spatial turnover was apparent in parasite lineages infecting one host species that was well-sampled within a single year across its range, plausibly reflecting localized adaptations of hosts and parasites. Overall, populations of avian hosts generally determine the geographic distributions of haemosporidian parasites. However, parasites are not dispersal-limited within their host distributions, and they may switch hosts readily.

Mixed species flock, nest height, and elevation partially explain avian haemoparasite prevalence in Colombia

The high avian biodiversity present in the Neotropical region offers a great opportunity to explore the ecology of host-parasite relationships. We present a survey of avian haemoparasites in a megadiverse country and explore how parasite prevalences are related to physical and ecological host characteristics. Using light microscopy, we documented the presence of haemoparasites in over 2000 individuals belonging to 246 species of wild birds, from nine localities and several ecosystems of Colombia. We analysed the prevalence of six avian haemoparasite taxa in relation to elevation and the following host traits: nest height, nest type, foraging strata, primary diet, sociality, migratory behaviour, and participation in mixed species flocks. Our analyses indicate significant associations between both mixed species flocks and nest height and Haemoproteus and Leucocytozoon prevalence. The prevalence of Leucocytozoon increased with elevation, whereas the prevalence of Trypanosoma and microfilariae decreased. Plasmodium and Haemoproteus prevalence did not vary significantly with elevation; in fact, both parasites were found up to 3300m above sea level. The distribution of parasite prevalence across the phylogeny of bird species included in this study showed little host phylogenetic signal indicating that infection rates in this system are evolutionarily labile. Vector distribution as well as the biology of transmission and the maintenance of populations of avian haemoparasites deserve more detailed study in this system.

Specialized avian Haemosporida trade reduced host breadth for increased prevalence

Parasite specialization on one or a few host species leads to a reduction in the total number of available host individuals, which may decrease transmission. However, specialists are thought to be able to compensate by increased prevalence in the host population and increased success in each individual host. Here, we use variation in host breadth among a community of avian Haemosporida to investigate consequences of generalist and specialist strategies on prevalence across hosts. We show that specialist parasites are more prevalent than generalist parasites in host populations that are shared between them. Moreover, the total number of infections of generalist and specialist parasites within the study area did not vary significantly with host breadth. This suggests that specialists can infect a similar number of host individuals as generalists, thus compensating for a reduction in host availability by achieving higher prevalence in a single host species. Specialist parasites also tended to infect older hosts, whereas infections by generalists were biased towards younger hosts. We suggest that this reflects different abilities of generalists and specialists to persist in hosts following infection. Higher abundance and increased persistence in hosts suggest that specialists are more effective parasites than generalists, supporting the existence of a trade‐off between host breadth and average host use among these parasites.

The ecology of host immune responses to chronic avian haemosporidian infection

Host responses to parasitism in the wild are often studied in the context of single host–parasite systems, which provide little insight into the ecological dynamics of host–parasite interactions within a community. Here we characterized immune system responses to mostly low-intensity, chronic infection by haemosporidian parasites in a sample of 424 individuals of 22 avian host species from the same local assemblage in the Missouri Ozarks. Two types of white blood cells (heterophils and lymphocytes) were elevated in infected individuals across species, as was the acute-phase protein haptoglobin, which is associated with inflammatory immune responses. Linear discriminant analysis indicated that individuals infected by haemosporidians occupied a subset of the overall white blood cell multivariate space that was also occupied by uninfected individuals, suggesting that these latter individuals might have harbored other pathogens or that parasites more readily infect individuals with a specific white blood cell profile. DNA sequence-defined lineages of haemosporidian parasites were sparsely distributed across the assemblage of hosts. In one well-sampled host species, the red-eyed vireo (Vireo olivaceus), heterophils were significantly elevated in individuals infected with one but not another of two common parasite lineages. Another well-sampled host, the yellow-breasted chat (Icteria virens), exhibited no differences in immune response to different haemosporidian lineages. Our results indicate that while immune responses to infection may be generalized across host species, parasite-specific immune responses may also occur.

Reciprocal Specialization in Multihost Malaria Parasite Communities of Birds: A Temperate-Tropical Comparison

How specialization of consumers with respect to resources varies with respect to latitude is poorly understood. Coexistence of many species in the tropics might be possible only if specialization also increases. Alternatively, lower average abundance of more diverse biotic resources in the tropics might force consumers to become more generalized foragers. We examine levels of reciprocal specialization in an antagonistic system—avian malaria—to determine whether the number of host species used and/or parasite lineages harbored differ between a temperate and a tropical assemblage. We evaluate the results of network analysis, which can incorporate both bird and parasite perspectives on specialization in one quantitative index, in comparison to null models. Specialization was significantly greater in both sample sites than predicted from null models. We found evidence for lower per-host species parasite diversity in temperate compared to tropical birds. However, specialization did not differ between the tropical and temperate sites from the parasite perspective. We supplemented the network analysis with estimates of specialization that incorporate phylogenetic relationships of associates and found no differences between sites. Thus, our analyses indicate that specialization within an antagonistic host-parasite (resource-consumer) system varies little between tropical and temperate localities.

Prevalence of avian haemosporidian parasites is positively related to the abundance of host species at multiple sites within a region.

Parasite prevalence is thought to be positively related to host population density owing to enhanced contagion. However, the relationship between prevalence and local abundance of multiple host species is underexplored. We surveyed birds and their haemosporidian parasites (genera Plasmodium and Haemoproteus) at multiple sites across eastern North America to test whether the prevalence of these parasites in a host species at a particular site is related to that host’s local abundance. Prevalence was positively related to host abundance within most sites, although the effect was stronger and more consistent for Plasmodium than for Haemoproteus. In contrast, prevalence was not related to variation in the abundance of most individual host species among sites across the region. These results suggest that parasite prevalence partly reflects the relative abundances of host species in local assemblages. However, three nonnative host species had low prevalence despite being relatively abundant at one site, as predicted by the enemy release hypothesis.

Breaking down seasonality: androgen modulation and stress response in a highly stable environment.

Previous studies show that most birds inhabiting temperate regions have well defined life history stages, and they modulate the production of testosterone (T) and corticosterone (CORT) in response to changes in seasonality. In this study we aimed to examine baseline and stress-induced levels of CORT and circulating T in relation with life history stages in the rufous-collared sparrow, Zonotrichia capensis. We carried out this study for a year in a population inhabiting riparian habitats in the Atacama Desert in Chile, one of the most climatically stable and driest places in the world. This environment shows minimal yearly change in average temperature and precipitation is virtually zero. We found individuals breeding, molting and overlapping breeding and molt year round, although most individuals were molting during March and in breeding condition during October. T levels were not related to individual breeding condition, and at population level they were not significantly different across sampling months. Baseline levels of CORT did not vary across the year. Stress-induced levels of CORT were suppressed during March when most of the birds were molting. This phenomenon was also observed in birds not molting during this period suggesting a mechanism other than molt in determining the stress-response suppression. Our results strongly suggest that in this study site, long-term extremely stable conditions could have relaxed the selective pressures over the timing of life history stages which was evidenced by the breeding and molt schedules, its overlap and endocrine profiles.

Habitat modification and seasonality influence avian haemosporidian parasite distributions in southeastern Brazil

Habitat modification may change vertebrate and vector-borne disease distributions. However, natural forest regeneration through secondary succession may mitigate these effects. Here we tested the hypothesis that secondary succession influences the distribution of birds and their haemosporidian parasites (genera Plasmodium and Haemoproteus) in a seasonally dry tropical forest, a globally threatened ecosystem, in Brazil. Moreover, we assessed seasonal fluctuations in parasite prevalence and distribution. We sampled birds in four different successional stages at the peak and end of the rainy season, as well as in the middle and at the end of the dry season. A non-metric multidimensional scaling analysis revealed that bird communities in the pasture (i.e., highly modified) areas were different from those in the early, intermediate, and late successional areas (secondary forests). Among 461 individual birds, haemosporidian prevalence was higher in pasture areas than in the more advanced successional stages, but parasite communities were homogeneous across these areas. Parasite prevalence was higher in pasture-specialists birds (resilient species) than in forest-specialists species, suggesting that pasture-specialists may increase infection risk for co-occurring hosts. We found an increase in prevalence between the middle and end of the dry season, a period associated with the beginning of the breeding season (early spring) in southeastern Brazil. We also found effects of seasonality in the relative prevalence of specific parasite lineages. Our results show that natural forest recovery through secondary succession in SDTFs is associated with compositional differences in avian communities, and that advanced successional stages are associated with lower prevalence of avian haemosporidian parasites.

Epaulet Size and Current Condition in Red-Winged Blackbirds: Examining a Semistatic Signal, Testosterone, Immune Function, and Parasites

Some sexually selected signals are thought to convey information about the current condition and genetic/epigenetic quality of the individual signaling, including the ability to resist parasites. However, it is unclear whether semistatic sexual signals that develop periodically and remain stable over protracted periods, such as avian breeding plumage, can relate to measures of current condition and health. We examined a semistatic signal (wing epaulet size) in male red-winged blackbirds (Agelaius phoeniceus) during the breeding season and looked for relationships between this trait and circulating testosterone (T), hematocrit, bacteria-killing ability (BKA) of the blood, and the infection status, richness, and abundance of four functional categories of parasite. We found that epaulet size was positively related to circulating levels of T and ectoparasite infections. We found no relationships between T and parasite infections. In adult males there was a negative relationship between T and BKA, whereas in yearling males there was no relationship. We found no evidence for a general reduction in immunocompetence in males with larger epaulets but rather an increase in susceptibility to specific types of parasites. Our results suggest that semistatic signals can be linked to measures of current condition, and we postulate that these relationships are modulated via activity levels related to breeding-season activities.