Aim: Despite the wide distribution of many parasites around the globe, the range of individual species varies significantly even among phylogenetically related taxa. Since parasites need suitable hosts to complete their development, parasite geographical and environmental ranges should be limited to communities where their hosts are found. Parasites may also suffer from a trade-off between being locally abundant or widely dispersed. We hypothesize that the geographical and environmental ranges of parasites are negatively associated to their host specificity and their local abundance.

Location: Worldwide

Time period: 2009 to 2021

Major taxa studied: Avian haemosporidian parasites

Methods: We tested these hypotheses using a global database which comprises data on avian haemosporidian parasites from across the world. For each parasite lineage, we computed five metrics: phylogenetic host-range, environmental range, geographical range, and their mean local and total number of observations in the database. Phylogenetic generalized least squares models were ran to evaluate the influence of phylogenetic host-range and total and local abundances on geographical and environmental range. In addition, we analysed separately the two regions with the largest amount of available data: Europe and South America.

Results: We evaluated 401 lineages from 757 localities and observed that generalism (i.e. phylogenetic host range) associates positively to both the parasites’ geographical and environmental ranges at global and Europe scales. For South America, generalism only associates with geographical range. Finally, mean local abundance (mean local number of parasite occurrences) was negatively related to geographical and environmental range. This pattern was detected worldwide and in South America, but not in Europe.

Main Conclusions: We demonstrate that parasite specificity is linked to both their geographical and environmental ranges. The fact that locally abundant parasites present restricted ranges, indicates a trade-off between these two traits. This trade-off, however, only becomes evident when sufficient heterogeneous host communities are considered.

We compiled data on haemosporidian lineages from the MalAvi database (http://130.235.244.92/Malavi/ , Bensch et al. 2009) including all the data available from the “Grand Lineage Summary” representing Plasmodium and Haemoproteus genera from wild birds and that contained information regarding location. After checking for duplicated sequences, this dataset comprised a total of ~6200 sequenced parasites representing 1602 distinct lineages (775 Plasmodium and 827 Haemoproteus) collected from 1139 different host species and 757 localities from all continents except Antarctica (Supplementary figure 1, Supplementary Table 1). The parasite lineages deposited in MalAvi are based on a cyt b fragment of 478 bp. This dataset was used to calculate the parasites’ geographical, environmental and phylogenetic ranges.

Geographical range

            All analyses in this study were performed using R version 4.02. In order to estimate the geographical range of each parasite lineage, we applied the R package “GeoRange” (Boyle, 2017) and chose the variable minimum spanning tree distance (i.e., shortest total distance of all lines connecting each locality where a particular lineage has been found). Using the function “create.matrix” from the “fossil” package, we created a matrix of lineages and coordinates and employed the function “GeoRange_MultiTaxa” to calculate the minimum spanning tree distance for each parasite lineage distance (i.e. shortest total distance in kilometers of all lines connecting each locality). Therefore, as at least two distinct sites are necessary to calculate this distance, parasites observed in a single locality could not have their geographical range estimated. For this reason, only parasites observed in two or more localities were considered in our phylogenetically controlled least squares (PGLS) models.

Host and Environmental diversity

Traditionally, ecologists use Shannon entropy to measure diversity in ecological assemblages (Pielou, 1966). The Shannon entropy of a set of elements is related to the degree of uncertainty someone would have about the identity of a random selected element of that set (Jost, 2006). Thus, Shannon entropy matches our intuitive notion of biodiversity, as the more diverse an assemblage is, the more uncertainty regarding to which species a randomly selected individual belongs. Shannon diversity increases with both the assemblage richness (e.g., the number of species) and evenness (e.g., uniformity in abundance among species).

To compare the diversity of assemblages that vary in richness and evenness in a more intuitive manner, we can normalize diversities by Hill numbers (Chao et al., 2014b). The Hill number of an assemblage represents the effective number of species in the assemblage, i.e., the number of equally abundant species that are needed to give the same value of the diversity metric in that assemblage. Hill numbers can be extended to incorporate phylogenetic information. In such case, instead of species, we are measuring the effective number of phylogenetic entities in the assemblage.

Here, we computed phylogenetic host-range as the phylogenetic Hill number associated with the assemblage of hosts found infected by a given parasite. Analyses were performed using the function “hill_phylo” from the “hillr” package (Chao et al., 2014a). Hill numbers are parameterized by a parameter “q” that determines the sensitivity of the metric to relative species abundance. Different “q” values produce Hill numbers associated with different diversity metrics.  We set q = 1 to compute the Hill number associated with Shannon diversity. Here, low Hill numbers indicate specialization on a narrow phylogenetic range of hosts, whereas a higher Hill number indicates generalism across a broader phylogenetic spectrum of hosts.

We also used Hill numbers to compute the environmental range of sites occupied by each parasite lineage. Firstly, we collected the 19 bioclimatic variables from WorldClim version 2 (http://www.worldclim.com/version2) for all sites used in this study (N = 713). Then, we standardized the 19 variables by centering and scaling them by their respective mean and standard deviation. Thereafter, we computed the pairwise Euclidian environmental distance among all sites and used this distance to compute a dissimilarity cluster. Finally, as for the phylogenetic Hill number, we used this dissimilarity cluster to compute the environmental Hill number of the assemblage of sites occupied by each parasite lineage. The environmental Hill number for each parasite can be interpreted as the effective number of environmental conditions in which a parasite lineage occurs. Thus, the higher the environmental Hill number, the more generalist the parasite is regarding the environmental conditions in which it can occur.

Parasite phylogenetic tree

            A Bayesian phylogenetic reconstruction was performed. We built a tree for all parasite sequences for which we were able to estimate the parasite’s geographical, environmental and phylogenetic ranges (see above); this represented 401 distinct parasite lineages. This inference was produced using MrBayes 3.2.2 (Ronquist & Huelsenbeck, 2003) with the GTR + I + G model of nucleotide evolution, as recommended by ModelTest (Posada & Crandall, 1998), which selects the best-fit nucleotide substitution model for a set of genetic sequences. We ran four Markov chains simultaneously for a total of 7.5 million generations that were sampled every 1000 generations. The first 1250 million trees (25%) were discarded as a burn-in step and the remaining trees were used to calculate the posterior probabilities of each estimated node in the final consensus tree. Our final tree obtained a cumulative posterior probability of 0.999. Leucocytozoon caulleryi was used as the outgroup to root the phylogenetic tree as Leucocytozoon spp. represents a basal group within avian haemosporidians (Pacheco et al., 2020).