Background
Avian haemosporidia, such as the genera
Plasmodium,
Haemoproteus and
Leucocytozoon (phylum Apicomplexa) are obligate blood parasites found in most bird species worldwide [
1], transmitted by dipteran vectors [
2]. Although genera of avian haemosporidia are not reciprocally monophyletic groups [
3,
4], current taxonomy helps to understand that richness of parasite lineages may be highly underestimated [
5]. Avian haemosporidians further exhibit high genetic diversity, but the understanding of its distribution across a large geographical scale is incipient.
Spatial distributional patterns of species diversity linking host-parasite relationships are an active topic of ecology and biogeography. The diversity of parasites varies considerably among ecologically distinct habitats [
6], and environmental variables seem promising in predicting on large-scale spatial assessment of parasite prevalence [
7,
8]. However, little is known about the influence of host assemblages as a change-effect factor of the evolution and spread of parasite diversity. The region of the tropical Andes is constituted by the northern and central Andes, sheltering
ca. 20% of the global avian fauna [
9]. In this region some studies have focused on local estimates of prevalence in multiple hosts species, as in Venezuela [
10], Colombia [
11,
12] and Ecuador [
4]. Very few studies have used a more regional approach to examine the prevalence of avian haemosporidia, but this has been made on specific avian hosts [
13,
14].
For studies of avian malaria parasites, the mitochondrial cytochrome
b gene (cyt
b) has become a popular molecular marker to rapidly gather phylogenetic information on
Plasmodium,
Haemoproteus and
Leucocytozoon [
15‐
17]. However, these studies are often not the subject of direct comparison because different criteria of cyt
b divergence are used to identify lineages [
18]. The lack of a uniform-criterion to identify lineages hinders any comprehensive, comparative analysis of the haemosporidians genetic variation in a broader geographic and host diversity context. An alternative to this is to establish the limits of haemosporidian lineages based on cyt
b polymorphism, by defining operative taxonomic units to facilitate data comparison among studies of local variation of parasites [
17].
Here a meta-analysis shows spatial patterns of avian malaria genetic diversity on a regional scale for the tropical Andes and areas of endemism nearby. Further, a methodological approach is provided for examining how richness and turnover of haemosporidian parasites may vary according to areas of host endemism and elevation following assemblages of montane avian fauna.
Discussion
Avian haemosporidia accessions in the GenBank and MalAvi databases used here show infection for roughly 14.2% of bird species with distribution in the Neotropics and 26.8% of the haplogroups including the tropical Andes in their geographical range. The cut-off level ≥ 99.3% sequence similarity to determine haplogroups (or ≈ 0.7% of differentiation among sequences) used in this study accounts for variation in haemosporidia that could be considered intraspecific, interspecific or both. Overall, the cyt
b gene can vary in sequence identity from 0.1 to 9.2% within well-supported haemosporidia species [
17,
34]. The resulting set of haplotype groups after using the less stringent clustering method than that commonly applied for cyt
b sequence divergence further suggest that this is a cautious approach to examine avian haemosporidia mtDNA variation. In contrast, the phylogeny shown here is of very limited use to determine operative taxonomical units, because: (i) as opposed to a
Leucocytozoon well-supported clade,
Plasmodium and
Haemoproteus haplotypes exhibit a paraphyletic pattern; and further, (ii) strict clade support occurs only for 28% of the tree nodes if the phylogeny were fully resolved, a pattern consistent with previous phylogenetic inferences [
4,
16].
The meta-analysis shown here contributes to the understanding of how assemblages of host communities may play a determinant role on the spatial distribution of parasites genetic diversity. It is important to emphasize that the nucleotide variation of
Plasmodium and
Haemoproteus distorts from a linear correlation with elevation. This suggests further support to the complex relationship between parasite richness and spatial distributions [
35,
36]. In contrast, the total number of haemosporidia haplogroups peaks at mid-elevation, such a curve is strikingly consistent to the unimodal pattern for richness of montane avian fauna in the tropical Andes that also peaks towards 2000–2500 masl (see Fig. 5 in [
31]). Therefore, the richness of avian haemosporidian forms at the mid-elevation may be influenced by the richness of montane birds susceptible to infection in this elevational zone [
37].
In the tropical Andes, it was found that cyt
b gene variation in avian haemosporidia is accumulated
within rather than
among elevation ranges. The distribution of haplogroups among areas of host endemism can explain roughly 9 and 23% of the cyt
b variation for
Plasmodium–
Haemoproteus and
Leucocytozoon, respectively. Clearly, areas that comprise avian fauna that exhibit phylogenetic and distributional congruence in the Neotropical region [
38] are also congruent with the spatial distribution of the genetic variation of obligate blood parasites, as avian haemosporidia. In addition, the amplification of the avian haemosporidia genetic diversity in mid-elevation of the tropical Andes is consistent with prevalence peaks at mid-elevation documented on a local scale for the
Plasmodium and
Haemoproteus in the Andes of Colombia, Ecuador and Peru [
4,
11,
13,
14]. It stands to reason that if the local array of hosts in a habitat is higher at mid-elevation as in the tropical Andes, the number of parasites would get amplified in order to exploit host opportunity [
3,
14,
35]. Therefore, host opportunities for haemosporidian parasites may increase as the endemism of montane bird populations increases towards middle and upper elevations in the tropical Andes [
39]. Collectively, reports of local prevalence of avian malaria parasites across the tropical Andes are consistent with how the large geographical scale pattern of haemosporidia genetic variation varies according to regional assemblages of avian hosts.
The phylogeny shows that 20.3% of the haplotype groups are distributed in two or more of the eight intervals of 500 m in altitude in the tropical Andes. These haemosporidian haplotypes forms are spatially generalists to infect avian hosts along elevation. Turnover of haemosporidians also shows a dramatic increasing overlap of haplotype assemblages among adjacent zones towards mid-elevation. This pattern minimally means that more homogeneous genetic assemblages of obligate blood parasites towards mid-elevation, where parasite diversity peaks. Such an assemblage of overlapping haplotypes succeeded in exploiting zones of the richest host habitats where also avian diversity tends to be maximized in the tropical Andes [
30,
31]. This finding suggests that parasites that can exploit host diversity are likely a better fit to habitats rich in hosts [
6]. Nevertheless, the groups of generalist haplotypes for elevation in the database are a minority of haemosporidia forms in the tropical Andes.
In contrast, 79.5% of the haplotype groups are restricted to one and only one elevational range among the eight intervals of 500 m in altitude in the tropical Andes; thus, more than three-quarters of haemosporidian haplotypes are elevation restricted to infect hosts. For instance, consistent with results here, it is well documented that
Leucocytozoon is mainly restricted to the highlands, where they are likely prevailing at lower temperatures and where their vectors are common as well [
40]. According to the results of this study, most haemosporidians could be restricted to certain elevation ranges to infect montane bird species because avian hosts also have a more or less limited distribution by altitudinal zones in the tropical Andes [
41]. This spatial distribution pattern could also be limited by the dynamics of the vectors, as observed on Hawaii island [
42]. Unfortunately for the tropical Andes, little is known about the influence of vectors on avian malaria infection yet.
Authors’ contributions
RS developed the concept and analytical framework. DG conducted most analysis. Both authors read and approved the final manuscript.