New species and records of Laboulbeniales from the subantarctic islands of New Zealand

Until now Rhachomyces kenodactyli Balazuc & W. Rossi has been the only species of Laboulbeniales known to occur on Coleoptera in the Bounty, Antipodes, Auckland, Campbell and Snares Islands, which lie 48° to 35° S. Four new species (Diphymyces depressus, Diphymyces leschenii, Laboulbenia subantarctica and Laboulbenia loxomeri) and five new records for the subantarctic (Cucujomyces phycophilus, Diphymyces penicillifer, Laboulbenia sp. 1, Rhachomyces sp. 1 and Teratomyces sp. 1) are reported, increasing the known number of taxa tenfold. An expanded geographic range for Rhachomyces kenodactyli is reported. A relatively high percentage (12%) of known beetle species in the subantarctic serve as hosts for Laboulbeniales. This host utilization rate is higher than that in tropical and north temperate regions. The high proportion of intertidal coleopteran taxa in the subantarctic fauna probably accounts for the greater number of host species utilized. Fungi on intertidal beetles (Omaliinae [Staphylinidae], Oopterus [Carabidae] and Kenodactylus audouini [Carabidae]) are known from many host individuals and collections, while those on terrestrial species are known from few, and in some cases, a single collection or host. The sporadic occurrence of some species encountered increases the likelihood that a few species of Laboulbeniales on Coleoptera probably remain undiscovered in the region.     

The relative importance of trees versus lianas as hosts for phytophagous beetles (Coleoptera) in tropical forests

Aim Insect assemblages associated with lianas in tropical forests are poorly studied compared with those associated with trees. The importance of lianas for the maintenance of local species richness of insect herbivores in tropical forests is therefore poorly understood. With this in mind, a comparative study of the relative importance of trees and lianas as hosts for phytophagous beetles was carried out. Location The study area was located in the canopy of a dry tropical forest in Parque Natural Metropolitano, Panama province, Republic of Panama. Methods A crane system was utilized to access the canopy. The number of species and host specialization of adult phytophagous beetles associated with twenty‐six liana species of ten different families, and twenty‐four tree species of twelve different families were compared. Results A total of 2561 host associations of 697 species of beetles were determined (1339 for trees and 1222 for lianas). On average 55.8 ± 6.8 beetle species were found to be associated with each tree species while the comparable number for lianas was 47.0 ± 6.1. The pooled numbers of phytophagous beetle species associated with trees and lianas, respectively, were not significantly different. However, there were significantly more species feeding on green plant parts on lianas than on trees, and there were significantly more wood eaters on trees than on lianas. Phytophagous beetles associated with lianas were significantly more specialized than the tree associates due to a higher degree of specialization among the species feeding on green plant parts of lianas. Wood eaters and flower visitors showed no differences in host specialization on different growth forms. Main conclusion The present study shows that lianas are at least as important as trees for the maintenance of local species diversity of phytophagous beetles at this site. The mechanisms that drive the patterns can only be hypothesized. Plant architecture, size, and length of growing season are probably involved. Further studies, should include measurements of plant traits to elucidate experimentally what mechanisms that drive the patterns. Additional insight would come from similar studies in other forest types, and also studies of other major taxonomic groups of arthropod herbivores.     

Host age determines parasite load of Laboulbeniales fungi infecting ants: Implications for host-parasite relationship and fungal life history

Arthropod-parasitic fungi of the order Laboulbeniales are known to exhibit specialization to individual host taxa in most cases. Some species exhibit ecological specificity to multiple, often unrelated hosts in certain microhabitats; and often position specificity to different host body parts. The myrmecophilous Rickia wasmannii (Ascomycota: Laboulbeniales) infects Myrmica species (Hymenoptera: Formicidae) (host specificity), and occasionally other arthropod inquilines inside the ant nest (ecological specificity). An effect of the position of infection on the thallus densities has also been reported. Another determinative factor that may also exist in the Rickia-Myrmica host-parasite system, the chronological age of ant worker hosts, has also been linked to parasite load. Comprehensive studies on the age-related infection intensity, however, are still lacking. Here we investigated whether the level of infection correlates with the age of the M. scabrinodis host consistently. We found that older hosts exhibited higher parasite load, even though the infection level of the different colonies varied widely. The results highlight that the level of R. wasmannii infections are strongly influenced by host individual and host colony factors.     

Wolbachia distribution in selected beetle taxa characterized by PCR screens and MLST data

Wolbachia (Alphaproteobacteria) is an inherited endosymbiont of arthropods and filarial nematodes and was reported to be widespread across insect taxa. While Wolbachia's effects on host biology are not understood from most of these hosts, known Wolbachia‐induced phenotypes cover a spectrum from obligate beneficial mutualism to reproductive manipulations and pathogenicity. Interestingly, data on Wolbachia within the most species‐rich order of arthropods, the Coleoptera (beetles), are scarce. Therefore, we screened 128 species from seven beetle families (Buprestidae, Hydraenidae, Dytiscidae, Hydrophilidae, Gyrinidae, Haliplidae, and Noteridae) for the presence of Wolbachia. Our data show that, contrary to previous estimations, Wolbachia frequencies in beetles (31% overall) are comparable to the ones in other insects. In addition, we used Wolbachia MLST data and host phylogeny to explore the evolutionary history of Wolbachia strains from Hydraenidae, an aquatic lineage of beetles. Our data suggest that Wolbachia from Hydraenidae might be largely host genus specific and that Wolbachia strain phylogeny is not independent to that of its hosts. As this contrasts with most terrestrial Wolbachia–arthropod systems, one potential conclusion is that aquatic lifestyle of hosts may result in Wolbachia distribution patterns distinct from those of terrestrial hosts. Our data thus provide both insights into Wolbachia distribution among beetles in general and a first glimpse of Wolbachia distribution patterns among aquatic host lineages.     

Dose-independent virulence in phoretic mites that parasitize burying beetles

Virulence, the negative impact of parasites on their hosts, typically increases with parasite dose. Parasites and hosts often compete for host resources and more parasites will consume more resources. Depending on the mechanism of competition, increasing host resources can benefit the host. Additional resources can also be harmful when the parasites are the main beneficiaries. Then, the parasites will thrive and virulence increases. While parasite dose is often easy to manipulate, it is less trivial to experimentally scale host resources. Here, we study a system with external host resources that can be easily manipulated: Nicrophorus burying beetles reproduce on vertebrate carcasses, with larger carcasses yielding more beetle offspring. Phoretic Poecilochirus mites reproduce alongside the beetles and reduce beetle fitness. The negative effect of mites could be due to competition for the carrion between beetle and mite offspring. We manipulated mite dose and carcass size to better understand the competition between the symbionts. We found that mite dose itself was not a strong predictor of virulence. Instead, the number of mite offspring determined beetle fitness. At larger doses, there was strong competition among adult parental mites as well as mite offspring. While increasing the carcass size increased both host and parasite fitness, it did surprisingly little to alleviate the negative effect that mites had on beetles. Instead, relative virulence was stronger on large carcasses, indicating that the parasites appropriate more of the additional resources. Our results demonstrate an ecological influence on the selection of parasites on their hosts and suggest that virulence can be dose-independent in principle.     

Experimental assemblage of novel plant–herbivore interactions: ecological host shifts after 40 million years of isolation

Geographic isolation is the first step in insect herbivore diet specialization. Such specialization is postulated to increase insect fitness, but may simultaneously reduce insect ability to colonize novel hosts. During the Paleocene‐Eocene, plants from the order Zingiberales became isolated either in the Paleotropics or in the Neotropics. During the Cretaceous, rolled‐leaf beetles diversified in the Neotropics concurrently with Neotropical Zingiberales. Using a community of Costa Rican rolled‐leaf beetles and their Zingiberales host plants as study system, we explored if previous geographic isolation precludes insects to expand their diets to exotic hosts. We recorded interactions between rolled‐leaf beetles and native Zingiberales by combining DNA barcodes and field records for 7450 beetles feeding on 3202 host plants. To determine phylogenetic patterns of diet expansions, we established 20 experimental plots in the field, in which we planted plots five exotic Zingiberales, recording beetles feeding on these exotic hosts. In the laboratory, using both native and exotic host plants, we reared a subset of insect species that had expanded their diets to the exotic plants. The original plant–herbivore community comprised 24 beetle species feeding on 35 native hosts, representing 103 plant–herbivore interactions. After exotic host plant introduction, 20 percent of the beetle species expanded their diets to exotic Zingiberales. Insects only established on exotic hosts that belong to the same plant family as their native hosts. Laboratory experiments show that beetles are able to complete development on these novel hosts. In conclusion, rolled‐leaf beetles are preadapted to expand their diets to novel host plants even after millions of years of geographic isolation.     

Pristionchus uniformis,should I stay or should I go? Recent host range expansion in a European nematode

Pristionchus pacificus has been developed as a model system in evolutionary developmental biology, evolutionary ecology, and population genetics. This species has a well-known ecological association with scarab beetles. Generally, Pristionchus nematodes have a necromenic association with their beetle hosts. Arrested dauer larvae invade the insect and wait for the host's death to resume development. Only one Pristionchus species is known to frequently associate with a non-scarab beetle. Pristionchus uniformis has been isolated from the chrysomelid Leptinotarsa decemlineata, also known as the Colorado potato beetle, in Europe and North America, but is also found on scarab beetles. This unusual pattern of association with two unrelated groups of beetles on two continents requires the involvement of geographical and host range expansion events. Here, we characterized a collection of 81 P. uniformis isolates from North America and Europe and from both scarab beetles and L. decemlineata. We used population genetic and phylogenetic analyses of the mitochondrial gene nd2 to reconstruct the genetic history of P. uniformis and its beetle association. Olfactory tests on beetles chemical extracts showed that P. uniformis has a unique chemoattractive profile toward its beetle hosts. Our results provide evidence for host range expansion through host-switching events in Europe where P. uniformis was originally associated with scarab beetles and the nematode's subsequent invasion of North America.     

Host-associated differences in fitness within and between populations of a seed beetle (Bruchidae): effects of plant variability

Summary Experiments were conducted with the sexually reproducing seed beetle Stator limbatus and its hosts in north-central Arizona to determine if it was substructured into units, each specialized for higher fitness on a specific host species. Unlike many studies, we incorporated scale, i.e., conducting experiments between and within beetle populations on seeds from within and between plant species. Of particular interest was whether intraspecific plant variability prevented beetle specialization within beetle populations. Results suggest that S. limbatus is specialized to certain hosts. On the palo verde Cercidium floridum, beetles originally reared from this host had significantly higher emergence compared to beetles transferred from other hosts. We did not test directly for a genetic basis for this. Alternative hypotheses of variation in symbiotic microorganisms in larval guts and maternal effects were assessed. Essentially no bacteria, yeast or protozoa were found, and maternal effects as expressed by varying egg weights were not detected; however, other microorganisms might have been present and maternal effects through inducible enzymes was possible. Caution, then, is needed in any genetic interpretations of our results. The differences on C. floridum were detected from tests between and within beetle populations. Evidence for specialization was not detected on the other hosts, Cercidium microphyllum and Acacia greggii. On the other hosts, beetles performed well regardless of their source. Significant differences were detected among individual plants of C. floridum as to the suitability of their seeds for deveoopment of S. limbatus. No such differences were detected among the other host plants. These patterns of conspecific plant variability are opposite of what is expected if plant variability prevents specialization of beetles to particular species of hosts. Thus, the data suggest seed variability among plants does not prevent specialization to host species in this system. We discuss how the patterns of host use in this study relate to the hypothesis of sympatric host race formation.     

Host plant scents attract rolled-leaf beetles to Neotropical gingers in a Central American tropical rain forest

Leaf volatile chemicals are known to reduce herbivory rates by repelling or intoxicating insect herbivores and by attracting the predators and parasitoids of herbivores. However, leaf volatiles may also be used by insect herbivores as cues to locate their host plants. Leaf volatiles are suggested to be important host search cues for herbivores in structurally complex and diverse habitats, such as tropical rain forests. A group of insect herbivores, the rolled-leaf beetles (Coleoptera: Chrysomelidae: Hispinae), have maintained a highly specialized interaction with Neotropical gingers (Zingiberales) for ca. 60 million years. In this study, we explored chemical attraction to host plants under controlled laboratory conditions, using four sympatric rolled-leaf beetle species, Cephaloleia dorsalis Baly, Cephaloleia erichsonii Baly, Cephaloleia fenestrata Weise, and Cephaloleia placida Baly. For each beetle species, we investigated (i) whether it was repelled or attracted by leaf scents produced by four host and four non-host plant species, including Neotropical gingers in the families Marantaceae, Costaceae, and Zingiberaceae; and (ii) its ability to use scents to detect its host plant. We found that rolled-leaf beetles can detect and are attracted by leaf volatiles from both host and non-host gingers. Additionally, when beetles were simultaneously exposed to leaf volatiles from host and non-host plants, three rolled-leaf beetle species were significantly more attracted by volatiles from their host plants than from non-hosts. Only one of the beetle species was not able to discriminate between host and non-host scents.     

The bacterial community of entomophilic nematodes and host beetles

Insects form the most species‐rich lineage of Eukaryotes and each is a potential host for organisms from multiple phyla, including fungi, protozoa, mites, bacteria and nematodes. In particular, beetles are known to be associated with distinct bacterial communities and entomophilic nematodes. While entomopathogenic nematodes require symbiotic bacteria to kill and reproduce inside their insect hosts, the microbial ecology that facilitates other types of nematode–insect associations is largely unknown. To illuminate detailed patterns of the tritrophic beetle–nematode–bacteria relationship, we surveyed the nematode infestation profiles of scarab beetles in the greater Los Angeles area over a five‐year period and found distinct nematode infestation patterns for certain beetle hosts. Over a single season, we characterized the bacterial communities of beetles and their associated nematodes using high‐throughput sequencing of the 16S rRNA gene. We found significant differences in bacterial community composition among the five prevalent beetle host species, independent of geographical origin. Anaerobes Synergistaceae and sulphate‐reducing Desulfovibrionaceae were most abundant in Amblonoxia beetles, while Enterobacteriaceae and Lachnospiraceae were common in Cyclocephala beetles. Unlike entomopathogenic nematodes that carry bacterial symbionts, insect‐associated nematodes do not alter the beetles' native bacterial communities, nor do their microbiomes differ according to nematode or beetle host species. The conservation of Diplogastrid nematodes associations with Melolonthinae beetles and sulphate‐reducing bacteria suggests a possible link between beetle–bacterial communities and their associated nematodes. Our results establish a starting point towards understanding the dynamic interactions between soil macroinvertebrates and their microbiota in a highly accessible urban environment.     

Host specificity of ambrosia and bark beetles (Col., Curculionidae: Scolytinae and Platypodinae) in a New Guinea rainforest

Abstract.  1. Bark and ambrosia beetles are crucial for woody biomass decomposition in tropical forests worldwide. Despite that, quantitative data on their host specificity are scarce.
2. Bark and ambrosia beetles (Scolytinae and Platypodinae) were reared from 13 species of tropical trees representing 11 families from all major lineages of dicotyledonous plants. Standardised samples of beetle-infested twigs, branches, trunks, and roots were taken from three individuals of each tree species growing in a lowland tropical rainforest in Papua New Guinea.
3. A total of 81 742 beetles from 74 species were reared, 67 of them identified. Local species richness of bark and ambrosia beetles was estimated at 80–92 species.
4. Ambrosia beetles were broad generalists as 95% of species did not show any preference for a particular host species or clade. Similarity of ambrosia beetle communities from different tree species was not correlated with phylogenetic distances between tree species. Similarity of ambrosia beetle communities from individual conspecific trees was not higher than that from heterospecific trees and different parts of the trees hosted similar ambrosia beetle communities, as only a few species preferred particular tree parts.
5. In contrast, phloeophagous bark beetles showed strict specificity to host plant genus or family. However, this guild was poor in species (12 species) and restricted to only three plant families (Moraceae, Myristicaceae, Sapindaceae).
6. Local diversity of both bark and ambrosia beetles is not driven by the local diversity of trees in tropical forests, since ambrosia beetles display no host specificity and bark beetles are species poor and restricted to a few plant families.     

Species richness and regional distribution of myrmecophilous beetles

Four major hypotheses have been put forward to explain local species richness of commensal or parasitic species. The resource distribution hypothesis predicts that regionally widespread host species are able to support higher local species richness of commensals or parasites. On the other hand, the resource size hypothesis predicts that larger hosts can support more species than smaller hosts, and comparably, the resource abundance hypothesis predicts that hosts that offer more resources are able to support more species. Finally, the resource concentration hypothesis predicts that hosts that occur in high-density patches support higher species richness. In this study, we tested the first three of the above hypotheses with myrmecophilous beetles and their host ants. In addition to species richness of myrmecophilous beetles, we also applied the above hypotheses to explain the distribution of the beetles. Our data are exclusively based on an extensive literature survey. Myrmecophilous beetles live in naturally fragmented environments composed of host ant colonies and they are exclusively dependent on ants. We found that the distribution of the host ants and the colony size of the host ants had a positive effect on both the species richness and the distribution of myrmecophilous beetles. In the same way, we found that myrmecophilous beetle species that are generalists, i.e. have more than one host ant species, and thus have more abundant resources, were more widely distributed than specialist species. Thus, we found support for the hypothesis that resource distribution, resource size and resource abundance have an effect on species richness and on the distribution of species.     

First Central European record of the fungus Prolixandromyces triandrus Santam. (Ascomycota: Laboulbeniales), a parasite of veliid bugs (Heteroptera: Veliidae), with notes on its biology and DNA barcoding

A new distribution record for Prolixandromyces triandrus Santam. (Ascomycota: Laboulbeniales) is presented from the Bükk Mountains in northeastern Hungary, from the host species Velia (Plesiovelia) saulii Tamanini, 1947 (Heteroptera: Veliidae). Hitherto, this fungal parasite had only been observed in the western Mediterranean region and the Macaronesia Archipelago. Prolixandromyces. triandrus seems to be abundant in the reported Hungarian host population. Additionally, ribosomal DNA barcodes for this fungal species are also presented. Incidence of the parasite and potential of the molecular investigations of host-parasite relationships of this ectoparasitic fungus is discussed. A brief review is given of known hosts of P. triandrus and of Laboulbeniales from aquatic/semiaquatic insect hosts in Hungary.     

Laboulbeniales hyperparasites (Fungi,Ascomycota) of bat flies: Independent origins and host associations

The aim of this study was to explore the diversity of ectoparasitic fungi (Ascomycota, Laboulbeniales) that use bat flies (Diptera, Hippoboscoidea) as hosts. Bat flies themselves live as ectoparasites on the fur and wing membranes of bats (Mammalia, Chiroptera); hence this is a tripartite parasite system. Here, we collected bats, bat flies, and Laboulbeniales, and conducted phylogenetic analyses of Laboulbeniales to contrast morphology with ribosomal sequence data. Parasitism of bat flies by Laboulbeniales arose at least three times independently, once in the Eastern Hemisphere (Arthrorhynchus) and twice in the Western Hemisphere (Gloeandromyces, Nycteromyces). We hypothesize that the genera Arthrorhynchus and Nycteromyces evolved independently from lineages of ectoparasites of true bugs (Hemiptera). We assessed phylogenetic diversity of the genus Gloeandromyces by considering the LSU rDNA region. Phenotypic plasticity and position‐induced morphological adaptations go hand in hand. Different morphotypes belong to the same phylogenetic species. Two species, G. pageanus and G. streblae, show divergence by host utilization. In our assessment of coevolution, we only observe congruence between the Old World clades of bat flies and Laboulbeniales. The other associations are the result of the roosting ecology of the bat hosts. This study has considerably increased our knowledge about bats and their associated ectoparasites and shown the necessity of including molecular data in Laboulbeniales taxonomy.     

The contribution of cacao agroforests to the conservation of lower canopy ant and beetle diversity in Indonesia

The ongoing destruction of tropical rainforests has increased the interest in the potential value of tropical agroforests for the conservation of biodiversity. Traditional, shaded agroforests may support high levels of biodiversity, for some groups even approaching that of undisturbed tropical forests. However, it is unclear to what extent forest fauna is represented in this diversity and how management affects forest fauna in agroforests. We studied lower canopy ant and beetle fauna in cacao agroforests and forests in Central Sulawesi, Indonesia, a region dominated by cacao agroforestry. We compared ant and beetle species richness and composition in forests and cacao agroforests and studied the impact of two aspects of management intensification (the decrease in shade tree diversity and in shade canopy cover) on ant and beetle diversity. The agroforests had three types of shade that represented a decrease in tree diversity (high, intermediate and low diversity). Species richness of ants and beetles in the canopies of the cacao trees was similar to that found in lower canopy forest trees. However, the composition of ant and beetle communities differed greatly between the agroforest and forest sites. Forest beetles suffered profoundly from the conversion to agroforests: only 12.5% of the beetle species recorded in the forest sites were also found in the agroforests and those species made up only 5% of all beetles collected from cacao. In contrast, forest ants were well represented in agroforests, with 75% of all species encountered in the forest sites also occurring on cacao. The reduction of shade tree diversity had no negative effect on ants and beetles on cacao trees. Beetle abundances and non-forest ant species richness even increased with decreasing shade tree diversity. Thinning of the shade canopy was related to a decrease in richness of forest ant species on cacao trees but not of beetles. The contrasting responses of ants and beetles to shade tree management emphasize that conservation plans that focus on one taxonomic group may not work for others. Overall ant and beetle diversity can remain high in shaded agroforests but the conservation of forest ants and beetles in particular depends primarily on the protection of natural forests, which for forest ants can be complemented by the conservation of adjacent shaded cacao agroforests.     

ALLOZYME AND MORPHOLOGICAL DIFFERENTIATION OF MOUNTAIN PINE BEETLES DENDROCTONUS PONDEROSAE HOPKINS (COLEOPTERA: SCOLYTIDAE) ASSOCIATED WITH HOST TREE

The purpose of this study was to determine whether mountain pine beetles utilizing different host species were differentiated for either morphological or protein variation. Genetic differentiation among host species has been reported for the southern pine beetle, the Douglas-fir beetle, the jeffrey pine beetle, and the mountain pine beetle. However, in these studies, the host trees were sampled at separate sites, and hence geographic variation and variation due to host tree were confounded. The mountain pine beetle occasionally utilizes three host trees (ponderosa pine, lodgepole pine, and limber pine) at single sites in Colorado. Five polymorphic enzyme loci and six morphological characters were used to describe beetles resident in different hosts. Differentiation within a site among host trees was detected at two of five polymorphic proteins, and for both size and morphological shape. The magnitude of genetic differentiation among hosts within a site was approximately equivalent to the magnitude of differentiation among sites. These data suggest that the species of host tree may be an important biotic factor associated with the genetic structure of bark beetle communities. The results are discussed in terms of their potential role in the process of speciation by host race formation.     

The importance of plant relatedness for host utilization among phytophagous insects

Current methods for measuring similarity among phytophagous insect communities fail to consider the phylogenetic relationship between host plants. We analysed this relation based on 3580 host observations of 1174 beetle species associated with 100 species of angiosperms in two different forest types in Panama. We quantified the significance of genetic distance as well as taxonomic rank among angiosperms in relation to species overlap in beetle assemblages. A logarithmic model describing the decrease in beetle species similarity between host-plant species of increasing phylogenetic distance explains 35% of the variation. Applied to taxonomic rank categories the results imply that except for the ancient branching of monocots from dicots, only adaptive radiations of plants on the family and genus level are important for host utilization among phytophagous beetles. These findings enable improvements in estimating host specificity and species richness through correction for phylogenetic relatedness between hosts and consideration of the host-specific fauna associated with monocots.     

Differential host defense against multiple parasites in ants

Host–parasite interactions are ideal systems for the study of coevolutionary processes. Although infections with multiple parasite species are presumably common in nature, most studies focus on the interactions of a single host and a single parasite. To the best of our knowledge, we present here the first study on the dependency of parasite virulence and host resistance in a multiple parasite system. We evaluated whether the strength of host defense depends on the potential fitness cost of parasites in a system of two Southeast Asian army ant hosts and five parasitic staphylinid beetle species. The potential fitness costs of the parasites were evaluated by their predation behavior on host larvae in isolation experiments. The host defense was assessed by the ants’ aggressiveness towards parasitic beetle species in behavioral studies. We found clear differences among the beetle species in both host–parasite interactions. Particular beetle species attacked and killed the host larvae, while others did not. Importantly, the ants’ aggressiveness was significantly elevated against predatory beetle species, while non-predatory beetle species received almost no aggression. As a consequence of this defensive behavior, less costly parasites are more likely to achieve high levels of integration in the ant society. We conclude that the selection pressure on the host to evolve counter-defenses is higher for costly parasites and, thus, a hierarchical host defense strategy has evolved that depends on the parasites’ impact.     

Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity

Knowing the genetic variation that occurs in pathogen populations and how it is distributed across geographical areas is essential to understand parasite epidemiology, local patterns of virulence, and evolution of host‐resistance. In addition, it is important to identify populations of pathogens that are evolutionarily independent and thus ‘free’ to adapt to hosts and environments. Here, we investigated genetic variation in the globally distributed, highly invasive avian malaria parasite Plasmodium relictum, which has several distinctive mitochondrial haplotyps (cyt b lineages, SGS1, GRW11 and GRW4). The phylogeography of P. relictum was accessed using the highly variable nuclear gene merozoite surface protein 1 (MSP1), a gene linked to the invasion biology of the parasite. We show that the lineage GRW4 is evolutionarily independent of GRW11 and SGS1 whereas GRW11 and SGS1 share MSP1 alleles and thus suggesting the presence of two distinct species (GRW4 versus SGS1 and GRW11). Further, there were significant differences in the global distribution of MSP1 alleles with differences between GRW4 alleles in the New and the Old World. For SGS1, a lineage formerly believed to have both tropical and temperate transmission, there were clear differences in MSP1 alleles transmitted in tropical Africa compared to the temperate regions of Europe and Asia. Further, we highlight the occurrence of multiple MSP1 alleles in GRW4 isolates from the Hawaiian Islands, where the parasite has contributed to declines and extinctions of endemic forest birds since it was introduced. This study stresses the importance of multiple independent loci for understanding patterns of transmission and evolutionary independence across avian malaria parasites.