Lessons from parasitic flatworms about evolution and historical biogeography of their vertebrate hosts

Cophylogenetic studies investigate the evolutionary trends within host-parasite associations. Examination of the different levels of fidelity between host and parasite phylogenies provides a powerful tool to inspect patterns and processes of parasite diversification over host evolution and geological times. Within the phylum Platyhelminthes, the monogeneans are mainly fish parasites. The Polystomatidae, however, are known from the sarcopterygian Australian lungfish and tetrapods such as amphibians, freshwater turtles, and the African hippopotamus. Cophylogenetic and biogeographic vicariance analyses, supplemented by molecular calibrations, showed that the Polystomatidae may track the evolutionary history of the first aquatic tetrapods in the Palaeozoic age. Evolutionary lines of the major polystome lineages would also be intimately related to the evolution of their hosts over hundreds of millions years. Since the Mesozoic, evolution of polystomes would have been shaped mainly by plate tectonics during the break-up of Gondwanaland and subsequent dispersal of ancestral neobatrachian host lineages. Therefore the Polystomatidae could serve as a novel model to improve cophylogenetic tools and to inspect a suite of questions about the evolution of vertebrate hosts. To cite this article: O. Verneau et al., C. R. Biologies 332 (2009).     

Origin and evolution of African Polystoma (Monogenea: Polystomatidae) assessed by molecular methods

Among Polystomatidae (Monogenea), the genus Polystoma, which mainly infests neobatrachian hosts, is the most diverse and occurs principally in Africa, from where half the species have been reported. Previous molecular phylogenetic studies have shown that this genus originated in South America, and later colonised Eurasia and Africa. No mention was made on dispersal corridors between Europe and Africa or of the origin of the African Polystoma radiation. Therefore, a molecular phylogeny was inferred from ITS1 sequences of 21 taxa comprising two species from America, seven representatives from Europe and 12 from Africa. The topology of the phylogenetic tree reveals that a single event of colonisation took place from Europe to Africa and that the putative host carrying along the ancestral polystome is to be found among ancestral pelobatids. Percentage divergences estimates suggest that some presumably distinct vesicular species in unrelated South African anurans and some neotenic forms found in several distinct hosts in Ivory Coast, could, in fact, belong to two single polystome species parasitising divergent hosts. Two main factors are identified that may explain the diversity of African polystomes: (i), we propose that following some degree of generalism, at least during the juvenile stages of both hosts and parasites, distinctive larval behaviour of polystomes engenders isolation between parasite populations that precludes sympatric speciations; (ii), cospeciation events between Ptychadena hosts and their parasites are another factor of diversification of Polystoma on the African continent. Finally, we discuss the systematic status of the Madagascan parasite Metapolystoma, as well as the colonisation of Madagascar by the host Ptychadena mascareniensis.     

Avian host composition,local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds

Identifying the ecological factors that shape parasite distributions remains a central goal in disease ecology. These factors include dispersal capability, environmental filters and geographic distance. Using 520 haemosporidian parasite genetic lineages recovered from 7,534 birds sampled across tropical and temperate South America, we tested (a) the latitudinal diversity gradient hypothesis and (b) the distance–decay relationship (decreasing proportion of shared species between communities with increasing geographic distance) for this host–parasite system. We then inferred the biogeographic processes influencing the diversity and distributions of this cosmopolitan group of parasites across South America. We found support for a latitudinal gradient in diversity for avian haemosporidian parasites, potentially mediated through higher avian host diversity towards the equator. Parasite similarity was correlated with climate similarity, geographic distance and host composition. Local diversification in Amazonian lineages followed by dispersal was the most frequent biogeographic events reconstructed for haemosporidian parasites. Combining macroecological patterns and biogeographic processes, our study reveals that haemosporidian parasites are capable of circumventing geographic barriers and dispersing across biomes, although constrained by environmental filtering. The contemporary diversity and distributions of haemosporidian parasites are mainly driven by historical (speciation) and ecological (dispersal) processes, whereas the parasite community assembly is largely governed by host composition and to a lesser extent by environmental conditions.     

Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles

We recovered 26 genetically distinct avian malaria parasite lineages, based on cytochrome b sequences, from a broad survey of terrestrial avifauna of the Lesser Antilles. Here we describe their distributions across host species within a regional biogeographic context. Most parasite lineages were recovered from a few closely related host species. Specialization on one host species and distribution across many hosts were both rare. Geographic patterns of parasite lineages indicated limited dispersal and frequent local extinction. The central islands of the archipelago share similar parasite lineages and patterns of infection. However, the peripheral islands harbor well-differentiated parasite communities, indicating long periods of isolation. Nonetheless, 20 of 26 parasite lineages were recovered from at least one of three other geographic regions, the Greater Antilles, North America, and South America, suggesting rapid dispersal relative to rate of differentiation. Six parasite lineages were restricted to the Lesser Antilles, primarily to endemic host species. Host differences between populations of the same parasite lineage suggest that host preference may evolve more rapidly than mitochondrial gene sequences. Taken together, distributions of avian malarial parasites reveal evidence of coevolution, host switching, extinction, and periodic recolonization events resulting in ecologically dynamic as well as evolutionarily stable patterns of infection.     

Amphisbaenian paleobiogeography: Evidence of vicariance and geodispersal patterns

Paleobiogeographic patterns within the Amphisbaenia were evaluated using the modified Brooks Parsimony Analysis (BPA) and recently published morphological and molecular phylogenies. Extant amphisbaenians are present in Africa, South America, North America, Europe, and the Middle East. The modified BPA was used to determine the relative effects of Pangean breakup, sea-level change, and climate change on evolutionary and distributional patterns within the Amphisbaenia. The modified BPA also tested the biogeographic effect of the Rhineuridae's phylogenetic position as either most basal in the morphologic phylogeny or most derived in the molecular phylogeny. The morphological and molecular analyses resulted in two different biogeographic hypotheses. The morphological analysis indicated three major biogeographic regions for the Amphisbaenia: 1) Africa, South America, and the Caribbean, 2) western Asia, and 3) North America. The molecular analysis indicated two major biogeographic regions: 1) Africa, western Asia, and North America, and 2) South America. The morphological biogeographic pattern corresponds with the known timing of the breakup of Pangea and the resulting paleogeographic reconstructions of the Mesozoic and Early Cenozoic. While the molecular pattern is similar to patterns recovered from dinosaurian biogeographic studies, the closer connection of Africa with North America rather than South America does not match well-constrained geologic evidence for the sequence of Pangean breakup. Both paleobiogeographic analyses, however, resulted in congruent patterns of speciation through vicariance and geodispersal. This suggests that in addition to the breakup of Pangea, such cyclical Earth history processes as sea-level and climate changes played an important role in the biogeographic patterns of the Amphisbaenia.     

Using regional comparative phylogeographic data from snake lineages to infer historical processes in Middle America

Understanding how historical processes have either similarly, or differentially, shaped the evolution of lineages or biotic assemblages is important for a broad spectrum of fields. Gaining such understanding can be particularly challenging, however, especially for regions that have a complex geologic and biological history. In this study we apply a broad comparative approach to distill such regional biogeographic perspectives, by characterizing sets of divergence times for major biogeographic boundaries estimated from multiple codistributed lineages of snakes. We use a large combined (mitochondrial gene sequence) phylogeographic/phylogenetic dataset containing several clades of snakes that range across Middle America – the tropical region between Mexico and northwestern South America. This region is known for its complex tectonic history, and poorly understood historical biogeography. Based on our results, we highlight how phylogeographic transition zones between Middle and South America and the Nicaragua Depression appear to have undergone multiple episodes of diversification in different lineages. This is in contrast to other examples we find where apparently a single vicariant period is shared across multiple lineages. We specifically evaluate the distributions of divergence time estimates across multiple lineages and estimate the number of temporal periods of lineage diversification per biogeographic break. Overall, our results highlight a great deal of shared temporal divergence, and provide important hypotheses for yet unstudied lineages. These multi‐lineage comparisons across multiple spatial and temporal scales provide excellent predictive power for identifying the roles of geology, climate, ecology and natural history in shaping regional biodiversity.     

Southern hemisphere biogeography inferred by event-based models: plant versus animal patterns

The Southern Hemisphere has traditionally been considered as having a fundamentally vicariant history. The common trans-Pacific disjunctions are usually explained by the sequential breakup of the supercontinent Gondwana during the last 165 million years, causing successive division of an ancestral biota. However, recent biogeographic studies, based on molecular estimates and more accurate paleogeographic reconstructions, indicate that dispersal may have been more important than traditionally assumed. We examined the relative roles played by vicariance and dispersal in shaping Southern Hemisphere biotas by analyzing a large data set of 54 animal and 19 plant phylogenies, including marsupials, ratites, and southern beeches (1,393 terminals). Parsimony-based tree fitting in conjunction with permutation tests was used to examine to what extent Southern Hemisphere biogeographic patterns fit the breakup sequence of Gondwana and to identify concordant dispersal patterns. Consistent with other studies, the animal data are congruent with the geological sequence of Gondwana breakup: (Africa(New Zealand(southern South America, Australia))). Trans-Antarctic dispersal (Australia <--> southern South America) is also significantly more frequent than any other dispersal event in animals, which may be explained by the long period of geological contact between Australia and South America via Antarctica. In contrast, the dominant pattern in plants, (southern South America(Australia, New Zealand)), is better explained by dispersal, particularly the prevalence of trans-Tasman dispersal between New Zealand and Australia. Our results also confirm the hybrid origin of the South American biota: there has been surprisingly little biotic exchange between the northern tropical and the southern temperate regions of South America, especially for animals.     

Return to Beringia: parasites reveal cryptic biogeographic history of North American pikas

Traditional concepts of the Bering Land Bridge as a zone of predominantly eastward expansion from Eurasia and a staging area for subsequent colonization of lower latitudes in North America led to early inferences regarding biogeographic histories of North American faunas, many of which remain untested. Here we apply a host-parasite comparative phylogeographical (HPCP) approach to evaluate one such history, by testing competing biogeographic hypotheses for five lineages of host-specific parasites shared by the collared pika (Ochotona collaris) and American pika (Ochotona princeps) of North America. We determine whether the southern host species (O. princeps) was descended from a northern ancestor or vice versa. Three parasite phylogenies revealed patterns consistent with the hypothesis of a southern origin, which is corroborated by four additional parasite lineages restricted to O. princeps. This finding reverses the traditional narrative for the origins of North American pikas and highlights the role of dispersal from temperate North America into Beringia in structuring northern diversity considerably prior to the Holocene. By evaluating multiple parasite lineages simultaneously, the study demonstrates the power of HPCP for resolving complex biogeographic histories that are not revealed by characteristics of the host alone.     

A view of early vertebrate evolution inferred from the phylogeny of polystome parasites (Monogenea: Polystomatidae)

The Polystomatidae is the only family within the Monogenea to parasitize sarcopterygians such as the Australian lungfish Neoceratodus poisteri and freshwater tetrapods (lissamphibians and chelonians). We present a phylogeny based on partial 18S rDNA sequences of 26 species of Polystomatidae and three taxon from the infrasubclass Oligonchoinea (= Polyopisthocotylea) obtained from the gills of teleost fishes. The basal position of the polystome from lungfish within the Polystomatidae suggests that the family arose during the evolutionary transition between actinopterygians and sarcopterygians, ca. 425 million years (Myr) ago. The monophyly of the polystomatid lineages from chelonian and lissamphibian hosts, in addition to estimates of the divergence times, indicate that polystomatids from turtles radiated ca. 191 Myr ago, following a switch from an aquatic amniote presumed to be extinct to turtles, which diversified in the Upper Triassic. Within polystomatids from lissamphibians, we observe a polytomy of four lineages, namely caudatan, neobatrachian, pelobatid and pipid polystomatid lineages, which occurred ca. 246 Myr ago according to molecular divergence-time estimates. This suggests that the first polystomatids of amphibians originated during the evolution and diversification of lissamphibian orders and suborders ca. 250 Myr ago. Finally, we report a vicariance event between two major groups of neobatrachian polystomes, which is probably linked to the separation of South America from Africa ca. 100 Myr ago.     

Biogeography and diversification of colletid bees (Hymenoptera: Colletidae): emerging patterns from the southern end of the world

Aim The evolutionary history of bees is presumed to extend back in time to the Early Cretaceous. Among all major clades of bees, Colletidae has been a prime example of an ancient group whose Gondwanan origin probably precedes the complete break‐up of Africa, Antarctica, Australia and South America, because modern lineages of this family occur primarily in southern continents. In this paper, we aim to study the temporal and spatial diversification of colletid bees to better understand the processes that have resulted in the present southern disjunctions. Location Southern continents. Methods We assembled a dataset comprising four nuclear genes of a broad sample of Colletidae. We used Bayesian inference analyses to estimate the phylogenetic tree topology and divergence times. Biogeographical relationships were investigated using event‐based analytical methods: a Bayesian approach to dispersal–vicariance analysis, a likelihood‐based dispersal–extinction–cladogenesis model and a Bayesian model. We also used lineage through time analyses to explore the tempo of radiations of Colletidae and their context in the biogeographical history of these bees. Results Initial diversification of Colletidae took place at the Late Cretaceous (≥ 70 Ma). Several (6–14) lineage exchanges between Australia and South America via Antarctica during the Late Cretaceous and Eocene epochs could explain the disjunctions observed between colletid lineages today. All biogeographical methods consistently indicated that there were multiple lineage exchanges between South America and Australia, and these approaches were valuable in exploring the degree of uncertainty inherent in the ancestral reconstructions. Biogeographical and dating results preclude an explanation of Scrapterinae in Africa as a result of vicariance, so one dispersal event is assumed to explain the disjunction in relation to Euryglossinae. The net diversification rate was found to be highest in the recent history of colletid evolution. Main conclusions The biogeography and macroevolutionary history of colletid bees can be explained by a combination of Cenozoic vicariance and palaeoclimatic changes during the Neogene. The austral connection and posterior break‐up of South America, Antarctica and Australia resulted in a pattern of disjunct sister lineages. Increased biome aridification coupled with floristic diversification in the southern continents during the Neogene may have contributed to the high rates of cladogenesis in these bees in the last 25–30 million years.     

Multilocus data of a manakin species reveal cryptic diversification moulded by vicariance

We used molecular tools and a multilocus approach to investigate the phylogeography of Lepidothrix coronata across most of its ample range. We sequenced six DNA fragments to produce phylogenies, molecular dating estimates, analyses of the dynamics of the demographic history of the species and a biogeographic analysis to estimate the events and changes in the ancestral distribution of the species. The results indicated the presence of four well-established lineages, with high levels of divergence. These lineages are delineated by well-defined geographic barriers, with one lineage, restricted to the west of the Andes, being the first to diverge from the complex. The other three lineages are exclusive to the Amazonian distribution of the species, with two being found north of the Amazon River, and the third, south of the Amazon. Some of the relationships found between these lineages were distinct from those described in previous studies. Important disagreements were found between the mtDNA phylogeny and that of the multilocus analysis, in relation to the lineages located to the west of the Andes. We propose that past introgression events may have influenced shifts in the relationships between lineages, despite the fact that the groups were well defined in both the phylogenies. The biogeographic analysis indicates that the lineages arose through successive vicariance events, which had a primary role in the diversification of the group. Two or three genetically structured subclades were also found within each Amazonian lineage, although these subclades are not isolated by an obvious geographic barrier.     

Local parasite lineage sharing in temperate grassland birds provides clues about potential origins of Galapagos avian Plasmodium

Oceanic archipelagos are vulnerable to natural introduction of parasites via migratory birds. Our aim was to characterize the geographic origins of two Plasmodium parasite lineages detected in the Galapagos Islands and in North American breeding bobolinks (Dolichonyx oryzivorus) that regularly stop in Galapagos during migration to their South American overwintering sites. We used samples from a grassland breeding bird assemblage in Nebraska, United States, and parasite DNA sequences from the Galapagos Islands, Ecuador, to compare to global data in a DNA sequence registry. Homologous DNA sequences from parasites detected in bobolinks and more sedentary birds (e.g., brown‐headed cowbirds Molothrus ater, and other co‐occurring bird species resident on the North American breeding grounds) were compared to those recovered in previous studies from global sites. One parasite lineage that matched between Galapagos birds and the migratory bobolink, Plasmodium lineage B, was the most common lineage detected in the global MalAvi database, matching 49 sequences from unique host/site combinations, 41 of which were of South American origin. We did not detect lineage B in brown‐headed cowbirds. The other Galapagos‐bobolink match, Plasmodium lineage C, was identical to two other sequences from birds sampled in California. We detected a close variant of lineage C in brown‐headed cowbirds. Taken together, this pattern suggests that bobolinks became infected with lineage B on the South American end of their migratory range, and with lineage C on the North American breeding grounds. Overall, we detected more parasite lineages in bobolinks than in cowbirds. Galapagos Plasmodium had similar host breadth compared to the non‐Galapagos haemosporidian lineages detected in bobolinks, brown‐headed cowbirds, and other grassland species. This study highlights the utility of global haemosporidian data in the context of migratory bird–parasite connectivity. It is possible that migratory bobolinks bring parasites to the Galapagos and that these parasites originate from different biogeographic regions representing both their breeding and overwintering sites.     

Polystomatidae (Monogenea) of southern African Anura: Polystoma claudecombesi n. sp. parasitic in Rana angolensis Bocage

Polystoma claudecombesi is described as a new species of the Polystomatidae (Monogenea) parasitic in the urinary bladder of the anuran host Rana angolensis. This parasite was collected at three localities in South Africa, namely Vernon Crookes Nature Reserve in Natal province, Witsieshoek Mountain Resort in the north-eastern Orange Free State and Bovenste Oog in the province of Transvaal. It is the largest African polystome described to date. Prevalence at Vernon Crookes Nature Reserve was 4.0% and 2.7% in two successive years, with a mean intensity of 1.0 (n=25 and 36, respectively). One of the two R. angolensis from Witsieshoek was infected with 5 parasites. The diversity and distribution of southern African polystomes is also discussed.     

Coevolution: a history of the macroevolutionary approach to studying host-parasite associations.

The year 1991 marked 100 yr of coevolution research. I have reviewed the first 90 yr of this history. Three chronological phases are apparent: recognition of predictable associations among hosts and their parasites; search for patterns of association and their underlying causes, emphasizing either correlated biogeographic patterns or correlated phylogenies; and development of objective and repeatable methodologies for reconstructing and interpreting these patterns of association. Von Ihering, an outspoken anti-Darwinian, was undoubtedly the first to recognize and make use of predictable host-parasite associations. Kellogg and Fahrenholz, however, had more profound influence on subsequent generations, but in different directions. Kellogg attempted to meld natural selection with speciation by isolation. He also considered host specificity a component of coevolution, important but variable. His work laid the foundation for future research concentrated on biogeographic interpretations of host-parasite relationships. This emphasis and Metcalf's failed attempts to provide adequate mechanisms for reconstructing phylogenies reduced the biogeographic approach to an empirical research program in the hands of Manter. Fahrenholz, on the other hand, exposed to a strong anti-Darwinian sentiment, emphasized the importance of strict host specificity. This led to Eichler's formulation of the first 3 coevolutionary rules and the conclusion that host specificity was not a component but the cause of coevolution and ultimately the tautology inherent in the phylogenetic approach. All had to rely on 1 assumption, that host and parasite phylogenies were reflected in the taxonomic hierarchy. Hennig criticized this assumption and provided a method whereby phylogenies are reconstructed independently. Brooks melded this new phylogenetic method (cladistics) with an equally new biogeographic method (vicariance biogeography), providing the foundations for the modern macroevolutionary approach to studying host-parasite associations.     

Host species,and not environment,predicts variation in blood parasite prevalence,distribution, and diversity along a humidity gradient in northern South America

Environmental factors strongly influence the ecology and evolution of vector‐borne infectious diseases. However, our understanding of the influence of climatic variation on host–parasite interactions in tropical systems is rudimentary. We studied five species of birds and their haemosporidian parasites (Plasmodium and Haemoproteus) at 16 sampling sites to understand how environmental heterogeneity influences patterns of parasite prevalence, distribution, and diversity across a marked gradient in water availability in northern South America. We used molecular methods to screen for parasite infections and to identify parasite lineages. To characterize spatial heterogeneity in water availability, we used weather‐station and remotely sensed climate data. We estimated parasite prevalence while accounting for spatial autocorrelation, and used a model selection approach to determine the effect of variables related to water availability and host species on prevalence. The prevalence, distribution, and lineage diversity of haemosporidian parasites varied among localities and host species, but we found no support for the hypothesis that the prevalence and diversity of parasites increase with increasing water availability. Host species and host × climate interactions had stronger effects on infection prevalence, and parasite lineages were strongly associated with particular host species. Because climatic variables had little effect on the overall prevalence and lineage diversity of haemosporidian parasites across study sites, our results suggest that independent host–parasite dynamics may influence patterns in parasitism in environmentally heterogeneous landscapes.     

Parasite diversity declines with host evolutionary distinctiveness: A global analysis of carnivores

Evolutionarily distinctive host lineages might harbor fewer parasite species because they have fewer opportunities for parasite sharing than hosts having extant close relatives, or because diverse parasite assemblages promote host diversification. We evaluate these hypotheses using data from 930 species of parasites reported to infect free‐living carnivores. We applied nonparametric richness estimators to estimate parasite diversity among well‐sampled carnivore species and assessed how well host evolutionary distinctiveness, relative to other biological and environmental factors, explained variation in estimated parasite diversity. Species richness estimates indicate that the current published literature captures less than 50% of the true parasite diversity for most carnivores. Parasite species richness declined with evolutionary distinctiveness of carnivore hosts (i.e., length of terminal ranches of the phylogeny) and increased with host species body mass and geographic range area. We found no support for the hypothesis that hosts from more diverse lineages support a higher number of generalist parasites, but we did find evidence that parasite assemblages might have driven host lineage diversification through mechanisms linked to sexual selection. Collectively, this work provides strong support for host evolutionary history being an essential predictor of parasite diversity, and offers a simple model for predicting parasite diversity in understudied carnivore species.     

Biogeography of avian blood parasites (Leucocytozoon spp.) in two resident hosts across Europe: phylogeographic structuring or the abundance–occupancy relationship?

Relationships between hosts and parasites represent complex co-evolving systems that can vary both temporally and spatially. This variation may result in different phylogeographic outcomes, ranging from highly geographically structured parasite populations comprised of specialist lineages that are locally abundant but have restricted global occupancy to geographically unstructured parasite populations consisting of widespread parasites. Here, we present results from a large biogeographic study of the Leucocytozoon blood parasites of two nonmigrant bird species, conducted at nine sites across Europe. The aim was to determine whether the parasite lineages of the two hosts were phylogeographically structured across Europe. Employing molecular methods, we found a large diversity of parasites, and although overall prevalence varied greatly, the parasites were not genetically structured. Several measures of local parasite abundance were associated with the number of sites that the lineage occurred in, which is consistent with the macroecological phenomenon of the abundance-occupancy relationship. Taken together, our results show that parasite dispersal is somewhat uncoupled to that of the host in this system: we suggest that broad host and/or vector preference may play an important role in determining the distribution of these parasites and in affecting host-parasite coevolution in this system.     

Biogeography explains cophylogenetic patterns in toucan chewing lice

Historically, comparisons of host and parasite phylogenies have concentrated on cospeciation. However, many of these comparisons have demonstrated that the phylogenies of hosts and parasites are seldom completely congruent, suggesting that phenomena other than cospeciation play an important role in the evolution of host-parasite assemblages. Other coevolutionary phenomena, such as host switching, parasite duplication (speciation on the host), sorting (extinction), and failure to speciate can also influence host-parasite assemblages. Using mitochondrial and nuclear protein-coding DNA sequences, I reconstructed the phylogeny of ectoparasitic toucan chewing lice in the Austrophilopterus cancellosus subspecies complex and compared this phylogeny with the phylogeny of the hosts, the Ramphastos toucans, to reconstruct the history of coevolutionary events in this host-parasite assemblage. Three salient findings emerged. First, reconstructions of host and louse phylogenies indicate that they do not branch in parallel, and their cophylogenetic history shows little or no significant cospeciation. Second, members of monophyletic Austrophilopterus toucan louse lineages are not necessarily restricted to monophyletic host lineages. Often, closely related lice are found on more distantly related but sympatric toucan hosts. Third, the geographic distribution of the hosts apparently plays a role in the speciation of these lice. These results suggest that for some louse lineages biogeography may be more important than host associations in structuring louse populations and species, particularly when host life history (e.g., hole nesting) or parasite life history (e.g., phoresis) might promote frequent host switching events between syntopic host species. These findings highlight the importance of integrating biogeographic information into cophylogenetic studies.     

Geography and host biogeography matter for understanding the phylogeography of a parasite

The co-evolution between hosts and parasites has long been recognized as a fundamental driver of macro-evolutionary patterns of diversification. The effect of co-differentiation on parasite diversification is, however, often confounded by underlying geographic patterns of host distribution. In order to disentangle the confounding effects of allopatric versus host speciation, the mitochondrial cytochrome b (cyt b) gene was sequenced in seventy individuals of the parasitic nematode genus Heligmosomoides sampled in the six Apodemus mice species common in the western Palearctic region. The nuclear internal transcribed spacers (ITS) 1 and 2 were also sequenced in fifteen parasites to confirm the mitochondrial data. All lineages differentiated according to a geographic pattern and independently from the sampled host species. This suggests that host speciation did not involve concurrent parasite speciation. However, the geographic distribution range of some parasite lineages mirrors that of A. sylvaticus lineages in SW Europe, and that of A. flavicollis lineages in the Balkans and in the Middle East. Thus, regional co-differentiation likely occurred between the parasite and the two sister Apodemus hosts in different parts of their distribution range. We suggest that differences in regional abundances of A. sylvaticus and A. flavicollis are responsible for generating this pattern of regional co-differentiation. This study highlights the importance of integrating both geography and biogeographic information from potential hosts to better understand their parasite phylogeography.     

Diversification by host switching and dispersal shaped the diversity and distribution of avian malaria parasites in Amazonia

Understanding how pathogens and parasites diversify through time and space is fundamental to predicting emerging infectious diseases. Here, we use biogeographic, coevolutionary and phylogenetic analyses to describe the origin, diversity, and distribution of avian malaria parasites in the most diverse avifauna on Earth. We first performed phylogenetic analyses using the mitochondrial cytochrome b (cyt b) gene to determine relationships among parasite lineages. Then, we estimated divergence times and reconstructed ancestral areas to uncover how landscape evolution has shaped the diversification of Parahaemoproteus and Plasmodium in Amazonia. Finally, we assessed the coevolutionary patterns of diversification in this host–parasite system to determine how coevolution may have influenced the contemporary diversity of avian malaria parasites and their distribution among Amazonian birds. Biogeographic analysis of 324 haemosporidian parasite lineages recovered from 4178 individual birds provided strong evidence that these parasites readily disperse across major Amazonian rivers and this has occurred with increasing frequency over the last five million years. We also recovered many duplication events within areas of endemism in Amazonia. Cophylogenetic analyses of these blood parasites and their avian hosts support a diversification history dominated by host switching. The ability of avian malaria parasites to disperse geographically and shift among avian hosts has played a major role in their radiation and has shaped the current distribution and diversity of these parasites across Amazonia.