Coevolution between hosts and parasites with partially overlapping geographic ranges

Many host species interact with a specific parasite within only a fraction of their geographical range. Where host and parasite overlap geographically, selection may be reciprocal constituting a coevolutionary hot spot. Host evolution, however, may be driven primarily by selection imposed by alternative biotic or abiotic factors that occur outside such hot spots. To evaluate the importance of coevolutionary hot spots for host and parasite evolution, we analyse a spatially explicit genetic model for a host that overlaps with a parasite in only part of its geographical range. Our results show that there is a critical amount of overlap beyond which reciprocal selection leads to a coevolutionary response in the host. This critical amount of overlap depends upon the explicit spatial configuration of hot spots. When the amount of overlap exceeds this first critical level, host-parasite coevolution commonly generates stable allele frequency clines rather than oscillations. It is within this region that one of the primary predictions of the geographic mosaic theory is realized, and local maladaptation is prevalent in both species. Past a further threshold of overlap between the species oscillations do evolve, but allele frequencies in both species are spatially synchronous and local maladaptation is absent in both species. A consequence of such transitions between coevolutionary dynamics is that parasite adaptation is inversely proportional to the fraction of its host's range that it occupies. Hence, as the geographical range of a parasite increases, it becomes increasingly maladapted to the host. This suggests a novel mechanism through which the geographical range of parasites may be limited.     

Experimental evolution of local parasite maladaptation

Sign and magnitude of local adaptation in host–parasite systems may vary with ecological, epidemiological or genetic parameters. To investigate the role of host genetic background, we established long‐term experimental populations of different genotypes of the protozoan Paramecium caudatum, infected with the bacterial parasite Holospora undulata. We observed the evolution of an overall pattern of parasite local maladaptation for infectivity, indicating a general coevolutionary disadvantage of this parasite. Maladaptation extended to host populations with the same genetic background, similar to extending from the local to a higher regional level in natural populations. Patterns for virulence were qualitatively similar, but with less statistical support. A nonsignificant correlation with levels of (mal)adaptation for infectivity suggests independent evolution of these traits. Our results indicate similar (co)evolutionary trajectories in populations with different genetic backgrounds. Nonetheless, the correlated clines of genetic distance and parasite performance illustrate how genetic background can shape spatial gradients of local adaptation.     

Development and characterization of microsatellite markers for the poplar rust fungi Melampsora medusae and Melampsora larici‐populina

Melampsora species and their hybrids are obligate parasites of Populus and Salix species worldwide. The increasing interest in Populus and Salix for biomass and fibre production necessitates genetic markers for population studies of Melampsora spp. Libraries enriched for simple sequence repeats were used to develop five microsatellite markers for Melampsora medusae and Melampsora larici‐populina. The variation detected by these markers will be valuable for phylogenetic and population genetic studies, substantiate putative hybrids, and deployment of resistant poplar clones.     

Spatial heterogeneity of daphniid parasitism within lakes

Spatially explicit models show that local interactions of hosts and parasites can strongly influence invasion and persistence of parasites and can create lasting spatial patchiness of parasite distributions. These predictions have been supported by experiments conducted in two-dimensional landscapes. Yet, three-dimensional systems, such as lakes, ponds, and oceans, have received comparatively little attention from epidemiologists. Freshwater zooplankton hosts often aggregate horizontally and vertically in lakes, potentially leading to local host–parasite interactions in one-, two-, or three-dimensions. To evaluate the potential spatial component of daphniid parasitism driven by these local interactions (patchiness), we surveyed vertical and horizontal heterogeneity of pelagic Daphnia infected with multiple microparasites in several north temperate lakes. These surveys uncovered little evidence for persistent vertical patchiness of parasitism, since the prevalence of two parasites showed little consistent trend with depth in four lakes (but more heterogeneity during day than at night). On a horizontal scale of tens of meters, we found little systematic evidence of strong aggregation and spatial patterning of daphniid hosts and parasites. Yet, we observed broad-scale, basin-wide patterns of parasite prevalence. These patterns suggest that nearshore offshore gradients, rather than local-scale interactions, could play a role in governing epidemiology of this open water host–parasite system. Electronic Supplementary Material Supplementary material is available for this article at     

ALTITUDINAL CLINAL VARIATION IN WING SIZE AND SHAPE IN AFRICAN DROSOPHILA MELANOGASTER: ONE CLINE OR MANY?

Geographical patterns of morphological variation have been useful in addressing hypotheses about environmental adaptation. In particular, latitudinal clines in phenotypes have been studied in a number of Drosophila species. Some environmental conditions along latitudinal clines—for example, temperature—also vary along altitudinal clines, but these have been studied infrequently and it remains unclear whether these environmental factors are similar enough for convergence or parallel evolution. Most clinal studies in Drosophila have dealt exclusively with univariate phenotypes, allowing for the detection of clinal relationships, but not for estimating the directions of covariation between them. We measured variation in wing shape and size in D. melanogaster derived from populations at varying altitudes and latitudes across sub‐Saharan Africa. Geometric morphometrics allows us to compare shape changes associated with latitude and altitude, and manipulating rearing temperature allows us to quantify the extent to which thermal plasticity recapitulates clinal effects. Comparing effect vectors demonstrates that altitude, latitude, and temperature are only partly associated, and that the altitudinal shape effect may differ between Eastern and Western Africa. Our results suggest that selection responsible for these phenotypic clines may be more complex than just thermal adaptation.     

Genomics of clinal variation in Drosophila: disentangling the interactions of selection and demography

Clines in phenotypes and genotype frequencies across environmental gradients are commonly taken as evidence for spatially varying selection. Classical examples include the latitudinal clines in various species of Drosophila, which often occur in parallel fashion on multiple continents. Today, genomewide analysis of such clinal systems provides a fantastic opportunity for unravelling the genetics of adaptation, yet major challenges remain. A well‐known but often neglected problem is that demographic processes can also generate clinality, independent of or coincident with selection. A closely related issue is how to identify true genic targets of clinal selection. In this issue of Molecular Ecology, three studies illustrate these challenges and how they might be met. Bergland et al. report evidence suggesting that the well‐known parallel latitudinal clines in North American and Australian D. melanogaster are confounded by admixture from Africa and Europe, highlighting the importance of distinguishing demographic from adaptive clines. In a companion study, Machado et al. provide the first genomic comparison of latitudinal differentiation in D. melanogaster and its sister species D. simulans. While D. simulans is less clinal than D. melanogaster, a significant fraction of clinal genes is shared between both species, suggesting the existence of convergent adaptation to clinaly varying selection pressures. Finally, by drawing on several independent sources of evidence, Bo?i?evi? et al. identify a functional network of eight clinal genes that are likely involved in cold adaptation. Together, these studies remind us that clinality does not necessarily imply selection and that separating adaptive signal from demographic noise requires great effort and care.     

Molecular and morphological analysis of secondary contact zones of Cottus gobio in Fennoscandia: geographical discordance of character transitions

Northern Europe was postglacially colonized from different directions by distinct phylogeographical lineages of the bullhead Cottus gobio L. (Pisces: Scorpaeniformes). These lineages have then come into contact in coastal habitats of the currently brackish Baltic Sea and in the freshwaters north of it. We studied the patterns of intergradation in the contact zones in four morphometric and six molecular characters. In the north, intergradation between the western (W) and eastern (E) bullhead lineages is found both among rivers (west‐to‐east) and along individual rivers (south‐to‐north). The locations of the transition zones probably relate to the timing of the initial contact, subsequent Baltic shoreline displacement (i.e. emergence of the lower river reaches), and dispersal barriers caused by variations of coastal salinity. The transitions (clines) in different characters are, however, not geographically coincident. Mitochondrial DNA clines are generally found upstream and to the east of the other transitions, and GPI‐1 allozyme clines are mostly shifted downstream in the rivers, and west of the other transitions on the broader scale of the Baltic Sea. The location of the mtDNA clines may best reflect the initial contact between lineages, and the displacement of the other clines could result from dispersal being overall asymmetric (predominantly downstream) and sex‐biased (stronger in males). Alternatively, the non‐coincidence might reflect selection against deleterious cytonuclear character combinations. No clear evidence of reproductive incompatibility between the lineages was seen in local population structures; no remaining genetic correlations were observed locally among traits. In another transition area, a coastal transect in southern Finland, clinal patterns similar to those in the northern contact zone were recorded, but the population compositions could not be explained by simple in situ mixing of any of the putatively pure, invading refugial lineages. Probably, the bullhead stocks that initially came into contact in this southern study area already represented mixtures of the invading lineages. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 81 , 535–552.     

Evolutionary genetics of Metridium senile. II. Geographic patterns of allozyme variation

Electrophoretic surveys have demonstrated that populations of the sea anemone Metridium senile along the northeast coast of the United States are polymorphic at four enzyme loci. Phosphoglucose isomerase (PGI) has two alleles in most populations, phosphoglucomutase (PGM) has three alleles, and two leucine aminopeptidase loci have two common alleles each. Phosphoglucose isomerase displays clinal variation and an apparent association with environmental temperature. Phosphoglucomutase shows clinal variation north of Cape Cod for two of the three alleles, while the two leucine aminopeptidase loci are not clinal. All loci show a great deal of variation in populations on Cape Cod, but there is no apparent systematic pattern to this variation. Temperature may be a selective agent in the maintenance of the PGI and PGM clines, although other possibilities cannot presently be completely excluded.Supported by Grant T-4 from the Health Research and Services Foundation, NSF DEB77-14442, NIH GM25809, and NIH GM28024.     

Complex patterns of local adaptation in heat tolerance in Drosophila simulans from eastern Australia

Latitudinal clines are considered a powerful means of investigating evolutionary responses to climatic selection in nature. However, most clinal studies of climatic adaptation in Drosophila have involved species that contain cosmopolitan inversion polymorphisms that show clinal patterns themselves, making it difficult to determine whether the traits or inversions are under selection. Further, although climatic selection is unlikely to act on only one life stage in metamorphic organisms, a few studies have examined clinal patterns across life stages. Finally, clinal patterns of heat tolerance may also depend on the assay used. To unravel these potentially confounding effects on clinal patterns of thermal tolerance, we examined adult and larval heat tolerance traits in populations of Drosophila simulans from eastern Australia using static and dynamic (ramping 0.06 °C min^?1) assays. We also used microsatellites markers to clarify whether demographic factors or selection are responsible for population differentiation along clines. Significant cubic clinal patterns were observed for adult static basal, hardened and dynamic heat knockdown time and static basal heat survival in larvae. In contrast, static, hardened larval heat survival increased linearly with latitude whereas no clinal association was found for larval ramping survival. Significant associations between adult and larval traits and climatic variables, and low population differentiation at microsatellite loci, suggest a role for climatic selection, rather than demographic processes, in generating these clinal patterns. Our results suggest that adaptation to thermal stress may be species and life‐stage specific, complicating our efforts to understand the evolutionary responses to selection for increasing thermotolerance.     

Parallel effects of the inversion In(3R)Payne on body size across the North American and Australian clines in Drosophila melanogaster

Chromosomal inversions are thought to play a major role in climatic adaptation. In D. melanogaster, the cosmopolitan inversion In(3R)Payne exhibits latitudinal clines on multiple continents. As many fitness traits show similar clines, it is tempting to hypothesize that In(3R)P underlies observed clinal patterns for some of these traits. In support of this idea, previous work in Australian populations has demonstrated that In(3R)P affects body size but not development time or cold resistance. However, similar data from other clines of this inversion are largely lacking; finding parallel effects of In(3R)P across multiple clines would considerably strengthen the case for clinal selection. Here, we have analysed the phenotypic effects of In(3R)P in populations originating from the endpoints of the latitudinal cline along the North American east coast. We measured development time, egg‐to‐adult survival, several size‐related traits (femur and tibia length, wing area and shape), chill coma recovery, oxidative stress resistance and triglyceride content in homokaryon lines carrying In(3R)P or the standard arrangement. Our central finding is that the effects of In(3R)P along the North American cline match those observed in Australia: standard arrangement lines were larger than inverted lines, but the inversion did not influence development time or cold resistance. Similarly, In(3R)P did not affect egg‐to‐adult survival, oxidative stress resistance and lipid content. In(3R)P thus seems to specifically affect size traits in populations from both continents. This parallelism strongly suggests an adaptive pattern, whereby the inversion has captured alleles associated with growth regulation and clinal selection acts on size across both continents.     

Parasite local adaptation in a geographic mosaic

A central prediction of the geographic mosaic theory of coevolution is that coevolving interspecific interactions will show varying degrees of local maladaptation. According to the theory, much of this local maladaptation is driven by selection mosaics and spatially intermingled coevolutionary hot and cold spots, rather than a simple balance between gene flow and selection. Here I develop a genetic model of host-parasite coevolution that is sufficiently general to incorporate selection mosaics, coevolutionary hot and cold spots, and a diverse array of genetic systems of infection/resistance. Results from this model show that the selection mosaics experienced by the interacting species are an important determinant of the sign and magnitude of local maladaptation. In some cases, this effect may be stronger than a previously described effect of relative rates of parasite and host gene flow. These results provide the first theoretical evidence that selection mosaics and coevolutionary hot and cold spots per se determine the magnitude and sign of local maladaptation. At the same time, however, these results demonstrate that coevolution in a geographic mosaic can lead to virtually any pattern of local adaptation or local maladaptation. Consequently, empirical studies that describe only patterns of local adaptation or maladaptation do not provide evidence either for or against the theory.     

HOST-PARASITE COEVOLUTION: EVIDENCE FOR RARE ADVANTAGE AND TIME-LAGGED SELECTION IN A NATURAL POPULATION

In theory, parasites can create time-lagged, frequency-dependent selection in their hosts, resulting in oscillatory gene-frequency dynamics in both the host and the parasite (the Red Queen hypothesis). However, oscillatory dynamics have not been observed in natural populations. In the present study, we evaluated the dynamics of asexual clones of a New Zealand snail, Potamopyrgus antipodarum, and its trematode parasites over a five-year period. During the summer of each year, we determined host-clone frequencies in random samples of the snail to track genetic changes in the snail population. Similarly, we monitored changes in the parasite population, focusing on the dominant parasite, Microphallus sp., by calculating the frequency of clones in samples of infected individuals from the same collections. We then compared these results to the results of a computer model that was designed to examine clone frequency dynamics for various levels of parasite virulence. Consistent with these simulations and with ideas regarding dynamic coevolution, parasites responded to common clones in a time-lagged fashion. Finally, in a laboratory experiment, we found that clones that had been rare during the previous five years were significantly less infectible by Microphallus when compared to the common clones. Taken together, these results confirm that rare host genotypes are more likely to escape infection by parasites; they also show that host-parasite interactions produce, in a natural population, some of the dynamics anticipated by the Red Queen hypothesis.     

Tetracycline treatment targeting Wolbachia affects expression of an array of proteins in Brugia malayi parasite

Wolbachia is an intracellular endosymbiont of Brugia malayi parasite whose presence is essential for the survival of the parasite. Treatment of B. malayi‐infected jirds with tetracycline eliminates Wolbachia, which affects parasite survival and fitness. In the present study we have tried to identify parasite proteins that are affected when Wolbachia is targeted by tetracycline. For this Wolbachia depleted parasites (B. malayi) were obtained by tetracycline treatment of infected Mongolian jirds (Meriones unguiculatus) and their protein profile after 2‐DE separation was compared with that of untreated parasites harboring Wolbachia. Approximately 100 protein spots could be visualized followed by CBB staining of 2‐D gel and included for comparative analysis. Of these, 54 showed differential expressions, while two new protein spots emerged (of 90.3 and 64.4 kDa). These proteins were subjected to further analysis by MALDI‐TOF for their identification using Brugia coding sequence database composed of both genomic and EST sequences. Our study unravels two crucial findings: (i) the parasite or Wolbachia proteins, which disappeared/down‐regulated appear be essential for parasite survival and may be used as drug targets and (ii) tetracycline treatment interferes with the regulatory machinery vital for parasites cellular integrity and defense and thus could possibly be a molecular mechanism for the killing of filarial parasite. This is the first proteomic study substantiating the wolbachial genome integrity with its nematode host and providing functional genomic data of human lymphatic filarial parasite B. malayi.     

Clinal colour variation within a panmictic population of tree squirrels,Tamiasciurus douglasii (Rodentia: Sciuridae), across an ecological gradient

Local adaptation occurs when a population in a heterogeneous environment experiences divergent ecological selection but only if selection is stronger than the homogenizing effects of gene flow. The forest environments of Oregon vary along a physical and biotic gradient from a wet, closed‐canopy forest near the coast to a drier open‐canopy forest eastward across the Cascade Mountains. The present study explores patterns of local adaptation in Douglas squirrels (Tamiasciurus douglasii) in relation to these transitions in forest structure and ecology. We test for the presence of morphological clines in relation to gene flow and, more specifically, whether any such character clines correspond with environmental clines. We sampled animals at six locations (10 specimens each) and evaluated environmental parameters across a 240‐km west‐to‐east transect. Population structure analysis of 18 microsatellite loci indicates a single, panmictic squirrel population across the entire transect. Coalescent‐based estimates show bidirectional gene flow at similar west–east intensities between squirrels in coastal and interior forests. Of the four skull traits examined, none shows a significant clinal transition. By contrast, ventral fur colour shows a strong clinal transition, from deep‐orange in coastal forest to whitish–yellow in the interior forest. This pattern of phenotypic divergence coincides with the gradient in tree‐canopy cover. Ventral fur colour of T. douglasii exemplifies a gradation of continuous phenotypic variation maintained despite ongoing gene flow in a panmictic population. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 536–546.     

Microfungal “Weeds” in the Leafcutter Ant Symbiosis

Leafcutter ants (Formicidae: tribe Attini) are well-known insects that cultivate basidiomycete fungi (Agaricales: Lepiotaceae) as their principal food. Fungus gardens are monocultures of a single cultivar strain, but they also harbor a diverse assemblage of additional microbes with largely unknown roles in the symbiosis. Cultivar-attacking microfungi in the genus Escovopsis are specialized parasites found only in association with attine gardens. Evolutionary theory predicts that the low genetic diversity in monocultures should render ant gardens susceptible to a wide range of diseases, and additional parasites with roles similar to that of Escovopsis are expected to exist. We profiled the diversity of cultivable microfungi found in 37 nests from ten Acromyrmex species from Southern Brazil and compared this diversity to published surveys. Our study revealed a total of 85 microfungal strains. Fusarium oxysporum and Escovopsis were the predominant species in the surveyed gardens, infecting 40.5% and 27% of the nests, respectively. No specific relationship existed regarding microfungal species and ant-host species, ant substrate preference (dicot versus grass) or nesting habit. Molecular data indicated high genetic diversity among Escovopsis isolates. In contrast to the garden parasite, F. oxysporum strains are not specific parasites of the cultivated fungus because strains isolated from attine gardens have similar counterparts found in the environment. Overall, the survey indicates that saprophytic microfungi are prevalent in South American leafcutter ants. We discuss the antagonistic potential of these microorganisms as “weeds” in the ant–fungus symbiosis.     

Geographic clines in wing morphology relate to colonization history in New World but not Old World populations of yellow dung flies

Geographic clines offer insights about putative targets and agents of natural selection as well as tempo and mode of adaptation. However, demographic processes can lead to clines that are indistinguishable from adaptive divergence. Using the widespread yellow dung fly Scathophaga stercoraria (Diptera: Scathophagidae), we examine quantitative genetic differentiation (Q_ST) of wing shape across North America, Europe, and Japan, and compare this differentiation with that of ten microsatellites (F_ST). Morphometric analyses of 28 populations reared at three temperatures revealed significant thermal plasticity, sexual dimorphism, and geographic differentiation in wing shape. In North America morphological differentiation followed the decline in microsatellite variability along the presumed route of recent colonization from the southeast to the northwest. Across Europe, where S. stercoraria presumably existed for much longer time and where no molecular pattern of isolation by distance was evident, clinal variation was less pronounced despite significant morphological differentiation (Q_ST>F_ST). Shape vector comparisons further indicate that thermal plasticity (hot‐to‐cold) does not mirror patterns of latitudinal divergence (south‐to‐north), as might have been expected under a scenario with temperature as the major agent of selection. Our findings illustrate the importance of detailed phylogeographic information when interpreting geographic clines of dispersal traits in an adaptive evolutionary framework.     

Picturing local adaptation: Spectral and structural traits from drone remote sensing reveal clinal responses to climate transfer in common-garden trials of interior spruce (Picea engelmannii × glauca)

Common-garden trials of forest trees provide phenotype data used to assess growth and local adaptation; this information is foundational to tree breeding programs, genecology, and gene conservation. As jurisdictions consider assisted migration strategies to match populations to suitable climates, in situ progeny and provenance trials provide experimental evidence of adaptive responses to climate change. We used drone technology, multispectral imaging, and digital aerial photogrammetry to quantify spectral traits related to stress, photosynthesis, and carotenoids, and structural traits describing crown height, size, and complexity at six climatically disparate common-garden trials of interior spruce (Picea engelmannii × glauca) in western Canada. Through principal component analysis, we identified key components of climate related to temperature, moisture, and elevational gradients. Phenotypic clines in remotely sensed traits were analyzed as trait correlations with provenance climate transfer distances along principal components (PCs). We used traits showing clinal variation to model best linear unbiased predictions for tree height (R² = .98–.99, root mean square error [RMSE] = 0.06–0.10 m) and diameter at breast height (DBH, R² = .71–.97, RMSE = 2.57–3.80 mm) and generated multivariate climate transfer functions with the model predictions. Significant (p < .05) clines were present for spectral traits at all sites along all PCs. Spectral traits showed stronger clinal variation than structural traits along temperature and elevational gradients and along moisture gradients at wet, coastal sites, but not at dry, interior sites. Spectral traits may capture patterns of local adaptation to temperature and montane growing seasons which are distinct from moisture-limited patterns in stem growth. This work demonstrates that multispectral indices improve the assessment of local adaptation and that spectral and structural traits from drone remote sensing produce reliable proxies for ground-measured height and DBH. This phenotyping framework contributes to the analysis of common-garden trials towards a mechanistic understanding of local adaptation to climate.     

An inversion supergene in Drosophila underpins latitudinal clines in survival traits

Chromosomal inversions often contribute to local adaptation across latitudinal clines, but the underlying selective mechanisms remain poorly understood. We and others have previously shown that a clinal inversion polymorphism in Drosophila melanogaster, In(3R)Payne, underpins body size clines along the North American and Australian east coasts. Here, we ask whether this polymorphism also contributes to clinal variation in other fitness‐related traits, namely survival traits (lifespan, survival upon starvation and survival upon cold shock). We generated homokaryon lines, either carrying the inverted or standard chromosomal arrangement, isolated from populations approximating the endpoints of the North American cline (Florida, Maine) and phenotyped the flies at two growth temperatures (18 °C, 25 °C). Across both temperatures, high‐latitude flies from Maine lived longer and were more stress resistant than low‐latitude flies from Florida, as previously observed. Interestingly, we find that this latitudinal pattern is partly explained by the clinal distribution of the In(3R)P polymorphism, which is at ~ 50% frequency in Florida but absent in Maine: inverted karyotypes tended to be shorter‐lived and less stress resistant than uninverted karyotypes. We also detected an interaction between karyotype and temperature on survival traits. As In(3R)P influences body size and multiple survival traits, it can be viewed as a ‘supergene’, a cluster of tightly linked loci affecting multiple complex phenotypes. We conjecture that the inversion cline is maintained by fitness trade‐offs and balancing selection across geography; elucidating the mechanisms whereby this inversion affects alternative, locally adapted phenotypes across the cline is an important task for future work.     

Host range and local parasite adaptation

Parasites may be expected to become locally adapted to their hosts. However, while many empirical studies have demonstrated local parasite adaptation, others have failed to demonstrate it, or have shown local parasite maladaptation. Researchers have suggested that gene flow can swamp local parasite-host dynamics and produce local adaptation only at certain geographical scales; others have argued that evolutionary lags can account for both null and maladaptive results. In this paper, we use item response theory (IRT) to test whether host range influences the likelihood of parasites locally adapting to their hosts. We collated 32 independent experiments testing for local adaptation, where parasites could be assigned as having either broad or narrow host ranges (BHR and NHR, respectively). Twenty-five tests based on BHR parasites had a significantly lower average effect size than seven NHR tests, indicating that studies based on BHR parasites are less likely to demonstrate local parasite adaptation. We argue that this may relate to evolutionary lags during diffuse coevolution of BHR parasites with their hosts, rather than differences in experimental approaches or other confounds between BHR and NHR studies.     

Phylogeography of Caribbean lizard malaria: tracing the history of vector‐borne parasites

The Anolis lizards of the eastern Caribbean islands are parasitized by several species of malaria parasites (Plasmodium). Here I focus on two species of Plasmodium, using molecular data (mitochondrial cytochrome b sequences) to recover the phylogeography of the parasites throughout the Lesser Antilles and Puerto Rico. The two parasites were originally described as a single species, P. azurophilum, which infects both red and white blood cells. Here the two species are termed P. azurophilum Red and P. azurophilum White based on their host cell type. Six haplotypes were found in 100 infections sequenced of P. azurophilum Red and six in 45 infections of P. azurophilum White. Nested clade analysis revealed a significant association of geographical location and clades as well as a pattern of past fragmentation of parasite populations. This is consistent with the hypothesis that vector‐borne parasites such as malaria may be subject to frequent local extinctions and recolonizations. Comparison of the phylogeography of the lizard and parasites shows only weak concordance; that is, the parasites colonized the lizards in the islands, but dispersal events between islands via vectors or failed lizard colonizations were present. The two parasites had different histories, P. azurophilum Red colonized the islands from both the north and south, and P. azurophilum White originated in the central Lesser Antilles, probably from P. azurophilum Red, then moved to both north and south. This is the first study to examine the biogeography of a pair of sibling species of vector‐borne parasites within an island archipelago system.