Parasite Speciation Research Articles

Active defence mechanisms in brood parasitism hosts and their consequences for parasite adaptation and speciation

Active defence mechanisms in brood parasitism hosts and their consequences for parasite adaptation and speciation

Testing the radiation cascade in postglacial radiations of whitefish and their parasites: founder events and host ecology drive parasite evolution.

Reciprocal effects of adaptive radiations on the evolution of interspecific interactions, like parasitism, remain barely explored. We test whether the recent radiations of European whitefish (Coregonus spp.) across and within perialpine and subarctic lakes promote its parasite Proteocephalus fallax (Platyhelminthes: Cestoda) to undergo host repertoire expansion via opportunity and ecological fitting, or adaptive radiation by specialization. Using de novo genomic data, we examined P. fallax differentiation across lakes, within lakes across sympatric host species, and the contributions of host genetics versus host habitat use and trophic preferences. Whitefish intralake radiations prompted parasite host repertoire expansion in all lakes, whereas P. fallax differentiation remains incipient among sympatric fish hosts. Whitefish genetic differentiation per se did not explain the genetic differentiation among its parasite populations, ruling out codivergence with the host. Instead, incipient parasite differentiation was driven by whitefish phenotypic radiation in trophic preferences and habitat use in an arena of parasite opportunity and ecological fitting to utilize resources from emerging hosts. Whilst the whitefish radiation provides a substrate for the parasite to differentiate along the same water-depth ecological axis as Coregonus spp., the role of the intermediate hosts in parasite speciation may be overlooked. Parasite multiple-level ecological fitting to both fish and crustacean intermediate hosts resources may be responsible for parasite population substructure in Coregonus spp. We propose parasites' delayed arrival was key to the initial burst of postglacial intralake whitefish diversification, followed by opportunistic tapeworm host repertoire expansion and a delayed nonadaptive radiation cascade of incipient tapeworm differentiation. At the geographical scale, dispersal, founder events, and genetic drift following colonization of spatially heterogeneous landscapes drove strong parasite differentiation. We argue that these microevolutionary processes result in the mirroring of host-parasite phylogenies through phylogenetic tracking at macroevolutionary and geographical scales.

Ancestral aneuploidy and stable chromosomal duplication resulting in differential genome structure and gene expression control in trypanosomatid parasites.

Aneuploidy is widely observed in both unicellular and multicellular eukaryotes, usually associated with adaptation to stress conditions. Chromosomal duplication stability is a tradeoff between the fitness cost of having unbalanced gene copies and the potential fitness gained from increased dosage of specific advantageous genes. Trypanosomatids, a family of protozoans that include species that cause neglected tropical diseases, are a relevant group to study aneuploidies. Their life cycle has several stressors that could select for different patterns of chromosomal duplications and/or losses, and their nearly universal use of polycistronic transcription increases their reliance on gene expansion/contraction, as well as post-transcriptional control as mechanisms for gene expression regulation. By evaluating the data from 866 isolates covering seven trypanosomatid genera, we have revealed that aneuploidy tolerance is an ancestral characteristic of trypanosomatids but has a reduced occurrence in a specific monophyletic clade that has undergone large genomic reorganization and chromosomal fusions. We have also identified an ancient chromosomal duplication that was maintained across these parasite's speciation, named collectively as the trypanosomatid ancestral supernumerary chromosome (TASC). TASC has most genes in the same coding strand, is expressed as a disomic chromosome (even having four copies), and has increased potential for functional variation, but it purges highly deleterious mutations more efficiently than other chromosomes. The evidence of stringent control over gene expression in this chromosome suggests that these parasites have adapted to mitigate the fitness cost associated with this ancient chromosomal duplication.

Diversity and Phylogeny of Gyrodactylus spp. (Monogenea: Gyrodactylidae) across the Strait of Gibraltar: Parasite Speciation and Historical Biogeography of West Mediterranean Cyprinid Hosts

Knowledge on the diversity of parasitic flatworms of Western Mediterranean cyprinids is extremely scarce. In the present study, we parasitologically investigated 12 cyprinid species across the Strait of Gibraltar inhabiting watersheds in northwest Africa (Morocco) and Iberia (Portugal and Spain). Taxonomically relevant features of the attachment organ and sequences of the 18S rDNA and ITS regions were used for species delineation and to investigate their phylogenetic relatedness. Among the Gyrodactylus collected from Morocco and Spain, we identified specimens with an unusual T-shaped dorsal bar observed herein for the first time. In contrast, the membranous patch-like structure surrounding the twisted inner roots of hamuli and the median ridge of the ventral bar have been generally observed in Eurasian relatives. Our analyses suggest vicariant speciation of Gyrodactylus across the Strait of Gibraltar. We describe herein G. gibraltarensis sp. nov. from Iberian Luciobarbus graellsii; G. moroccensis sp. nov. from northwest African cyprinids, i.e., L. maghrebensis, L. rabatensis, L. rifensis, L. yahyaouii, and L. zayanensis; and finally, G. pseudomoroccensis sp. nov. from Moroccan L. ksibi, all possessing a new haptoral configuration. The genetic divergence and conservative morphologies in populations of G. moroccensis sp. nov. from five cyprinid species support its ongoing speciation in Northwest Africa. The West Mediterranean lineage was revealed to be monophyletic, with Eurasian species forming a sister group. Morphologically, West Mediterranean Gyrodactylus also appeared to be of Middle Eastern origin. Gyrodactylus spp. possessing an unusual T-shaped dorsal bar have most likely speciated, allowing for the appearance of a haptoral morphology that is restricted to the region across the Strait of Gibraltar. To conclude, viviparous Gyrodactylus reflect parasite speciation across the Strait of Gibraltar and the historical biogeography of cyprinids in the West Mediterranean.

Molecular Phylogenies of Leeches and Haemoparasites Infecting Freshwater Turtles in Aquatic Ecosystems of Northern Africa Suggest Phylogenetic Congruence between Placobdella costata Sensu Lato and Haemogregarina stepanowi Sensu Lato.

Haemogregarines are blood parasites with a life-cycle involving a vertebrate as the intermediate host and an invertebrate as the definitive host and vector. Extensive phylogenetic investigations based on 18S-rRNA gene sequences have shown that Haemogregarina stepanowi (Apicomplexa: Haemogregarinidae) is able to infest a large diversity of freshwater turtle species, including the European pond turtle Emys orbicularis, the Sicilian pond turtle Emys trinacris, the Caspian turtle Mauremys caspica, the Mediterranean pond turtle Mauremys leprosa, and the Western Caspian turtle Mauremys rivulata, among others. From the same molecular markers, H. stepanowi is further considered to be a complex of cryptic species predisposed to infect the same host species. While Placobdella costata is known to be the unique vector of H. stepanowi, it is only recently that independent lineages within P. costata have been illustrated-suggesting the presence of at least five unique leech species across Western Europe. The aims of our study were therefore to investigate from mitochondrial markers (COI) the genetic diversity within haemogregarines and leeches infecting freshwater turtles of the Maghreb, in order to identify processes of parasite speciation. We showed that H. stepanowi consists of at least five cryptic species in the Maghreb, while two Placobella species were identified in the same area. Although an Eastern-Western speciation pattern was apparent for both leeches and haemogregarines, we cannot make definitive conclusions regarding co-speciation patterns between parasites and vectors. However, we cannot reject the hypothesis of a very strict host-parasite specificity within leeches.

Population Genetic Structure of Anisakis simplex Infecting the European Hake from North East Atlantic Fishing Grounds.

The European hake, one of the most commercially valuable species in ICES fishing areas, is considered an important neglected source of zoonotic risk by nematode parasites belonging to the genus Anisakis. Merluccius merluccius is, by far, the most important host of Anisakis spp. at the European fishing grounds, in terms of demographic infection values, and carries the highest parasite burden. These high parasite population densities within an individual fish host offer a chance to explore new sources of variations for the genetic structure of Anisakis spp. populations. A total of 873 Anisakis spp. third-stage larvae, originally sampled from viscera and muscular sections of hake collected at ten fishing grounds, were primarily identified using ITS rDNA region as molecular marker. After that, we used mtDNA cox2 gene to reveal the high haplotype diversity and the lack of genetic structure for A. simplex. Dominant haplotypes were shared among the different fishing areas and fish sections analyzed. Results indicate a clear connection of A. simplex from European hake along the Northern North Sea to the Portuguese coast, constituting a single genetic population but revealing a certain level of genetic sub-structuring on the Northwest coast of Scotland. This study also provides useful information to advance the understanding of parasite speciation to different fish host tissues or microenvironments.

SD-Bioline malaria rapid diagnostic test performance and time to become negative after treatment of malaria infection in Southwest Nigerian Children.

Given the challenges of microscopy, we compared its performance with SD-Bioline malaria rapid diagnostic test (MRDT) and polymerase chain reaction (PCR) and evaluated the time it took for positive results to become negative after treatment of children with acute uncomplicated malaria. We present the report of 485 participants with complete MRDT, microscopy, and PCR data out of 511 febrile children aged 3-59 months who participated in a cohort study over a 12-month period in rural and urban areas of Ibadan, Nigeria. MRDT-positive children received antimalaria and tested at every visit over 28 days. Speciation was also carried out by PCR. With microscopy as the gold standard, SD-Bioline™ had 95.2% sensitivity, 66.4% specificity, 67.5% positive predictive value (PPV), and 94.9 negative predictive value (NPV), while with PCR the findings were 84.3% sensitivity, 66.5% specificity, 72.7% PPV, and 80.1% NPV. PCR speciation of malaria parasites revealed 91.6% Plasmodium falciparum, 18.9% Plasmodium malariae, and 4.4% Plasmodium ovale. Among the 47 children with P. malariae infections, 66.0% were coinfected with P. falciparum, while 54.6% cases of P. ovale occurred as coinfections with P. falciparum. The median time to a negative MRDT was 23.2 days, while the median time to a negative malaria microscopy was 3.8 days. The two survival curves were significantly different. The SD-BiolineTM MRDT performed well, with remarkable persistence of rapid test-positive for an average of 23 days post treatment. The prevalence of P. malaria is somewhat greater than expected.

Historical dispersal and host-switching formed the evolutionary history of a globally distributed multi-host parasite – The Ligula intestinalis species complex

Studies on parasite biogeography and host spectrum provide insights into the processes driving parasite diversification. Global geographical distribution and a multi-host spectrum make the tapeworm Ligula intestinalis a promising model for studying both the vicariant and ecological modes of speciation in parasites. To understand the relative importance of host association and biogeography in the evolutionary history of this tapeworm, we analysed mtDNA and reduced-represented genomic SNP data for a total of 139 specimens collected from 18 fish-host genera across a distribution range representing 21 countries. Our results strongly supported the existence of at least 10 evolutionary lineages and estimated the deepest divergence at approximately 4.99–5.05 Mya, which is much younger than the diversification of the fish host genera and orders. Historical biogeography analyses revealed that the ancestor of the parasite diversified following multiple vicariance events and was widespread throughout the Palearctic, Afrotropical, and Nearctic between the late Miocene and early Pliocene. Cyprinoids were inferred as the ancestral hosts for the parasite. Later, from the late Pliocene to Pleistocene, new lineages emerged following a series of biogeographic dispersal and host-switching events. Although only a few of the current Ligula lineages show narrow host-specificity (to a single host genus), almost no host genera, even those that live in sympatry, overlapped between different Ligula lineages. Our analyses uncovered the impact of historical distribution shifts on host switching and the evolution of host specificity without parallel host-parasite co-speciation. Historical biogeography reconstructions also found that the parasite colonized several areas (Afrotropical and Australasian) much earlier than was suggested by only recent faunistic data.

Prevalence and speciation of malaria parasites among patients attending Ahoada and Amassoma Communities’ general hospitals in Rivers and Bayelsa State, Nigeria

Malaria is one of the deadly diseases recognized globally in children and adults especially in Nigeria and some African countries. This study was designed to determine Prevalence and Speciation of malaria parasites from patients attending Ahoada and Amassoma Communities’ General Hospitals in Rivers and Bayelsa States respectively. A total of two hundred (200) venous blood collected from Amassoma [101(40 males, 61 Female) and Ahoada [99; 46male, 53 females) into sterile Ethylene Diamine Tetra Acetic Acid (EDTA) bottles from patients attending the above mentioned General Hospitals were immediately transferred to Medical Microbiology Laboratory, Department of Medical Laboratory Science for analysis using Microscopy by staining, Rapid Diagnostic Tests kits (SD Bioline kits; Pf/pan and Pf specific kit) and molecular analysis by Polymerase Chain Reaction (PCR) technique. Twenty (20) positive samples were subjected to Polymerase Chain Reaction Technique for Speciation. Findings showed 141(70.5%) subjects positive to malaria parasites comprised of Children 25(12.5%) between age of 6 and 17 years, adult female 63(31.5%) and male 53(26.5%) between the age of 18 and 90. Also noted were subjects with age ranges of 6-10, 21-25, 51-55 and 86-90 years had the highest percentage prevalence of 100%, followed by 41-45 years with a prevalence rate of 83.3% and the least prevalence was 33.3% from 56-60 years. Observations showed that out of 20 positive samples subjected to molecular diagnosis for Speciation, 17(85%) were Plasmodium falciparum, thus revealing their predominance of 90%. In conclusion, Plasmodium falciparum was the predominant parasite among Plasmodia species responsible for malaria infection in both Rivers and Bayelsa States. Female and children are vulnerable to malaria infection as revealed in this study. Therefore, the government is encouraged to take women and children’s health into consideration by conducting malaria test for them weekly to enable prompt treatment where applicable.

Prevalence and speciation of malaria parasites among patients attending Ahoada and Amassoma Communities' general hospitals in Rivers and Bayelsa State, Nigeria

Prevalence and speciation of malaria parasites among patients attending Ahoada and Amassoma Communities' general hospitals in Rivers and Bayelsa State, Nigeria

EVALUATION OF PERFORMANCE OF TWO MONOPLEX QUANTITATIVE REAL TIME PCR ASSAYS IN COMPARISON TO MICROSCOPY FOR IDENTIFICATION OF MALARIA PARASITES.

Background: Microscopy is the gold standard for Malaria diagnosis with shortcomings such as false positives, false negatives,errors in species identification,and errors in enumeration of parasites.Quantitative real-time PCR (qPCR) has improved submicroscopic malaria diagnosis. This study evaluated the performance, concordance, correlation and methods agreement of two monoplex qPCR assays against expert malaria microscopy for the detection and enumeration of malaria parasites. Methods: This was a cross sectional study utilizing 127 archived blood samples collected from five provinces in Kenya. Malaria microscopy was conducted by two independent microscopists then 18S-rRNA-qPCR and non-18S-rRNA-qPCR assays were done to identify and quantify the infecting species.The sensitivity,specificity,and predictive values.Cohen Kappa value was used to quantify the method agreement and Bland Altman test was used to assess the bias and limits of agreement.Correlation between microscopy and qPCR parasite densities was determined by the Spearman's rank test. Statistical significance was taken at p<0.05. Results: A higher sensitivity and a lower specificity were observed in all the three plasmodium species in non 18SrRNA-qPCR compared to 18S-rRNA-qPCR. The sensitivity and specificity of 18S-rRNA-qPCR was 91.3% and 75% in detection of P.falciparum,67.6% and 88.1% in detection of P.malariae,and 55.8% and 91.4% in detection of P.ovale.The sensitivity and specificity of non 18S-rRNA-qPCR was 99.1% and 66.7% in detection of P.falciparum,77.9% and 88.1% in detection of P. malariae, and 79.4% and 90.3% in detection of P. ovale. All the positive and negative predictive values were above 70% except the negative predictive value for 18S-rRNA-qPCR (47.4%).Kappa of more than 0.5 was observed between microscopy and both18S-rRNA-qPCR and non-18S-rRNA-qPCR in the detection of all three malaria parasites. The non-18S-rRNA-qPCR method had higher kappa > 0.65,in all the three species compared to 18S-rRNA-qPCR method (kappa < 0.55).There was a clear positive correlation between microscopy parasite density and the parasite densities estimated by the 18S-rRNA-qPCR and Non-18S-rRNA-qPCR (P<0.001). Conclusion: The results showed that both monoplex realtime PCR methods demonstrated a high performance compared to microscopy proving to be better methods in the identification and speciation of malaria parasites especially of low parasitemia.The realtime PCR methods also had a positive correlation with parasite density and hence can be used in accurate determination of parasite densities when compared to microscopy. Therefore, this study recommends the utilization of realtime PCR methods in the detection,speciation and quantification of both microscopic and submicroscopic malaria parasites.

Long-distance dispersal of pigeons and doves generated new ecological opportunities for host-switching and adaptive radiation by their parasites.

Adaptive radiation is an important mechanism of organismal diversification and can be triggered by new ecological opportunities. Although poorly studied in this regard, parasites are an ideal group in which to study adaptive radiations because of their close associations with host species. Both experimental and comparative studies suggest that the ectoparasitic wing lice of pigeons and doves have adaptively radiated, leading to differences in body size and overall coloration. Here, we show that long-distance dispersal by dove hosts was central to parasite diversification because it provided new ecological opportunities for parasites to speciate after host-switching. We further show that among extant parasite lineages host-switching decreased over time, with cospeciation becoming the more dominant mode of parasite speciation. Taken together, our results suggest that host dispersal, followed by host-switching, provided novel ecological opportunities that facilitated adaptive radiation by parasites.

The Fate of the Extended Genome

The Fate of the Extended Genome

Malaria infection and anemia status in under-five children from Southern Tanzania where seasonal malaria chemoprevention is being implemented.

Malaria and anemia remain major public health challenges in Tanzania. Household socioeconomic factors are known to influence these conditions. However, it is not clear how these factors influence malaria transmission and anemia in Masasi and Nanyumbu Districts. This study presents findings on malaria and anemia situation in under-five children and its influencing socioeconomic factors in Masasi and Nanyumbu Districts, surveyed as part of an ongoing seasonal malaria chemoprevention operational study. A community-based cross-sectional survey was conducted between August and September 2020. Finger-prick blood samples collected from children aged 3-59 months were used to test for malaria infection using malaria rapid diagnostic test (mRDT), thick smears for determination of asexual and sexual parasitemia, and thin smear for parasite speciation. Hemoglobin concentration was measured using a HemoCue spectrophotometer. A structured questionnaire was used to collect household socioeconomic information from parents/caregivers of screened children. The prevalence of malaria was the primary outcome. Chi-square tests, t-tests, and logistic regression models were used appropriately. Overall mRDT-based malaria prevalence was 15.9% (373/2340), and was significantly higher in Nanyumbu (23.7% (167/705) than Masasi District (12.6% (206/1635), p<0.001. Location (Nanyumbu), no formal education, household number of people, household number of under-fives, not having a bed net, thatched roof, open/partially open eave, sand/soil floor, and low socioeconomic status were major risks for malaria infection. Some 53.9% (1196/2218) children had anemia, and the majority were in Nanyumbu (63.5% (458/705), p<0.001. Location (Nanyumbu), mRDT positive, not owning a bed net, not sleeping under bed net, open/partially open eave, thatched window, sex of the child, and age of the child were major risk factors for anemia. Prevalence of malaria and anemia was high and was strongly associated with household socioeconomic factors. Improving household socioeconomic status is expected to reduce the prevalence of the conditions in the area.

The interplay between host biogeography and phylogeny in structuring diversification of the feather louse genus Penenirmus

Parasite diversification is influenced by many of the same factors that affect speciation of free-living organisms, such as biogeographic barriers. However, the ecology and evolution of the host lineage also has a major impact on parasite speciation. Here we explore the interplay between biogeography and host-association on the pattern of diversification in a group of ectoparasitic lice (Insecta: Phthiraptera: Penenirmus) that feeds on the feathers of woodpeckers, barbets, and honeyguides (Piciformes) and some songbirds (Passeriformes). We use whole genome sequencing of 41 ingroup and 12 outgroup samples to develop a phylogenomic dataset of DNA sequences from a reference set of 2395 single copy ortholog genes, for a total of nearly four million aligned base positions. The phylogenetic trees resulting from both concatenated and gene-tree/species-tree coalescent analyses were nearly identical and highly supported. These trees recovered the genus Penenirmus as monophyletic and identified several major clades, which tended to be associated with one major host group. However, cophylogenetic analysis revealed that host-switching was a prominent process in the diversification of this group. This host-switching generally occurred within single major biogeographic regions. We did, however, find one case in which it appears that a rare dispersal event by a woodpecker lineage from North America to Africa allowed its associated louse to colonize a woodpecker in Africa, even though the woodpecker lineage from North America never became established there.

Atypical behavior of a black fly species connects cavity-nesting birds with generalist blood parasites in an arid area of Spain

BackgroundThe feeding behavior of bloodsucking insects determines the transmission, distribution, host spectrum and evolution of blood parasites in the wild. Conventional wisdom suggests that some vector groups (e.g. black flies, family Simuliidae) are consistently exophagous daytime biters. We aimed to understand more about the exceptions to this pattern by combining targeted trapping and molecular identification of parasites in vectors.MethodsIn this study, we collected black flies in nest boxes used by European rollers Coracias garrulus in southeastern Spain. We molecularly analyzed 434 individual insects, identifying the black fly species caught in the nest boxes, their potential vertebrate blood meals, and the haemosporidian parasite lineages that they carried.ResultsOnly one black fly species, Simulium rubzovianum, appeared to enter the nest boxes of rollers. Among the trapped specimens, 15% contained vertebrate DNA, which always belonged to rollers, even though only half of those specimens were visibly engorged. Furthermore, 15% of all black flies contained Leucocytozoon lineages, indicating previous feeding on avian hosts but probably not on infected adult rollers. The known vertebrate hosts of the recorded Leucocytozoon lineages suggested that large and/or abundant birds are their hosts. Particularly represented were cavity-nesting species breeding in the vicinity, such as pigeons, corvids and owls. Open-nesting species such as thrushes and birds of prey were also represented.ConclusionsOur data strongly suggest that S. rubzovianum bites uninfected roller nestlings and infected individuals of other species, potentially incubating adults, inside nest boxes and natural cavities. This simuliid does not appear to have a strong preference for specific host clades. Contrary to the general pattern for the group, and possibly enhanced by the harsh environmental conditions in the study area, this black fly appeared to intensively use and may even have a preference for confined spaces such as cavities for feeding and resting. Preferences of vectors for atypical microhabitat niches where hosts are less mobile may enable social and within-family transmission and parasite speciation in the long term. At the same time, a lack of host preference in concentrated multispecies communities can lead to host switches. Both processes may be underappreciated driving forces in the evolution of avian blood parasites.Graphical abstract

Assessment of Platelet Numbers and Prevalence of Thrombocytopenia among Children with Severe Malaria at a Tertiary Teaching Hospital

Background: Thrombocytopenia plays an important role in the diagnosis of malaria in most countries because of the rapid decrease of platelets during malaria onset and also in severe forms of the disease. The study sought to assess platelet numbers and determine the prevalence of malarial thrombocytopenia among children with febrile malaria at the Korle-Bu Teaching Hospital (KBTH). Methodology: It was a cross-sectional study carried out in the Department of Child Health and the Polyclinic of KBTH from April to July 2018. A total of 100 children aged from 1 to 12 years who tested malaria positive for both thick and thin blood film and Rapid Diagnostic Tests (RDTs) were recruited into the study. Venous blood sample was obtained from the children and analyzed for platelet count using a haematology auto analyzer. Parasite speciation and quantification was used to classify the disease into mild, moderate and severe, and platelet numbers were also categorized into low, normal and high. Data obtained was then analyzed for prevalence of malarial thrombocytopenia in severe malaria. Results: The total studied participants were 100, 61 (61%) were males whiles 39 (39%) were females. Both severe malaria and thrombocytopenia were mostly seen in children less than 5 years of age and the males recorded more thrombocytopenia (66%) and normal platelet numbers 34 (64.2%) than the females. There was a significant higher percentage of malaria children with thrombocytosis being females (64%) as compared to those being males (36%). 53 (53%) children had normal platelet numbers, 33 (33%) had thrombocytopenia, and 14 (14%) had thrombocytosis. The prevalence of uncomplicated malaria and complicated malaria were 80% and 20% respectively. The overall prevalence of thrombocytopenia was 33%, and the prevalence of thrombocytopenia in uncomplicated and severe malaria was 18.8% and 90% respectively. The prevalence of malaria types among children with thrombocytopenia was assessed. Out of the 33 (33%) patients who had thrombocytopenia, 15 (45.5%) of them had uncomplicated malaria and 18 (54.5%) of them had complicated or severe malaria. No child was found to have thrombocytosis during complicated malaria. Conclusion: The study indicates a significant higher prevalence of thrombocytopenia in severe malaria among children at the Korle-Bu Teaching Hospital, and this could be used as a useful indicator to investigate malaria or as a diagnostic clue for malaria in children.

Dictyocoela microsporidia diversity and co-diversification with their host, a gammarid species complex (Crustacea, Amphipoda) with an old history of divergence and high endemic diversity

BackgroundAlthough the processes of co-evolution between parasites and their hosts are well known, evidence of co-speciation remains scarce. Microsporidian intracellular parasites, due to intimate relationships with their hosts and mixed mode of transmission (horizontal but also vertical, from mother to offspring), may represent an interesting biological model for investigating co-speciation. Amphipod crustaceans, especially gammarids, are regular hosts of microsporidian parasites, in particular the Dictyocoela spp., which have so far been found limited to these amphipods and are known to use a vertical mode of transmission. The amphipod genus Gammarus has a diversification history spanning the last 50–60 Mya and an extensive cryptic diversity in most of the nominal species. Here, we investigated the degree of co-diversification between Dictyocoela and Gammarus balcanicus, an amphipod with high degrees of ancient cryptic diversification and lineage endemism, by examining the genetic diversity of these parasites over the entire geographic range of the host. We hypothesised that the strong host diversification and vertical transmission of Dictyocoela would promote co-diversification.ResultsUsing the parasite SSU rDNA as a molecular marker, analyzing 2225 host specimens from 88 sites covering whole host range, we found 31 haplogroups of Dictyocoela, 30 of which were novel, belonging to four Dictyocoela species already known to infect other Gammarus spp. The relationships between Dictyocoela and gammarids is therefore ancient, with the speciation in parasites preceding those of the hosts. Each novel haplogroup was nevertheless specific to G. balcanicus, leaving the possibility for subsequent co-diversification process during host diversification. A Procrustean Approach to Co-phylogeny (PACo) analysis revealed that diversification of Dictyocoela was not random with respect to that of the host. We found high degrees of congruence between the diversification of G. balcanicus and that of Dictyocoela roeselum and D. muelleri. However, we also found some incongruences between host and Dictyocoela phylogenies, e.g. in D. duebenum, probably due to host shifts between different G. balcanicus cryptic lineages.ConclusionThe evolutionary history of Dictyocoela and Gammarus balcanicus represents an example of an overall host-parasite co-diversification, including cases of host shifts.

Taxon pulse dynamics, episodic dispersal and host colonization across Beringia drive diversification of a Holarctic tapeworm assemblage

AbstractAimWe test the predictions of the Stockholm Paradigm, a synthesis of eco‐evolutionary theory explaining the nature of faunal assembly, host range and parasite diversification. Faunal diversification and assembly, manifested in patterns of host colonization, co‐adaptation and parasite speciation, are predicted to emerge as a consequence of alternating episodes of ecological disruption and stability. Specifically, for a diverse cestode genus (Arostrilepis), we evaluate the number and direction of Pleistocene dispersal events across Beringia, the number and relative timing of host colonization events and the relationship between host and parasite biogeographic histories and associations through time.LocationBeringia and adjacent temperate to arctic biomes in North America and Eurasia.TaxonArostrilepis (Cyclophyllidea: Hymenolepididae) and its rodent hosts.MethodsMulti‐locus phylogenetic reconstruction and biogeographic ancestral range estimation.ResultsArostrilepis lineages crossed Beringia eastward into North America a minimum of four times and westward into Asia twice in association with temporally disjunct geographic expansions of three major tribes of cricetid rodents (Arvicolini, Myodini, Lemmini). Inferences of ancestral host associations support at least nine instances of host colonization involving shifts from one rodent tribe or family to another. Several previously unrecognized lineages of Arostrilepis are revealed.Main conclusionsConsistent with expectations of the Stockholm Paradigm, episodes of intercontinental dispersal were both frequent in the history of Arostrilepis and preceded a majority of inferred host‐colonization events. Events of historical geographic expansion created numerous opportunities for development of novel host–parasite associations through ecological fitting, as parasites tracked historically conserved resources available across diverse host taxa. Beringia played a major role in shaping rodent/parasite assemblages by mediating dispersal between the northern continents during glacial episodes of the Pleistocene, rather than by serving as a zone of refugial isolation.

Ecological divergence and hybridization of Neotropical Leishmania parasites

The tropical Andes are an important natural laboratory to understand speciation in many taxa. Here we examined the evolutionary history of parasites of the Leishmania braziliensis species complex based on whole-genome sequencing of 67 isolates from 47 localities in Peru. We first show the origin of Andean Leishmania as a clade of near-clonal lineages that diverged from admixed Amazonian ancestors, accompanied by a significant reduction in genome diversity and large structural variations implicated in host-parasite interactions. Within the Andean species, patterns of population structure were strongly associated with biogeographical origin. Molecular clock and ecological niche modeling suggested that the history of diversification of the Andean lineages is limited to the Late Pleistocene and intimately associated with habitat contractions driven by climate change. These results suggest that changes in forestation over the past 150,000 y have influenced speciation and diversity of these Neotropical parasites. Second, genome-scale analyses provided evidence of meiotic-like recombination between Andean and Amazonian Leishmania species, resulting in full-genome hybrids. The mitochondrial genome of these hybrids consisted of homogeneous uniparental maxicircles, but minicircles originated from both parental species. We further show that mitochondrial minicircles-but not maxicircles-show a similar evolutionary pattern to the nuclear genome, suggesting that compatibility between nuclear-encoded mitochondrial genes and minicircle-encoded guide RNA genes is essential to maintain efficient respiration. By comparing full nuclear and mitochondrial genome ancestries, our data expand our appreciation on the genetic consequences of diversification and hybridization in parasitic protozoa.