Host and parasite life history interplay to yield divergent population genetic structures in two ectoparasites living on the same bat species

Host–parasite interactions are ubiquitous in nature. However, how parasite population genetic structure is shaped by the interaction between host and parasite life history remains understudied. Studies comparing multiple parasites infecting a single host can be used to investigate how different parasite life history traits interplay with host behaviour and life history. In this study, we used 10 newly developed microsatellite loci to investigate the genetic structure of a parasitic bat fly (Basilia nana). Its host, the Bechstein's bat (Myotis bechsteinii), has a social system and roosting behaviour that restrict opportunities for parasite transmission. We compared fly genetic structure to that of the host and another parasite, the wing‐mite, Spinturnix bechsteini. We found little spatial or temporal genetic structure in B. nana, suggesting a large, stable population with frequent genetic exchange between fly populations from different bat colonies. This contrasts sharply with the genetic structure of the wing‐mite, which is highly substructured between the same bat colonies as well as temporally unstable. Our results suggest that although host and parasite life history interact to yield similar transmission patterns in both parasite species, the level of gene flow and eventual spatiotemporal genetic stability is differentially affected. This can be explained by the differences in generation time and winter survival between the flies and wing‐mites. Our study thus exemplifies that the population genetic structure of parasites on a single host can vary strongly as a result of how their individual life history characteristics interact with host behaviour and life history traits.     

Phoretic dispersal influences parasite population genetic structure

Dispersal is a fundamental component of the life history of most species. Dispersal influences fitness, population dynamics, gene flow, genetic drift and population genetic structure. Even small differences in dispersal can alter ecological interactions and trigger an evolutionary cascade. Linking such ecological processes with evolutionary patterns is difficult, but can be carried out in the proper comparative context. Here, we investigate how differences in phoretic dispersal influence the population genetic structure of two different parasites of the same host species. We focus on two species of host‐specific feather lice (Phthiraptera: Ischnocera) that co‐occur on feral rock pigeons (Columba livia). Although these lice are ecologically very similar, “wing lice” (Columbicola columbae) disperse phoretically by “hitchhiking” on pigeon flies (Diptera: Hippoboscidae), while “body lice” (Campanulotes compar) do not. Differences in the phoretic dispersal of these species are thought to underlie observed differences in host specificity, as well as the degree of host–parasite cospeciation. These ecological and macroevolutionary patterns suggest that body lice should exhibit more genetic differentiation than wing lice. We tested this prediction among lice on individual birds and among lice on birds from three pigeon flocks. We found higher levels of genetic differentiation in body lice compared to wing lice at two spatial scales. Our results indicate that differences in phoretic dispersal can explain microevolutionary differences in population genetic structure and are consistent with macroevolutionary differences in the degree of host–parasite cospeciation.     

Population structure and dispersal of the coral‐excavating sponge Cliona delitrix

Some excavating sponges of the genus Cliona compete with live reef corals, often killing and bioeroding entire colonies. Important aspects affecting distribution of these species, such as dispersal capability and population structure, remain largely unknown. Thus, the aim of this study was to determine levels of genetic connectivity and dispersal of Cliona delitrix across the Greater Caribbean (Caribbean Sea, Bahamas and Florida), to understand current patterns and possible future trends in their distribution and effects on coral reefs. Using ten species‐specific microsatellite markers, we found high levels of genetic differentiation between six genetically distinct populations: one in the Atlantic (Florida‐Bahamas), one specific to Florida and four in the South Caribbean Sea. In Florida, two independent breeding populations are likely separated by depth. Gene flow and ecological dispersal occur among other populations in the Florida reef tract, and between some Florida locations and the Bahamas. Similarly, gene flow occurs between populations in the South Caribbean Sea, but appears restricted between the Caribbean Sea and the Atlantic (Florida‐Bahamas). Dispersal of C. delitrix was farther than expected for a marine sponge and favoured in areas where currents are strong enough to transport sponge eggs or larvae over longer distances. Our results support the influence of ocean current patterns on genetic connectivity, and constitute a baseline to monitor future C. delitrix trends under climate change.     

The influence of dispersal on macroecological patterns of Lesser Antillean birds

Aim Dispersal is often assumed to be a major force in shaping macroecological patterns, but this is rarely tested. Here I describe macroecological patterns for two groups of Lesser Antillean birds and then use population genetic data to assess if differences in dispersal ability could be responsible for the groups’ contrasting patterns. Importantly, the population genetic data are derived independently from any data used to generate the macroecological patterns. Location The Lesser Antilles, Caribbean. Methods I used data from the literature to construct species–area curves and evaluate the decline in species compositional similarity with geographic distance (hereafter distance–decay) for two sets of bird communities in the Lesser Antilles, those found in rain forest and those in dry forest. I then used mitochondrial DNA sequences from island populations to assess the dispersal ability of rain forest and dry forest species. Results Rain forest species show steeper species–area curves and greater distance–decay in community similarity than dry forest species, patterns that could be explained by rain forest species having more limited dispersal ability. Both conventional analyses of M, the number of migrants per generation between populations, and alternative analyses of D_A, the genetic distance between populations, suggest that rain forest species disperse between islands less frequently than dry forest species. Main conclusions Differences in dispersal ability are a plausible explanation for the contrasting macroecological patterns of rain forest and dry forest species. Additionally, historical factors, such as the taxon cycle and Pleistocene climate fluctuations, may have played a role in shaping the distribution patterns of Lesser Antillean birds.     

Ecological coassociations influence species' responses to past climatic change: an example from a Sonoran Desert bark beetle

Ecologically interacting species may have phylogeographical histories that are shaped both by features of their abiotic landscape and by biotic constraints imposed by their coassociation. The Baja California peninsula provides an excellent opportunity to examine the influence of abiotic vs. biotic factors on patterns of diversity in plant-insect species. This is because past climatic and geological changes impacted the genetic structure of plants quite differently to that of codistributed free-living animals (e.g. herpetofauna and small mammals). Thus, ‘plant-like’ patterns should be discernible in host-specific insect herbivores. Here, we investigate the population history of a monophagous bark beetle, Araptus attenuatus, and consider drivers of phylogeographical patterns in the light of previous work on its host plant, Euphorbia lomelii. Using a combination of phylogenetic, coalescent-simulation-based and exploratory analyses of mitochondrial DNA sequences and nuclear genotypic data, we found that the evolutionary history of A. attenuatus exhibits similarities to its host plant that are attributable to both biotic and abiotic processes. Southward range expansion and recent colonization of continental Sonora from the Baja peninsula appear to be unique to this taxon pair and probably reflect influences of the host plant. On the other hand, abiotic factors with landscape-level influences on a diverse suite of codistributed arid-adapted taxa, such as Plio- and Pleistocene-aged marine incursions in the region, also left genetic signatures in beetle and host plant populations. Superimposed on these similarities, bark beetle-specific patterns and processes were also evident: our data revealed two secondarily sympatric, reproductively isolated genetic lineages, as well as a previously unrecognized mid-peninsular warm desert refuge. Taken together, this work illustrates that the evolutionary history of species-specific insect herbivores may represent a mosaic of influences, including—but not limited to—those imposed by the host plant.     

Host-specialization and species diversity in fish parasites: phylogenetic conservatism?

The pattern of parasite species diversification and specialization, appreciated by host range, is investigated in fish parasites. We test whether host range is linked with phylogeny at a high taxonomic level, and if there is a relationship between host range and host species diversification. For this purpose we used two sets of data, one on macro-parasites of marine fishes of the Mediterranean Sea and the other on macro-parasites of marine and freshwater fishes of Canada. Similar patterns of host range among parasitic groups were found. Our findings suggest that habitat (marine vs freshwater) and geographic localization (Canada vs Mediterranean region) play little role in determining the observed patterns of host range. We highlight the potential influence of phylogeny (high-taxonomic level) on the level host range in parasites. We find that parasites with free-swimming larval stages and with direct life cycles have a narrower range of host species than do parasites with indirect life cycle, even if we cannot control for phylogenetic effects because of the lack of variation of life cycles within each parasitic group. Finally, a positive relationship was found between the number of known hosts and parasite species diversity in the case of Mediterranean parasite species. The relationship between host range and species diversification should be related to the mechanism of cospeciation.     

Isolation over 35 years in a heated biotest basin causes selection on MHC class IIß genes in the European perch (Perca fluviatilis L.)

Genes that play key roles in host immunity such as the major histocompatibility complex (MHC) in vertebrates are expected to be major targets of selection. It is well known that environmental conditions can have an effect on host–parasite interactions and may thus influence the selection on MHC. We analyzed MHC class IIß variability over 35 years in a population of perch (Perca fluviatilis) from the Baltic Sea that was split into two populations separated from each other. One population was subjected to heating from cooling water of a nuclear power plant and was isolated from the surrounding environment in an artificial lake, while the other population was not subjected to any change in water temperature (control). The isolated population experienced a change of the allelic composition and a decrease in allelic richness of MHC genes compared to the control population. The two most common MHC alleles showed cyclic patterns indicating ongoing parasite–host coevolution in both populations, but the alleles that showed a cyclic behavior differed between the two populations. No such patterns were observed at alleles from nine microsatellite loci, and no genetic differentiation was found between populations. We found no indications for a genetic bottleneck in the isolated population during the 35 years. Additionally, differences in parasitism of the current perch populations suggest that a change of the parasite communities has occurred over the isolation period, although the evidence in form of in‐depth knowledge of the change of the parasite community over time is lacking. Our results are consistent with the hypothesis of a selective sweep imposed by a change in the parasite community.     

Population Genetics of a Trochid Gastropod Broadens Picture of Caribbean Sea Connectivity

Background

Regional genetic connectivity models are critical for successful conservation and management of marine species. Even though rocky shore invertebrates have been used as model systems to understand genetic structure in some marine environments, our understanding of connectivity in Caribbean communities is based overwhelmingly on studies of tropical fishes and corals. In this study, we investigate population connectivity and diversity of Cittarium pica, an abundant rocky shore trochid gastropod that is commercially harvested across its natural range, from the Bahamas to Venezuela.

Methodology/Principal Findings

We tested for genetic structure using DNA sequence variation at the mitochondrial COI and 16S loci, AMOVA and distance-based methods. We found substantial differentiation among Caribbean sites. Yet, genetic differentiation was associated only with larger geographic scales within the Caribbean, and the pattern of differentiation only partially matched previous assessments of Caribbean connectivity, including those based on larval dispersal from hydrodynamic models. For instance, the Bahamas, considered an independent region by previous hydrodynamic studies, showed strong association with Eastern Caribbean sites in our study. Further, Bonaire (located in the east and close to the meridional division of the Caribbean basin) seems to be isolated from other Eastern sites.

Conclusions/Significance

The significant genetic structure and observed in C. pica has some commonalities in pattern with more commonly sampled taxa, but presents features, such as the differentiation of Bonaire, that appear unique. Further, the level of differentiation, together with regional patterns of diversity, has important implications for the application of conservation and management strategies in this commercially harvested species.     

The socially parasitic ant Polyergus mexicanus has host‐associated genetic population structure and related neighbouring colonies

The genetic structure of populations can be both a cause and a consequence of ecological interactions. For parasites, genetic structure may be a consequence of preferences for host species or of mating behaviour. Conversely, genetic structure can influence where conspecific interactions among parasites lay on a spectrum from cooperation to conflict. We used microsatellite loci to characterize the genetic structure of a population of the socially parasitic dulotic (aka “slave‐making”) ant (Polyergus mexicanus), which is known for its host‐specificity and conspecific aggression. First, we assessed whether the pattern of host species use by the parasite has influenced parasite population structure. We found that host species use was correlated with subpopulation structure, but this correlation was imperfect: some subpopulations used one host species nearly exclusively, while others used several. Second, we examined the viscosity of the parasite population by measuring the relatedness of pairs of neighbouring parasitic ant colonies at varying distances from each other. Although natural history observations of local dispersal by queens suggested the potential for viscosity, there was no strong correlation between relatedness and distance between colonies. However, 35% of colonies had a closely related neighbouring colony, indicating that kinship could potentially affect the nature of some interactions between colonies of this social parasite. Our findings confirm that ecological forces like host species selection can shape the genetic structure of parasite populations, and that such genetic structure has the potential to influence parasite‐parasite interactions in social parasites via inclusive fitness.     

Mites as biological tags of their hosts

Movements and spatial distribution of host populations are expected to shape the genetic structure of their parasite populations. Comparing the genetic patterns of both interacting species may improve our understanding of their evolutionary history. Moreover, genetic analyses of parasites with horizontal transmission may serve as indicators of historical events or current demographic processes that are not apparent in the genetic signature of their hosts. Here, we compared mitochondrial variation in populations of the ectoparasitic mite Spinturnix myoti with the genetic pattern of its host, the Maghrebian bat Myotis punicus in North Africa and in the islands of Corsica and Sardinia. Mite mitochondrial differentiation among populations was correlated with both host mitochondrial and nuclear differentiation, suggesting spatial co‐differentiation of the lineages of the two interacting species. Therefore our results suggest that parasite dispersal is exclusively mediated by host movements, with open water between landmasses as a main barrier for host and parasite dispersal. Surprisingly the unique presence of a continental European mite lineage in Corsica was inconsistent with host phylogeographical history and strongly suggests the former presence of European mouse‐eared bats on this island. Parasites may thus act as biological tags to reveal the presence of their now locally extinct host.     

Local adaptation and oceanographic connectivity patterns explain genetic differentiation of a marine diatom across the North Sea–Baltic Sea salinity gradient

Drivers of population genetic structure are still poorly understood in marine micro‐organisms. We exploited the North Sea–Baltic Sea transition for investigating the seascape genetics of a marine diatom, Skeletonema marinoi. Eight polymorphic microsatellite loci were analysed in 354 individuals from ten locations to analyse population structure of the species along a 1500‐km‐long salinity gradient ranging from 3 to 30 psu. To test for salinity adaptation, salinity reaction norms were determined for sets of strains originating from three different salinity regimes of the gradient. Modelled oceanographic connectivity was compared to directional relative migration by correlation analyses to examine oceanographic drivers. Population genetic analyses showed distinct genetic divergence of a low‐salinity Baltic Sea population and a high‐salinity North Sea population, coinciding with the most evident physical dispersal barrier in the area, the Danish Straits. Baltic Sea populations displayed reduced genetic diversity compared to North Sea populations. Growth optima of low salinity isolates were significantly lower than those of strains from higher native salinities, indicating local salinity adaptation. Although the North Sea–Baltic Sea transition was identified as a barrier to gene flow, migration between Baltic Sea and North Sea populations occurred. However, the presence of differentiated neutral markers on each side of the transition zone suggests that migrants are maladapted. It is concluded that local salinity adaptation, supported by oceanographic connectivity patterns creating an asymmetric migration pattern between the Baltic Sea and the North Sea, determines genetic differentiation patterns in the transition zone.     

Phylogeography of related diadromous species in continental and island settings,and a comparison of their potential and realized dispersal patterns

Aim To compare patterns of potential and realized dispersal in ecologically similar and phylogenetically related amphidromous shrimps (Atyidae) in continental and island‐dominated landscapes. Location Eastern Australia and the Caribbean region. Methods Population genetic and phylogeographic analyses of mitochondrial DNA data for Australatya striolata from eastern Australia (a continental landscape) and Atya scabra from the Caribbean (an island‐dominated landscape). Results Australatya striolata contained two highly divergent genetic lineages in eastern Australia, corresponding to the disjunct northern and southern populations, respectively. These lineages probably represent allopatric cryptic species, both of which were found to have genetically homogeneous population structures within their regions of occurrence. Atya scabra was genetically homogeneous throughout the Caribbean. Recent population expansions were detected for Atya scabra in the Caribbean, but not for northern or southern Australatya striolata. Main conclusions The findings of this study are consistent with previously reported patterns of genetic population structure in amphidromous species in both continental and island‐dominated landscapes, suggesting that potential for widespread dispersal is typically matched by realized patterns of panmixia. We therefore raise the hypothesis that landscape setting (i.e. continent or island‐dominated) does not influence dispersal patterns in amphidromous species. Further studies, especially of population genetic patterns of amphidromous species on continents, are needed to test this idea. Interestingly, results of the genetic neutrality tests led us to hypothesize that demographic and drift‐mutation equilibrium is attainable although not always evident for amphidromous species on continents, but is not attainable for those species distributed across island settings.     

Dispersal in a parasitic worm and its two hosts: consequence for local adaptation

Characterizing host and parasite population genetic structure and estimating gene flow among populations is essential for understanding coevolutionary interactions between hosts and parasites. We examined the population genetic structure of the trematode Schistosoma mansoni and its two host species (the definitive host Rattus rattus and the intermediate host Biomphalaria glabrata) using microsatellite markers. Parasites were sampled from rats. The study was conducted in five sites of the Guadeloupe Island, Lesser Antilles. Mollusks display a pattern of isolation by distance whereas such a pattern is not found neither in schistosomes nor in rats. The comparison of the distribution of genetic variability in S. mansoni and its two host species strongly suggests that migration of parasites is principally determined by that of the vertebrate host in the marshy focus of Guadeloupe. However, the comparison between genetic differentiation values in schistosomes and rats suggests that the efficacy of the schistosome rat-mediated dispersal between transmission sites is lower than expected given the prevalence, parasitic load and migration rate of rats among sites. This could notably suggest that rat migration rate could be negatively correlated to the age or the infection status of individuals. Models made about the evolution of local adaptation in function of the dispersal rates of hosts and parasites suggest that rats and mollusks should be locally adapted to their parasites.     

Population structure of a vector‐borne plant parasite

Parasites are among the most diverse groups of life on Earth, yet complex natural histories often preclude studies of their speciation processes. The biology of parasitic plants facilitates in situ collection of data on both genetic structure and the mechanisms responsible for that structure. Here, we studied the role of mating, dispersal and establishment in host race formation of a parasitic plant. We investigated the population genetics of a vector‐borne desert mistletoe (Phoradendron californicum) across two legume host tree species (Senegalia greggii and Prosopis velutina) in the Sonoran desert using microsatellites. Consistent with host race formation, we found strong host‐associated genetic structure in sympatry, little genetic variation due to geographic site and weak isolation by distance. We hypothesize that genetic differentiation results from differences in the timing of mistletoe flowering by host species, as we found initial flowering date of individual mistletoes correlated with genetic ancestry. Hybrids with intermediate ancestry were detected genetically. Individuals likely resulting from recent, successful establishment events following dispersal between the host species were detected at frequencies similar to hybrids between host races. Therefore, barriers to gene flow between the host races may have been stronger at mating than at dispersal. We also found higher inbreeding and within‐host individual relatedness values for mistletoes on the more rare and isolated host species (S. greggii). Our study spanned spatial scales to address how interactions with both vectors and hosts influence parasitic plant structure with implications for parasite virulence evolution and speciation.     

Impact of a mouth parasite in a marine fish differs between geographical areas

Considerable variation exists in parasite virulence and host tolerance which may have a genetic and/or environmental basis. In this article, we study the effects of a striking, mouth‐dwelling, blood‐feeding isopod parasite (Ceratothoa italica) on the life history and physiological condition of two Mediterranean populations of the coastal fish, Lithognathus mormyrus. The growth and hepatosomatic index (HSI) of fish in a heavily human‐exploited population were severely impacted by this parasite, whereas C. italica showed negligible virulence in fish close to a marine protected area. In particular, for HSI, the parasite load explained 34.4% of the variation in HSI in the exploited population, whereas there was no significant relationship (0.3%) between parasite load and HSI for fish in the marine protected area. Both host and parasite populations were not differentiated for neutral genetic variation and were likely to exchange migrants. We discuss the role of local genetic adaptation and phenotypic plasticity, and how deteriorated environmental conditions with significant fishing pressure can exacerbate the effects of parasitism. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 842–852.     

Divergent parasite infections in sympatric cichlid species in Lake Victoria

Parasitism has been proposed as a factor in host speciation, as an agent affecting coexistence of host species in species‐rich communities and as a driver of post‐speciation diversification. Young adaptive radiations of closely related host species of varying ecological and genomic differentiation provide interesting opportunities to explore interactions between patterns of parasitism, divergence and coexistence of sympatric host species. Here, we explored patterns in ectoparasitism in a community of 16 fully sympatric cichlid species at Makobe Island in Lake Victoria, a model system of vertebrate adaptive radiation. We asked whether host niche, host abundance or host genetic differentiation explains variation in infection patterns. We found significant differences in infections, the magnitude of which was weakly correlated with the extent of genomic divergence between the host species, but more strongly with the main ecological gradient, water depth. These effects were most evident with infections of Cichlidogyrus monogeneans, whereas the only host species with a strictly crevice‐dwelling niche, Pundamilia pundamilia, deviated from the general negative relationship between depth and parasitism. In accordance with the Janzen–Connell hypothesis, we also found that host abundance tended to be positively associated with infections in some parasite taxa. Data on the Pundamilia sister species pairs from three other islands with variable degrees of habitat (crevice) specialization suggested that the lower parasite abundance of P. pundamilia at Makobe could result from both habitat specialization and the evolution of specific resistance. Our results support influences of host genetic differentiation and host ecology in determining infections in this diverse community of sympatric cichlid species.     

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.