Karen D. McCoy

Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla

Mothers are predicted to invest in their offspring depending on the quality of their mate, their opportunity to invest in future reproduction and the characteristics of the habitat in which their offspring will be born. Recent studies have suggested a transfer of maternal immunity to offspring as an induced response to the local presence of parasites in the environment, but evidence has been indirect. Here, we show the presence of antibodies against the Lyme disease agent Borrelia burgdorferi sensu lato, a spirochaete transmitted by the seabird tick Ixodes uriae, in the eggs of kittiwakes Rissa tridactyla. We report higher prevalence of antibodies against Borrelia in eggs from breeding areas with higher prevalence and abundance of ticks. Further, high repeatabilities of antibody–positive eggs within clutches and between first and replacement clutches show that, within a breeding season, females differ consistently with respect to the expression of this induced maternal response. Our results suggest that mothers can alter investment in their young depending on local conditions. Such maternal effects clearly have implications for the ecology and evolution of host–parasite interactions.

Public information affects breeding dispersal in a colonial bird: kittiwakes cue on neighbours

Habitat selection and dispersal behaviour are key processes in evolutionary ecology. Recent studies have suggested that individuals may use the reproductive performance of conspecifics as a source of public information on breeding patch quality for dispersal decisions, but experimental evidence is still limited for species breeding in aggregates, i.e. colonial species. We addressed this issue by manipulating the local breeding success of marked individuals and that of their neighbours on a series of breeding patches of a colonial seabird, the black-legged kittiwake (Rissa tridactyla). Based on previous observations in this species, we predicted that individuals that lost their eggs on successful patches would attend their nest and come back to it the year after at a higher rate than individuals that lost their eggs on patches where their neighbours were also in failure. As predicted, the attendance of breeders and prospectors was strongly affected by the local level of breeding success, resulting in differential site fidelity and recruitment. This suggests that individuals used information conveyed by conspecific breeding performance to make decisions relative to breeding site selection. This process can amplify the response of these populations to environmental change and may have contributed to the evolution of colonial breeding.

Host race formation in the Acari

Host race formation generates diversity within species and may even lead to speciation. This phenomenon could be particularly prevalent in the Acari due to the often intimate interaction these species have with their hosts. In this review, we explore the process of host race formation, whether it is likely to occur in this group and what features may favour its evolution. Although few studies are currently available and tend to be biased toward two model species, results suggest that host races are indeed common in this group, and more likely to occur when hosts are long-lived. We discuss future directions for research on host-associated adaptations in this group of organisms and the potential relevance of host race formation for the biodiversity of mites and ticks.

Changing distributions of ticks: causes and consequences.

Today, we are witnessing changes in the spatial distribution and abundance of many species, including ticks and their associated pathogens. Evidence that these changes are primarily due to climate change, habitat modifications, and the globalisation of human activities are accumulating. Changes in the distribution of ticks and their invasion into new regions can have numerous consequences including modifications in their ecological characteristics and those of endemic species, impacts on the dynamics of local host populations and the emergence of human and livestock disease. Here, we review the principal causes for distributional shifts in tick populations and their consequences in terms of the ecological attributes of the species in question (i.e. phenotypic and genetic responses), pathogen transmission and disease epidemiology. We also describe different methodological approaches currently used to assess and predict such changes and their consequences. We finish with a discussion of new research avenues to develop in order to improve our understanding of these host–vector–pathogen interactions in the context of a changing world.

The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen, Coxiella burnetii

Q fever is a highly infectious disease with a worldwide distribution. Its causative agent, the intracellular bacterium Coxiella burnetii, infects a variety of vertebrate species, including humans. Its evolutionary origin remains almost entirely unknown and uncertainty persists regarding the identity and lifestyle of its ancestors. A few tick species were recently found to harbor maternally-inherited Coxiella-like organisms engaged in symbiotic interactions, but their relationships to the Q fever pathogen remain unclear. Here, we extensively sampled ticks, identifying new and atypical Coxiella strains from 40 of 58 examined species, and used this data to infer the evolutionary processes leading to the emergence of C. burnetii. Phylogenetic analyses of multi-locus typing and whole-genome sequencing data revealed that Coxiella-like organisms represent an ancient and monophyletic group allied to ticks. Remarkably, all known C. burnetii strains originate within this group and are the descendants of a Coxiella-like progenitor hosted by ticks. Using both colony-reared and field-collected gravid females, we further establish the presence of highly efficient maternal transmission of these Coxiella-like organisms in four examined tick species, a pattern coherent with an endosymbiotic lifestyle. Our laboratory culture assays also showed that these Coxiella-like organisms were not amenable to culture in the vertebrate cell environment, suggesting different metabolic requirements compared to C. burnetii. Altogether, this corpus of data demonstrates that C. burnetii recently evolved from an inherited symbiont of ticks which succeeded in infecting vertebrate cells, likely by the acquisition of novel virulence factors.

Worldwide distribution and diversity of seabird ticks : implications for the ecology and epidemiology of tick-borne pathogens

The ubiquity of ticks and their importance in the transmission of pathogens involved in human and livestock diseases are reflected by the growing number of studies focusing on tick ecology and the epidemiology of tick-borne pathogens. Likewise, the involvement of wild birds in dispersing pathogens and their role as reservoir hosts are now well established. However, studies on tick-bird systems have mainly focused on land birds, and the role of seabirds in the ecology and epidemiology of tick-borne pathogens is rarely considered. Seabirds typically have large population sizes, wide geographic distributions, and high mobility, which make them significant potential players in the maintenance and dispersal of disease agents at large spatial scales. They are parasitized by at least 29 tick species found across all biogeographical regions of the world. We know that these seabird-tick systems can harbor a large diversity of pathogens, although detailed studies of this diversity remain scarce. In this article, we review current knowledge on the diversity and global distribution of ticks and tick-borne pathogens associated with seabirds. We discuss the relationship between seabirds, ticks, and their pathogens and examine the interesting characteristics of these relationships from ecological and epidemiological points of view. We also highlight some future research directions required to better understand the evolution of these systems and to assess the potential role of seabirds in the epidemiology of tick-borne pathogens.

Cryptic vector divergence masks vector-specific patterns of infection: an example from the marine cycle of Lyme borreliosis

Vector organisms are implicated in the transmission of close to a third of all infectious diseases. In many cases, multiple vectors (species or populations) can participate in transmission but may contribute differently to disease ecology and evolution. The presence of cryptic vector populations can be particularly problematic as differences in infection can be difficult to evaluate and may lead to erroneous evolutionary and epidemiological inferences. Here, we combine site‐occupancy modeling and molecular assays to evaluate patterns of infection in the marine cycle of Lyme borreliosis, involving colonial seabirds, the tick Ixodes uriae, and bacteria of the Borrelia burgdorferi s.l. complex. In this cycle, the tick vector consists of multiple, cryptic (phenotypically undistinguishable but genetically distinct) host races that are frequently found in sympatry. Our results show that bacterial detection varies strongly among tick races leading to vector‐specific biases if raw counts are used to calculate Borrelia prevalence. These differences are largely explained by differences in infection intensity among tick races. After accounting for detection probabilities, we found that overall prevalence in this system is higher than previously suspected and that certain vector–host combinations likely contribute more than others to the local dynamics and large‐scale dispersal of Borrelia spirochetes. These results highlight the importance of evaluating vector population structure and accounting for detection probability when trying to understand the evolutionary ecology of vector‐borne diseases.

Recent evolution of host‐associated divergence in the seabird tick Ixodes uriae

Ecological interactions are an important source of rapid evolutionary change and thus may generate a significant portion of novel biodiversity. Such changes may be particularly prevalent in parasites, where hosts can induce strong selection for adaptation. To understand the relative frequency at which host‐associated divergences occur, it is essential to examine the evolutionary history of the divergence process, particularly when it is occurring over large geographical scales where both geographical and host‐associated isolation may playa part. In this study, we use population genetics and phylogeography to study the evolutionary history of host‐associated divergence in the seabird tick Ixodes uriae (Acari, Ixodidae). We compare results from microsatellite markers that reflect more ecological timescales with a conserved mitochondrial gene (COIII) that reflects more ancient divergence events. Population structure based on microsatellites showed clear evidence of host‐associated divergence in all colonies examined. However, isolated populations of the same host type did not always group together in overall analyses and the genetic differentiation among sympatric host races was highly variable. In contrast, little host or geographical structure was found for the mitochondrial gene fragment. These results suggest that host race formation in I. uriae is a recent phenomenon, that it may have occurred several times and that local interactions are at different points in the divergence process. Rapid divergence in I. uriae implies a strong interaction with its local host species, an interaction that will alter the ecological dynamics of the system and modify the epidemiological landscape of circulating micropathogens.

Host races in Ixodes ricinus, the European vector of Lyme borreliosis

Ixodes ricinus is a European tick that transmits numerous pathogenic agents, including the bacteria that cause Lyme disease (some genospecies of Borrelia burgdorferi sensu lato complex). This tick has been considered as a classic example of an extreme generalist vector. However, host-associations in such vector species are difficult to determine from field observations alone and recent work suggests that host specificity may be more frequent in ticks than previously thought. The presence of host-associated vector groups can significantly alter the circulation and evolutionary pathway of associated pathogens. In this paper, we explicitly test for host-associated genetic structure in I. ricinus. We analyzed genetic variability at 11 microsatellite markers in a large sample of ticks collected directly from trapped wild animals (birds, rodents, lizards, wild boar and roe deer) at five sites in Western and Central Europe. We found significant levels of genetic structure both among host individuals and among host types within local populations, suggesting that host use is not random in I. ricinus. These results help explain previous patterns of structure found in off-host tick samples, along with epidemiological observations of Lyme disease.

Prevalence and diversity of Lyme borreliosis bacteria in marine birds.

A potential role of seabirds in spreading Lyme disease (LB) spirochetes over large spatial scales was suggested more than 10 years ago when Borrelia garinii was observed in marine birds of both hemispheres. Since then, there have been few studies examining the diversity of Borrelia spp. circulating in seabirds, or the potential interaction between terrestrial and marine disease cycles. To explore these aspects, we tested 402 Ixodes uriae ticks collected from five colonial seabird species by amplification of the flaB gene. Both the average prevalence (26.0%+/-3.9) and diversity of LB spirochetes was high. Phylogenetic analyses grouped marine isolates in two main clades: one associated with B. garinii and another with B. lusitaniae, a genospecies typically associated with lizards. One sequence also clustered most closely with B. burgdorferi sensu stricto. Prevalence in ticks varied both among seabird species within colonies and among colonies. However, there was no clear association between different Borrelia isolates and a given seabird host species. Our findings indicate that LB spirochetes circulating in the marine system are more diverse than previously described and support the hypothesis that seabirds may be an important component in the global epidemiology and evolution of Lyme disease. Future work should help determine the extent to which isolates are shared between marine and terrestrial systems.