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. How virulent infectious diseases emerge from non-pathogenic organisms is a challenging question. Here, we address this evolutionary issue in the case of Q fever. Its causative agent, the intracellular bacterium Coxiella burnetii, is extremely infectious to humans and a variety of animals. However, uncertainty persists regarding its evolutionary origin, including the identity and lifestyle of its ancestors. In this article, we show that C. burnetii arose from a rare evolutionary transformation of a maternally-inherited endosymbiont of ticks into a specialized and virulent pathogen of vertebrates. While arthropod symbionts are typically transmitted maternally and thought not to be infectious to vertebrates, we establish here that one Coxiella symbiont has evolved the necessary adaptations to exploit the vertebrate cell, leading to the emergence of Q fever.

A growing body of evidence points towards epigenetic mechanisms being responsible for a wide range of biological phenomena, from the plasticity of plant growth and development to the nutritional control of caste determination in honeybees and the etiology of human disease (e.g., cancer). With the (partial) elucidation of the molecular basis of epigenetic variation and the heritability of certain of these changes, the field of evolutionary epigenetics is flourishing. Despite this, the role of epigenetics in shaping host–pathogen interactions has received comparatively little attention. Yet there is plenty of evidence supporting the implication of epigenetic mechanisms in the modulation of the biological interaction between hosts and pathogens. The phenotypic plasticity of many key parasite life-history traits appears to be under epigenetic control. Moreover, pathogen-induced effects in host phenotype may have transgenerational consequences, and the bases of these changes and their heritability probably have an epigenetic component. The significance of epigenetic modifications may, however, go beyond providing a mechanistic basis for host and pathogen plasticity. Epigenetic epidemiology has recently emerged as a promising area for future research on infectious diseases. In addition, the incorporation of epigenetic inheritance and epigenetic plasticity mechanisms to evolutionary models and empirical studies of host–pathogen interactions will provide new insights into the evolution and coevolution of these associations. Here, we review the evidence available for the role epigenetics on host–pathogen interactions, and the utility and versatility of the epigenetic technologies available that can be cross-applied to host–pathogen studies. We conclude with recommendations and directions for future research on the burgeoning field of epigenetics as applied to host–pathogen interactions.

The importance of sympatric speciation (the evolution of reproductive isolation between codistributed populations) in generating biodiversity is highly controversial. Whereas potential examples of sympatric speciation exist for plants, insects, and fishes, most theoretical models suggest that it requires conditions that are probably not common in nature, and only two possible cases have been described for tetrapods. One mechanism by which it could occur is through allochronic isolation—separation of populations by breeding time.Oceanodroma castro(the Madeiran or band-rumped storm-petrel) is a small seabird that nests on tropical and subtropical islands throughout the Atlantic and Pacific Oceans. In at least five archipelagos, different individuals breed on the same islands in different seasons. We compared variation in five microsatellite loci and the mitochondrial control region among 562O. castrofrom throughout the species' range. We found that sympatric seasonal populations differ genetically within all five archipelagos and have ceased to exchange genes in two. Population and gene trees all indicate that seasonal populations within four of the archipelagos are more closely related to each other than to populations from the same season from other archipelagos; divergence of the fifth sympatric pair is too ancient for reliable inference. Thus, seasonal populations appear to have arisen sympatrically at least four times. This is the first evidence for sympatric speciation by allochrony in a tetrapod, and adds to growing indications that population differentiation and speciation can occur without geographic barriers to gene flow.

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.

P. falciparumphenotypic plasticity is linked to the variant expression of clonal multigene families such as thevargenes. We have examined changes in transcription and histone modifications that occur during sporogonic development ofP. falciparumin the mosquito host. Allvargenes are silenced or transcribed at low levels in blood stages (gametocyte/ring) of the parasite in the human host. After infection of mosquitoes, a singlevargene is selected for expression in the oocyst, and transcription of this gene increases dramatically in the sporozoite. The same PF3D7_1255200vargene was activated in 4 different experimental infections. Transcription of thisvargene during parasite development in the mosquito correlates with the presence of low levels of H3K9me3 at the binding site for the PF3D7_1466400 AP2 transcription factor. This chromatin state in the sporozoite also correlates with the expression of an antisense long non-coding RNA (lncRNA) that has previously been shown to promotevargene transcription during the intraerythrocytic cyclein vitro. Expression of both the sense protein-coding transcript and the antisense lncRNA increase dramatically in sporozoites. The findings suggest a complex process for the activation of a single particularvargene that involves AP2 transcription factors and lncRNAs.