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Cytoplasmic Incompatibility (CI) causes embryonic lethality in arthropods, resulting in a significant reduction in reproductive success. In most cases, this reproductive failure is driven by Wolbachia endosymbionts through their cifA - cifB gene pair, whose products disrupts arthropod DNA replication during embryogenesis. While a cif pair has been considered a hallmark of Wolbachia , its presence and functional significance in other bacterial lineages remains poorly investigated. Here, we conducted a comprehensive survey of 762 genomes spanning non- Wolbachia endosymbionts and their close relatives, revealing that the cif pair is far more widespread than previously recognized. We identified cif loci in 8.4% of the surveyed genomes, with a striking incidence of 17.4% in facultative symbionts. Beyond Wolbachia , cif pair occurs across eight bacterial genera spanning α-Proteobacteria, γ-Proteobacteria, Mollicutes, and Bacteroidota. Notably, cif pair has been identified in several intracellular pathogens of mammals showing high rate of transovarial transmission in their arthropod hosts, suggesting a potential role of cif pair and CI in vector-borne disease dynamics. Structural analyses further reveal that the PD(D/E)-XK nucleases and AAA-ATPase-like motifs are consistently conserved across cif pairs in all bacterial taxa. Moreover, cif pairs are frequently integrated within diverse mobile genetic elements, from transposons to large intact WO prophages in Wolbachia and RAGEs in Rickettsiaceae. Phylogenetic analyses reveal recent and potentially ongoing horizontal transfers of cif pair between distantly related bacterial lineages, a process potentially facilitated by mobile genetic elements. Indeed, the PDDEXK2 transposase exhibits a phylogenetic pattern consistent with the co-transmission of cif genes, suggesting that it may facilitate horizontal transfers of cif across bacterial lineages. Furthermore, the detection of endosymbionts harboring cif pair in arthropod groups where Wolbachia is scarce, such as ticks, suggests that CI may be more widespread than previously known, with significant implications for arthropod symbiosis, reproductive manipulation, and future biocontrol strategies.

In the last decade, the Chikungunya and Zika virus outbreaks have turned public attention to the possibility of the expansion of vector-borne infectious diseases worldwide. Medical entomology is focused on the study of arthropods involved in human health. We review here some of the research approaches taken by the medical entomology team of the University Hospital Institute (UHI) Méditerranée Infection of Marseille, France, with the support of recent or representative studies. We propose our approaches to technical innovations in arthropod identification and the detection of microorganisms in arthropods, the use of arthropods as epidemiological or diagnostic tools, entomological investigations around clinical cases or within specific populations, and how we have developed experimental models to decipher the interactions between arthropods, microorganisms, and humans.

The impact of the microbiota on the immune status of its host is a source of intense research and publicity. In comparison, the effect of arthropod microbiota on vector-borne infectious diseases has received little attention. A better understanding of the vector microbiota in relation to mammalian host immune responses is vital, as it can lead to strategies that affect transmission and improve vaccine design in a field of research where few vaccines exist and effective treatment is rare. Recent demonstrations of how microbiota decrease pathogen development in arthropods, and thus alter vector permissiveness to vector-borne diseases (VBDs), have led to renewed interest. However, hypotheses on the interactions between the arthropod-derived microbiota and the mammalian hosts have yet to be addressed. Advances in DNA sequencing technology, increased yield and falling costs, mean that these studies are now feasible for many microbiologists and entomologists. Here, we distill current knowledge and put forward key questions and experimental designs to shed light on this burgeoning research topic.

Wolbachia are intracellular bacteria that manipulate the reproduction of their arthropod hosts in remarkable ways. They are predominantly transmitted vertically from mother to offspring but also occasionally horizontally between species. In doing so, they infect a huge range of arthropod species worldwide. Recently, a statistical analysis estimated the infection frequency of Wolbachia among arthropod hosts to be 66%. At the same time, the authors of this analysis highlighted some weaknesses of the underlying data and concluded that in order to improve the estimate, a larger number of individuals per species should be assayed and species be chosen more randomly. Here we apply the statistical approach to a more appropriate data set from a recent survey that tested both a broad range of species and a sufficient number of individuals per species. Indeed, we find a substantially different infection frequency: We now estimate the proportion of Wolbachia-infected species to be around 40% which is lower than the previous estimate but still points to a surprisingly high number of arthropods harboring the bacteria. Notwithstanding this difference, we confirm the previous result that, within a given species, typically most or only a few individuals are infected. Moreover, we extend our analysis to include several reproductive parasites other than Wolbachia that were also screened for in the aforementioned empirical survey. For these symbionts we find a large variation in estimated infection frequencies and corroborate the finding that Wolbachia are the most abundant endosymbionts among arthropod species.

Key Points This Review focuses on intracellular Wolbachia , which are globally widespread Rickettsia -like bacteria that infect many arthropod species, as well as filarial nematodes. The authors discuss recent advances in Wolbachia research, with an emphasis on genetics and genomics, ecology, evolution and applications to pest and disease control. Wolbachia are primarily reproductive parasites that have several different effects on hosts, including feminization, induced parthenogenesis, male killing and a sperm–egg incompatibility that is known as cytoplasmic incompatibility. Wolbachia can effectively manipulate the biology of host cells, and have evolved mutualisms with their hosts. These and other effects of Wolbachia are discussed, as well as recent advances on the understanding of cytological interactions between bacteria and their host. Maintenance of the global Wolbachia pandemic is discussed, including factors that affect the spread of Wolbachia , transfer between host species and persistence within a host lineage. The usefulness of multilocus strain typing to characterize the movement and diversity of these bacteria is also emphasized. The evolutionary implications of Wolbachia infection are discussed, including the possible role of this endosymbiont in the promotion of reproductive isolation and speciation, as well as its potential to contribute to host genome evolution through horizontal transfer of genes from the bacteria into their host. Finally, the authors outline possible practical applications of Wolbachia in pest and disease vector management strategies and highlight the main unanswered questions regarding Wolbachia biology. Wolbachia are symbiotic bacteria that live inside invertebrate host cells and can manipulate host biology in dramatic ways, such as sperm–egg incompatibility, feminization and male killing. This Review focuses on the basic biology of these symbionts and their interaction with a range of host invertebrates. Wolbachia are common intracellular bacteria that are found in arthropods and nematodes. These alphaproteobacteria endosymbionts are transmitted vertically through host eggs and alter host biology in diverse ways, including the induction of reproductive manipulations, such as feminization, parthenogenesis, male killing and sperm–egg incompatibility. They can also move horizontally across species boundaries, resulting in a widespread and global distribution in diverse invertebrate hosts. Here, we review the basic biology of Wolbachia , with emphasis on recent advances in our understanding of these fascinating endosymbionts.

Microorganisms that reside within or transmit through arthropod reproductive tissues have profound impacts on host reproduction, health and evolution. In this Review, we discuss select principles of the biology of microorganisms in arthropod reproductive tissues, including bacteria, viruses, protists and fungi. We review models of specific symbionts, routes of transmission, and the physiological and evolutionary outcomes for both hosts and microorganisms. We also identify areas in need of continuing research, to answer the fundamental questions that remain in fields within and beyond arthropod–microorganism associations. New opportunities for research in this area will drive a broader understanding of major concepts as well as the biodiversity, mechanisms and translational applications of microorganisms that interact with host reproductive tissues.In this Review, Perlmutter and Bordenstein discuss our current knowledge of microbial symbionts that inhabit or transmit through the reproductive tissues of arthropods, their modes of transmission, and the physiological and evolutionary outcomes of their symbiotic relationships.

Animal hosts have initiated myriad symbiotic associations with microorganisms and often have maintained these symbioses for millions of years, spanning drastic changes in ecological conditions and lifestyles. The establishment and persistence of these relationships require genetic innovations on the parts of both symbionts and hosts. The nature of symbiont innovations depends on their genetic population structure, categorized here as open, closed or mixed. These categories reflect modes of inter-host transmission that result in distinct genomic features, or genomic syndromes, in symbionts. Although less studied, hosts also innovate in order to preserve and control symbiotic partnerships. New capabilities to sequence host-associated microbial communities and to experimentally manipulate both hosts and symbionts are providing unprecedented insights into how genetic innovations arise under different symbiont population structures and how these innovations function to support symbiotic relationships.The evolutionary persistence of animal symbioses depends on both host and symbiont innovations. Perreau and Moran review how genome sequencing and related experiments have clarified how these innovations arise under different symbiont population structures, categorized here as open, closed and mixed.

Extracellular vesicles are thought to facilitate pathogen transmission from arthropods to humans and other animals. Here, we reveal that pathogen spreading from arthropods to the mammalian host is multifaceted. Extracellular vesicles from Ixodes scapularis enable tick feeding and promote infection of the mildly virulent rickettsial agent Anaplasma phagocytophilum through the SNARE proteins Vamp33 and Synaptobrevin 2 and dendritic epidermal T cells. However, extracellular vesicles from the tick Dermacentor andersoni mitigate microbial spreading caused by the lethal pathogen Francisella tularensis . Collectively, we establish that tick extracellular vesicles foster distinct outcomes of bacterial infection and assist in vector feeding by acting on skin immunity. Thus, the biology of arthropods should be taken into consideration when developing strategies to control vector-borne diseases. Extracellular vesicles have been implicated in the transmission of pathogens from the arthropod to the human host. Here the authors show that tick-derived extracellular vesicles play a role in feeding and modulate the outcome of bacterial infection.

Intracellular endosymbiotic bacteria are found in many terrestrial arthropods and have a profound influence on host biology. A basic question about these symbionts is why they infect the hosts that they do, but estimating symbiont incidence (the proportion of potential host species that are actually infected) is complicated by dynamic or low prevalence infections. We develop a maximum-likelihood approach to estimating incidence, and testing hypotheses about its variation. We apply our method to a database of screens for bacterial symbionts, containing more than 3600 distinct arthropod species and more than 150 000 individual arthropods. After accounting for sampling bias, we estimate that 52% (CIs: 48–57) of arthropod species are infected with Wolbachia, 24% (CIs: 20–42) with Rickettsia and 13% (CIs: 13–55) with Cardinium. We then show that these differences stem from the significantly reduced incidence of Rickettsia and Cardinium in most hexapod orders, which might be explained by evolutionary differences in the arthropod immune response. Finally, we test the prediction that symbiont incidence should be higher in speciose host clades. But while some groups do show a trend for more infection in species-rich families, the correlations are generally weak and inconsistent. These results argue against a major role for parasitic symbionts in driving arthropod diversification.

ABSTRACT Symbiosis between intracellular bacteria (endosymbionts) and animals are widespread. The alphaproteobacterium Wolbachia pipientis is known to maintain a variety of symbiotic associations, ranging from mutualism to parasitism, with a wide range of invertebrates. Wolbachia infection might deeply affect host fitness (e.g. reproductive manipulation and antiviral protection), which is thought to explain its high prevalence in nature. Bacterial loads significantly influence both the infection dynamics and the extent of bacteria-induced host phenotypes. Hence, fine regulation of bacterial titers is considered as a milestone in host-endosymbiont interplay. Here, we review both environmental and biological factors modulating Wolbachia titers in arthropods. Extrinsic and intrinsic factors shaping titers of the endosymbiotic bacterium Wolbachia pipientis in arthropods.