From 1938 through the 1960s, an enigmatic, intraspecific incompatibility that caused embryonic death was reported between geographically isolated strains of Culex pipiens mosquitoes (Laven, 1951; Marshall, 1938), Aedes scutellaris mosquitoes (Smith-White and Woodhill, 1955), and Nasonia vitripennis parasitoid wasps (Ryan and Saul, 1968). Crossing experiments in both Culex and Nasonia surprisingly revealed that the incompatibility was caused by a maternally-inherited cytoplasmic factor (Laven, 1951; Ryan and Saul, 1968). This cytoplasmic incompatibility (CI) manifested as embryonic death when males carried the factor, but it was rescued if the female was from the same maternal lineage (Figure 1A). Intriguingly, Cu. pipiens (Laven, 1951) and N. vitripennis (Ryan and Saul, 1968) that had this cytoplasmic factor were either compatible, unidirectionally incompatible (Figure 1A,B), or bidirectionally incompatible (Figure 1C) with strains of different geographic origin. The underlying cause of these incompatibilities would remain a mystery for several decades.

Figure 1

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Motivated by the finding that Typhus is a Rickettsial disease (da Rocha-Lima, 1916), microbiologists Hertig and Wolbach conducted a survey of Rickettsia-like bacteria among numerous arthropod orders in and around Boston, Massachusetts in 1924 (Hertig and Wolbach, 1924). The bacteria were classified as Rickettsia-like based on size (often smaller than other bacteria), shape (cocciform or rod), Gram staining (gram-negative), and a Giemsa nucleotide stain (to separate microscopy artifacts from cells with DNA). In the Cu. pipiens mosquito, they found tiny rod-like or coccoid, gram-negative, Rickettsial bacteria residing within male and female reproductive cells (Hertig and Wolbach, 1924). The bacteria were absent in various other tissues including oesophageal diverticula, gut tissues, malphighian tubes, fat-body, heart and pericardial cells, salivary glands, and accessory reproductive organs (Hertig and Wolbach, 1924). Intriguingly, when Cu. pipiens with the bacteria were reared in the lab, offspring also harbored them in their reproductive tissues as early larva, suggesting that the bacteria were maternally inherited (Hertig and Wolbach, 1924). These bacteria would later be named Wolbachia pipientis by Dr. Marshall Hertig: Wolbachia for Dr. Simeon Burt Wolbach, Hertig’s PhD advisor, and pipientis for the mosquito it was discovered in Hertig, 1936. In this review, we will refer to the symbiont as Wolbachia since it currently remains a genus of only one recognized species.

In 1971, Yen and Barr investigated the effects of CI on embryonic development and discovered Rickettsia-like bacteria matching the description of Wolbachia in the eggs of symbiont-bearing Cu. pipiens females (Yen and Barr, 1971). This finding led them to the breakthrough hypothesis that CI is caused by these long-overlooked bacteria (Yen and Barr, 1971). They later tested this hypothesis using crosses with antibiotic-treated and untreated Cu. pipiens mosquitoes and determined that CI is a symbiont-derived phenotype caused by Wolbachia (Yen and Barr, 1973), thus substantiating Wolbachia as the etiological agent of CI phenotypes. This initial characterization of Wolbachia and CI in Cu. pipiens opened the floodgates, with many ensuing studies reporting cases of CI-inducing Wolbachia in Diptera (Baton et al., 2013; Bian et al., 2013; Hoffmann et al., 1986; Riegler and Stauffer, 2002), Hymenoptera (Betelman et al., 2017; Dittmer et al., 2016), Coleoptera (Kajtoch and Kotásková, 2018), Hemiptera (Ju et al., 2017; Ramírez-Puebla et al., 2016), Orthoptera (Martínez-Rodríguez and Bella, 2018), Lepidoptera (Arai et al., 2019; Hornett et al., 2008), Thysanoptera (Nguyen et al., 2017), Acari (Gotoh et al., 2007; Gotoh et al., 2003; Vala et al., 2002), Isopoda (Cordaux et al., 2012; Sicard et al., 2014), and Arachnids (Curry et al., 2015).

Among these orders, Wolbachia are highly diverse and phylogenetically divided into 17 ‘supergroups’ (denoted A-S, excluding G and R), and CI-inducing Wolbachia are so far restricted to supergroups A and B (Lefoulon et al., 2020; Lo et al., 2007; Wang et al., 2016). However, despite the considerable diversity between Wolbachia strains, the most studied models for CI are the Wolbachia of Culex (wPip), Drosophila (wRi and wMel), Nasonia (wVitA and wVitB), and Laodelphax (wStr). Aside from Wolbachia, the far less common (Weinert et al., 2015; Zchori-Fein and Perlman, 2004) Bacteroidetes bacteria Cardinium were found to cause CI nearly three decades later (Hunter et al., 2003; Yen and Barr, 1973). Additionally, unknown symbionts of Brontispa longissimi coconut beetles and Lariophagus distinguendus parasitoid wasps cause CI, but they are not Wolbachia or Cardinium (König et al., 2019; Takano et al., 2017). In addition, Gammaproteobacteria of the genus Rickettsiella cause CI in Mermessus fradeorum spiders (Rosenwald et al., 2020). This review will focus primarily on Wolbachia-induced CI, but other symbionts will be discussed when information is available.

CI has attracted considerable, applied interest in the last decade from scientists, companies, and governments because it is at forefront of efforts to reduce the spread of dengue, Zika, and other arboviral infections (Caragata et al., 2016; Crawford et al., 2020; Ford et al., 2019; Hoffmann et al., 2011; O'Connor et al., 2012; O'Neill, 2018; Rasgon, 2007; Rasgon, 2008; Teixeira et al., 2008; WHO, 2016; Xi et al., 2005). Two CI-based vector control strategies are deployed worldwide. First, the incompatible insect technique (IIT), also known as population suppression, aims to reduce the population size of disease vectors through release of CI-inducing male insects (Figure 2A; Ant et al., 2020; Caputo et al., 2020; Chambers et al., 2011; Crawford et al., 2020; Fresno, 2018; Kyritsis et al., 2019; Laven, 1967; Mains et al., 2019; Mains et al., 2016; O'Connor et al., 2012; Puggioli et al., 2016; Zheng et al., 2019a). Conversely, the population replacement strategy (PRS) does not reduce population sizes, but instead it aims to convert a native population that transmits arboviruses to humans with one that has reduced vectoral capacity (Figure 2B; Caragata et al., 2016; Hoffmann et al., 2011; Moreira et al., 2009; O'Neill, 2018; Tantowijoyo et al., 2020; Teixeira et al., 2008; van den Hurk et al., 2012). PRS uses two characteristics of CI-Wolbachia: the ability to rapidly spread through populations using CI and the ability of some strains to inhibit replication of arboviruses including dengue, Zika, chikungunya, and yellow fever (Caragata et al., 2016; Moreira et al., 2009; Teixeira et al., 2008; van den Hurk et al., 2012). When male and female mosquitoes bearing pathogen blocking Wolbachia are released to sufficiently high frequencies, CI drives them to frequencies approaching fixation that significantly alleviates the transmission of disease in the region. Both methods have been widely successful in their respective approaches (Crawford et al., 2020; Fresno, 2018; O'Neill et al., 2018; Tantowijoyo et al., 2020).

Figure 2

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In addition to combatting arthropod-borne diseases, CI has attracted interest from evolutionary biologists because it can cause reproductive isolation and thus be a contributor to speciation (Figure 2C). The Biological Species Concept defines groups of individuals as different species if they cannot interbreed (Dobzhansky, 1937; Mayr, 1963), and species emerge when reproductive isolation between two populations prevents gene flow (Coyne, 2001). Bidirectional and unidirectional CI can both reproductively isolate populations with different symbiont states, but to different degrees (Brucker and Bordenstein, 2012). Since bidirectional CI restricts gene flow in both cross directions, it can strongly reproductively isolate populations that harbor incompatible symbionts. This is indeed the case between Nasonia parasitoid wasps that diverged between ~0.25 and 1 million years ago (Bordenstein et al., 2001; Breeuwer and Werren, 1990). Alternatively, unidirectional CI restricts gene flow in one direction and does not appear to contribute to speciation in some host-Wolbachia symbioses such as in the D. yakuba clade (Cooper et al., 2017). However, North American populations of male symbiont-bearing D. recens cause unidirectional CI when mated with aposymbiotic D. subquinaria (Jaenike et al., 2006; Shoemaker et al., 1999), reducing gene flow between populations. Intriguingly, Cardinium yields similar patterns of asymmetric unidirectional CI between lab populations of Encarsia suzannae and its sister species E. gennaroi (Gebiola et al., 2017). Together, these studies suggest a role for symbiont-induced CI in reproductive isolation and incipient speciation.

In this review, we comprehensively synthesize the CI literature by discussing the rapid advances in understanding CI’s genetic basis, biochemical properties associated with CI, CI-associated abnormalities, CI strength variation, and host factors that correlate with CI expression. The reviewed works provide a concrete foundation for new testable and robust models, hypotheses, and evidence. Thus, we end with a description of the field’s models to explain the mechanistic underpinnings of CI and place them into the framework of current literature. Under these models, we identify key predictions and questions that motivate future areas of research to continue to build textbook knowledge on one of the most widespread selfish adaptations of symbionts.

It is common that researchers leverage correlations between Wolbachia symbiont state and host expression phenotypes (RNA, protein, etc.) to understand how Wolbachia impact their host. When differential expression is correlated with CI phenotypes, these data can yield valuable insights regarding CI’s mechanism. Significant correlations between Wolbachia symbiont state and host expression have been measured in D. melanogaster (Biwot et al., 2020; He et al., 2019; LePage et al., 2014; Liu et al., 2014; Ote et al., 2016; Xi et al., 2008; Yuan et al., 2015; Zheng et al., 2019b; Zheng et al., 2011), D. simulans (Brennan et al., 2012; Clark et al., 2006; Xi et al., 2008), La. striatellus (Huang et al., 2019; Ju et al., 2017; Liu et al., 2019), T. urticae (Bing et al., 2020a; Zhang et al., 2015), Cu. pipiens (Pinto et al., 2013), and A. albopictus (Baldridge et al., 2017; Baldridge et al., 2014; Brennan et al., 2012; Brennan et al., 2008). Challengingly, as many as 1613 transcripts are differentially expressed between Wolbachia symbiont states (Bing et al., 2020a), and as with the cytological abnormalities described above, it is difficult to untangle the effects of Wolbachia and CI on host expression profiles.

However, the most promising candidates associated with CI are those that can be experimentally over- or under-expressed to recapitulate CI-like hatch rates and cytological defects. For example, overexpression of the tumor suppressor gene lethal giant larvae [l(2)gl] and myosin II gene zipper in aposymbiotic D. simulans induces a considerable reduction in hatching that is accompanied with CI-associated cytological defects (Clark et al., 2006). However, CI is not just associated with hatch rate defects, but also the ability to rescue those defects. When l(2)gl and zipper over-expressing males were mated to symbiont-bearing females, no change in hatching was observed (Clark et al., 2006), suggesting that hatch rate reductions associated with these factors cannot be rescued and thus are not CI-associated. Nevertheless, there have been numerous studies that have identified host factors that contribute to CI-like embryonic abnormalities and can be rescued by symbiont-bearing females: the aminotransferase iLve which mediated branched-chain amino acid biosynthesis in La. striatellus (Ju et al., 2017), the sRNA nov-miR-12 which negatively regulates the DNA-binding protein pipsqueak (psq) in chromatin remodeling in D. melanogaster (Zheng et al., 2019b), cytosol amino-peptidase-like which are in the sperm acrosome and involved in fertilization in La. striatellus (Huang et al., 2019), two seminal fluid proteins (CG9334 and CG2668) with unknown function in D. melanogaster (Yuan et al., 2015), the histone chaperone Hira in D. melanogaster and D. simulans (Zheng et al., 2011), a Juvenile Hormone protein (JHI-26) involved in development in D. melanogaster (Liu et al., 2014), and the immunity-related gene kenny (key) in D. melanogaster (Biwot et al., 2020). Since misexpression of these host products in aposymbiotic males mimic CI-like embryonic defects in a way that can be rescued by symbiont-bearing females, there is support that these products or their pathways are involved in CI, but how these factors relate to cause CI remains unknown, and there is no current evidence that these are binding partners with Cif proteins.

In addition to RNA and/or protein expression differences, changes in host physiology and cell biology are correlated with CI. For example, Wolbachia-bearing D. melanogaster, D. simulans, A. albopictus, A. polynesiensis, and T. urticae males often have higher reactive oxygen species (ROS) in their testes than aposymbiotic males (Brennan et al., 2012; Brennan et al., 2008; Zug and Hammerstein, 2015). It has been hypothesized that this variation in ROS expression patterns is due to an elevated host immune response to Wolbachia symbiosis (Zug and Hammerstein, 2015). However, multiple lines of evidence link ROS expression with CI. For example, increased ROS levels are consistently observed among CI-inducing strains (Zug and Hammerstein, 2015), and ROS leads to DNA damage in spermatocytes in D. simulans (Brennan et al., 2012). Additionally, lipid hydroperoxide markers of ROS-induced oxidative damage are higher in symbiont-bearing D. melanogaster (Driver et al., 2004), and PCNA retention is another marker for DNA damage and is observed during the first mitosis of CI-affected embryos (Landmann et al., 2009). Interestingly, overexpression of the D. melanogaster gene key increases ROS levels and DNA damage in males when mimicking rescuable CI-like hatching and embryonic defects (Biwot et al., 2020). Together, these data support a role for ROS in CI’s mechanism, but direct connections remain unclear. One hypothesis is that CifA’s putative catalase-related domain does indeed function to interact with ROS (Lindsey et al., 2018). Though, alternatively, ROS may be a byproduct of the host immune response (Zug and Hammerstein, 2015). Biochemical and immunological assays will unravel these relationships.

Some Wolbachia strains exhibit CI that can vary between 10–100% embryonic death (Awrahman et al., 2014; Clark et al., 2003; Cooper et al., 2017; Hoffmann, 1988; Layton et al., 2019; Reynolds and Hoffmann, 2002; Turelli et al., 2018; Yamada et al., 2007; Zabalou et al., 2004). In fact, a number of Wolbachia, including wMel of D. melanogaster and wYak of D. yakuba, were initially characterized as non-parasitic since they had minimal to no impact on embryonic hatching (Charlat et al., 2004; Holden et al., 1993; Zabalou et al., 2004). Later studies would correct these early reports to suggest they can indeed cause CI, but their CI strength is highly dependent on a variety of factors including the age of fathers and grandmothers (Cooper et al., 2017; Layton et al., 2019; Reynolds and Hoffmann, 2002). Generally speaking, the work reviewed below describes a complex relationship between biotic and abiotic factors that influence CI strength. Notably, the bacterial density model of CI, whereby Wolbachia densities positively correlate with CI strength, is likely the major factor driving most of these relationships (Breeuwer and Werren, 1993). Phage WO lysis, host suppressors, and other undescribed interactors may control the variation in Wolbachia titers (Figure 6; Awrahman et al., 2014; Bordenstein and Bordenstein, 2011; Funkhouser-Jones et al., 2018; Layton et al., 2019; Poinsot et al., 1998; Walker et al., 2011). However, there are instances where CI strength variation does not correlate with Wolbachia densities (Yamada et al., 2007). Below, we review these works and describe what is known and unknown about the proximal basis of CI strength variation.

Figure 6

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Numerous models have been proposed to explain CI and rescue mechanisms. First, we discuss the utility of the classical phenotype-based modification/rescue (mod/resc) model in a post-genomic world (Shropshire and Bordenstein, 2019; Werren, 1997). Additionally, despite considerable advances in the genetics and biochemistry of CI, numerous mechanistic models are used to describe CI and rescue (Beckmann et al., 2019a; Poinsot et al., 2003; Shropshire et al., 2019). These models divide into two discrete categories: host-modification (HM) (Figure 7A) and toxin-antidote (TA) (Figure 7B; Beckmann et al., 2019a; Shropshire et al., 2019). HM-based models assume that the CI-inducing factors act directly to modify host male products and that rescue occurs through either removal of these modifications or otherwise reversing the effects through a separate host-modification in the female. TA-based models assume that the CI-inducing factors are transported into the embryo via the sperm and are toxic after fertilization unless the rescue factor is present, binds to the CI toxin, and inhibits its toxicity. We discuss each of these models and their variants in the context of a Two-by-One genetic framework (Shropshire and Bordenstein, 2019), but it is crucial to reemphasize that while both CifA and CifB proteins are required to induce CI, the specific biochemical mechanism underlying each protein’s contribution to CI and rescue remains unknown and there remains insufficient data to confirm any of these models.

Figure 7

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HM-based mechanistic models

HM models (Figure 7A) make at least two key predictions. First, male host products are modified by Cifs (Shropshire et al., 2019). There are numerous, pre-fertilization defects associated with CI-inducing Wolbachia including changes in sperm morphology and competitive ability (Champion de Crespigny and Wedell, 2006; Riparbelli et al., 2007), supporting that the host is modified prior to fertilization. It is unknown, however, whether these outcomes are due to pre-fertilization defects causally related to CI or general responses to Wolbachia in the testes. Second, and most crucially, the proximal CI modifications causing death of the fertilized embryo is rescued (e.g., replaced or otherwise negated) by CifA in the embryo (Shropshire et al., 2018; Shropshire and Bordenstein, 2019). CifA does not rescue through binding with male-transferred CifB products since Cif protein yields the modification prior to fertilization in testes and thus does not need to be transfered with the sperm to the embryo. Instead, CifA may interact with host processes to reverse or otherwise stop the effects of CI caused by CifA and CifB protein expression in males. As such, assessment of the location of CifA and CifB binding (testes or embryo), the transfer of Cif products, if any, with the sperm, and the interactions that Cif have with the host will further inform this model. We discuss three additional non-exclusive HM-based models below: titration-restitution, mistiming, and goalkeeper.

The titration-restitution model (a.k.a. the ‘sink’ hypothesis) was originally proposed by Werren, 1997 and posits that CI is induced by over- or under-expression of host products or pathways in the testes/sperm and rescue occurs when the same products are misregulated in the opposite direction in the ovaries/embryo (Figure 8A; Kose and Karr, 1995; Poinsot et al., 2003; Werren, 1997). Indeed, Wolbachia have a considerable impact on expression profiles, some host genes are differentially expressed in male and female reproductive tissues, and numerous host factors meet these criteria (Baldridge et al., 2017; Baldridge et al., 2014; Bing et al., 2020a; Yuan et al., 2015), as described in the section above. There are at least two ways in which CifA and CifB proteins can underpin the titration-restitution model. First, since CI and rescue would occur through titration of the same host product or pathway, it is feasible that CifA, which acts on both sides of the phenotype (Shropshire and Bordenstein, 2019), may drive these expression changes. Under such a model, CifB may act as an ‘accessory protein’ that enables CifA to target a paternally derived product that it would otherwise not be able to reach on its own. Second, CifA may act on its own to up- or down-regulate host products but has the opposite impact on that product when CifB is present. As such, rescue would occur through CifA’s lone action which counteracts the misregulation caused by CifA and CifB dual expression.

Figure 8

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Notably, titration-restitution models can explain bidirectional CI if Cif products from different strains have variable impacts on multiple host expression pathways. Thus, rescue would not be possible from a second strain since it could be targeting the wrong host factor or pathway. Indeed, divergent CI genes may differentially impact host pathways. For example, only the CifB_[T1] sequences maintain a functional Ulp1 domain while the other four CifB clades have a dimer of PDDEXK nucleases that is also present in CifB_[T1] (Beckmann et al., 2017; Bing et al., 2020b; Lindsey et al., 2018; Martinez et al., 2020). It is feasible that CifB with different domains impact different host pathways. Alternatively, Cif proteins may have differential impacts on the level of misregulation instead of or in addition to impacting multiple host pathways which may influence incompatibility relationships. More work will be necessary to understand if cif expression influences transcriptional and translational variation and how that variation corresponds to CI.

The mistiming model (a.k.a. the ‘slow motion’ hypothesis) was first explicitly proposed by Tram and Sullivan, 2002 and is based on the observation that the paternal pronucleus has slowed development relative to the female pronucleus in CI crosses, the rescue cross has normal cell cycle timing, and the female pronucleus continues development despite the slowdown in both Drosophila and Nasonia species (Figure 8B; Callaini et al., 1996; Ferree and Sullivan, 2006; Ryan and Saul, 1968; Tram and Sullivan, 2002). This established the hypotheses that delayed male pronuclear development is responsible for emergent defects in early embryogenesis, and that resynchronization of the development may occur by comparably slowing down the development of the female pronucleus or slowing the cell cycle in rescue. Since the cell cycle timing of the female pronucleus is what establishes the timing for the first mitosis (Bossan et al., 2011), symbiont-bearing females do not induce CI because the male pronucleus reach apposition prior to the female pronucleus. Though, the reciprocal cross would be incompatible because the female pronucleus finished development prior to the male, and the first mitosis would have initiated before the male pronucleus arrives. Importantly, this model predicts that CI crosses are subject to haploidization of diploid offspring since the male pronucleus could be completely excluded from mitosis if it was significantly slowed. This is indeed the case in N. vitripennis where CI often manifests as only male offspring since haploid offspring are viable in this species but develop as males (Bordenstein et al., 2003).

The mistiming model proposes that CI and rescue have comparable impacts on the development of male and female gametes, respectively. As such, a single gene could in theory be responsible for both CI and rescue (Poinsot et al., 2003). Under this paradigm, CifA may enact a slowdown in both tissues since it is involved in both phenotypes (Shropshire and Bordenstein, 2019). However, if this were the case, then what would be the purpose of CifB? It is possible that CifB is responsible for localizing CifA to a male-specific target where it imposes the same outcomes on its host. Since this hypothetical male product would not be available in the embryo, CifB would not have a role in rescue. However, an alternative model for mistiming is that rescue may not occur through slowing down the female pronucleus but may instead work by removing the slowdown agents from the male pronucleus. Together, these models would help to explain the proximal cause (misregulation) and culminating effects (mistiming) of CI. More work will be necessary to understand if rescue occurs via slowdown of the female pronucleus or from speeding-up the male pronucleus.

A major limitation of the mistiming model is that it cannot explain bidirectional CI. Since mistiming proposes that rescue happens through delaying the female pronucleus as much as or greater than the male pronucleus, a sufficiently strong delay should yield compatibility with any strain that has a weaker male delay. As such, only unidirectional CI should manifest between strains where the strain inducing the stronger delay is capable of rescue. The goalkeeper model was proposed in 2011 as a way to address this limitation (Figure 8C; Bossan et al., 2011). In addition to the expectations of the mistiming model, goalkeeper suggests that a secondary factor unassociated with this mistiming may also be involved in CI. The combined contributions of these two mod factors leads to CI. Under this paradigm, CifA and CifB may contribute to different kinds of defects during spermatogenesis, each contributing in somewhat independent ways to CI. Rescue must then negate the impacts of both factors. Thus for CifA to rescue CI, it would not only need to contribute to a delay in the pronuclear development but also reverse the impacts of a secondary source of modification. Notably, since the titration-restitution model does not make predictions about the developmental timing of the male and female pronuclei, it is compatible with both mistiming and goalkeeper models and can help explain mistiming through misregulation of host factors in a manner that leads to slowed development. More functional genetic, biochemical, and cytological studies are necessary to understand how a goalkeeper model and/or a combination of these HM-based models may contribute to CI.

Wolbachia were first discovered in Cu. pipiens mosquitoes in 1924 and later linked to CI in 1973 (Hertig and Wolbach, 1924; Yen and Barr, 1973). Since then, advances have significantly expanded our recognition of Wolbachia’s incredible and complex toolset. In particular, biologists now appreciate CI as a common form of reproductive parasitism that symbionts, including Wolbachia and Cardinium, use to rapidly spread through populations (Hunter et al., 2003; Rosenwald et al., 2020; Takano et al., 2017; Turelli, 1994; Weinert et al., 2015; Zug and Hammerstein, 2012). CI is associated with reproductive isolation (Bordenstein et al., 2001; Gebiola et al., 2017; Jaenike et al., 2006) and is leveraged as a successful tool in the prevention of arboviral diseases that infect humans (Crawford et al., 2020; O'Neill, 2018; Tantowijoyo et al., 2020). The last decade has seen a rapid expansion in our understanding of phage WO’s role in CI genetics (Beckmann et al., 2019c; Chen et al., 2019; LePage et al., 2017; Shropshire et al., 2018; Shropshire and Bordenstein, 2019), phylogenetics (Bing et al., 2020b; LePage et al., 2017; Lindsey et al., 2018; Martinez et al., 2020), and mechanism (Beckmann et al., 2019c; Beckmann et al., 2017; Chen et al., 2019; Shropshire et al., 2020). Moreover, considerable effort has been made to describe CI-defining cytological defects (Ferree and Sullivan, 2006; Landmann et al., 2009), link variation in host expression with CI phenotypes (Biwot et al., 2020; Liu et al., 2014; Zheng et al., 2011), and untangle factors that influence CI strength such as Wolbachia densities and phage WO lytic activity (Bordenstein and Bordenstein, 2011; Layton et al., 2019; Reynolds and Hoffmann, 2002; Yamada et al., 2007). Together, this significant body of literature has motivated models to explain how CI works (Beckmann et al., 2019a; Bossan et al., 2011; Poinsot et al., 2003; Shropshire et al., 2019). These studies have stone-by-stone erected a steady foundation that will serve as a launching point for exciting new discoveries to fully appreciate the complexity of this powerful form of reproductive manipulation. Looking forward, key areas of investigation will involve the relative roles of CifA and CifB in the induction of CI, the cell biology of the Cif proteins, the genetic basis of bidirectional CI, the cytogenetic basis of CI strength variation, linkage of Cif expression with cytological abnormalities pre- and post-fertilization, Cif-induced CI’s molecular and biochemical basis, and mechanisms of host suppression of CI.

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Author details

1. J Dylan Shropshire

   1. Department of Biological Sciences, Vanderbilt University, Nashville, United States
   2. Vanderbilt Microbiome Initiative, Vanderbilt University, Nashville, United States

   For correspondence

   shropxp@gmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4221-2178

2. Brittany Leigh

   1. Department of Biological Sciences, Vanderbilt University, Nashville, United States
   2. Vanderbilt Microbiome Initiative, Vanderbilt University, Nashville, United States

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5668-9925

3. Seth R Bordenstein

   1. Department of Biological Sciences, Vanderbilt University, Nashville, United States
   2. Vanderbilt Microbiome Initiative, Vanderbilt University, Nashville, United States
   3. Department of Pathology, Microbiology, and Immunology, Vanderbilt University, Nashville, United States
   4. Vanderbilt Institute for Infection, Immunology, and Inflammation, Vanderbilt University Medical Center, Nashville, United States

   For correspondence

   s.bordenstein@vanderbilt.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7346-0954

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