Why Antagonistic Traits against Cytoplasmic Incompatibility Are So Elusive

Intracellular symbionts are present in a wide variety of animals, plants and other life forms (Correa and Ballard, 2016); and have an intriguing lifestyle. To enhance their spread, intracellular symbionts have evolved a variety of mechanisms. Some of them provide benefits to their host and are effectively mutualists (e.g., Buchnera in aphids; Douglas, 1998), while others bias the sex ratio of the hosts’ offspring toward females (e.g., Wolbachia in many insects; Reuter et al., 2008; Werren et al., 2008; Zug and Hammerstein, 2015). In the latter, the mode of transmission is strictly maternal. Therefore, such symbionts induce their female hosts to produce higher numbers of daughters than the average number produced in the population (Reuter et al., 2008). A more indirect strategy impedes reproduction of uninfected females, where infected males that mate with uninfected females render the female sterile by cytoplasmic incompatibility (CI; Werren et al., 2008). CI is a type of conditional sterility independently evolved in two bacteria: Wolbachia (Alphaproteobacteria) and Cardinium (Bacteroidetes) that infect arthropod hosts (Penz et al., 2012; Santos-Garcia et al., 2014). CI occurs when a host gamete from an infected male fuses with the gamete of either an uninfected female or that of a female infected with a different strain typically resulting embryonic death (Tram and Sullivan, 2002; Werren et al., 2008; Correa and Ballard, 2016). As a consequence, the infection frequency increases in the population due to reduced fitness of uninfected females instead of any direct benefit to infected females (Champion de Crespigny et al., 2005). Such costs in fitness led many authors to speculate that antagonistic strategies could have evolved in the host against the symbiont (Turelli, 1994; Charlat et al., 2003; Vala et al., 2004; Crespigny and Wedell, 2007; Champion de Crespigny et al., 2008), although most of the studies have failed to confirm antagonisms that evolved exclusively in response to CI-phenotype (Vala et al., 2004; Crespigny and Wedell, 2007). Antagonistic strategies include any strategy against the CI-phenotype through either avoidance or resistance mechanisms. Moreover, when the evolution of such strategies was modeled, the results were varied; showing that evolution of CI-antagonism is conditional, for instance, it could depend on the frequency of CI in the population (see Champion de Crespigny et al., 2005, 2008). Therefore, it remains unclear whether the evolution of such strategies is possible. Hereby, I provide a conceptual framework taking in consideration that infection frequency affects the proportion of a population under selection for CI-antagonism; this may explain why CI-antagonistic traits have been so elusive.