Wolbachiastrengthens the match between pre-mating and early post-mating isolation in spider mites

Abstract

Endosymbiotic reproductive manipulators are widely studied as sources of post-zygotic isolation in arthropods, but their effect on pre-zygotic isolation between genetically differentiated populations has garnered less attention. We tested this using two partially isolated populations of the red and green colour forms ofTetranychus urticae, either uninfected or infected with aWolbachiastrain inducing or not cytoplasmic incompatibility. We first investigated male and female preferences, and found that, in absence of infection, females were not choosy but all males preferred red-form females.Wolbachiaeffects were more subtle, with only the CI-inducing strain slightly strengthening colour-form based preferences. We then performed a double-mating experiment to test how incompatible matings affect subsequent mating behaviour and offspring production, as compared to compatible mating. Females mated with an incompatible male (infected and/or heterotypic) were more attractive and/or receptive to subsequent (compatible) matings, although analyses of offspring production revealed no clear benefit for this remating behaviour (i.e., apparently unaltered first male sperm precedence). Finally, by computing the relative contributions of each reproductive barrier to total isolation, we showed that pre-mating isolation matches both host-associated andWolbachia-induced post-mating isolation, suggesting thatWolbachiacould assist speciation processes in this system.

Competition for food affects the strength of reproductive interference and its consequences for species coexistence

“…Many studies have investigated the strength of reproductive isolation between T. urticae and T. cinnabarinus [48][49][50]53,54 , but reproductive interference and its consequences for population dynamics have barely been considered (but see 53 ). Here, in absence of competition for food, we found asymmetric reproductive interference between T. cinnabarinus and T. urticae-, a result that is congruent with previous findings on pre-and post-mating reproductive isolation between the two populations used in this study 50,54 . This is also compatible with earlier studies using Chinese populations of these species, in which T. cinnabarinus consistently displaces T. urticae when at an even initial frequency 41,47 .…”

“…We used one population of T. urticae (‘Tu’) and one of T. cinnabarinus (‘Tc’), both free of any known endosymbiont (see details in Supplementary Box S1). Due to incomplete pre-zygotic isolation 54 and strong post-zygotic isolation 50 between these two populations, strong reproductive interference is expected when they share the same environment 43 . Indeed, females do not display any mate preference (non-assortative mating), whereas males of both species prefer to mate with Tc females 54 .…”

“…Due to incomplete pre-zygotic isolation 54 and strong post-zygotic isolation 50 between these two populations, strong reproductive interference is expected when they share the same environment 43 . Indeed, females do not display any mate preference (non-assortative mating), whereas males of both species prefer to mate with Tc females 54 . Moreover, sex ratio distortion occurs in heterospecific crosses between Tu females and Tc males (with an overproduction of haploid sons instead of hybrid daughters probably due to fertilization failure 50 ), and both directions of heterospecific cross result in fully sterile hybrids (most hybrid females do not lay eggs and the few eggs laid do not hatch) 50 .…”

“…First, to quantify how food competition affected the growth of both species in absence of reproductive interference (Experiment 1), focal females that had mated with conspecific males were exposed to increasing densities of conspecific and heterospecific competitors 68 , and their number of descendants was counted (Figure 5a). Spider mites have first-male sperm precedence 69 , hence females that have mated with conspecifics will drastically reduce their receptivity and not produce offspring from subsequent mates 54 . Second, to quantify the strength of reproductive interference while restricting competition for food (Experiment 2), we counted the number of offspring produced by females isolated on individual food patches after they interacted sexually with conspecific males only (control), or with both conspecific and heterospecific males.…”

Infection dynamics of endosymbionts that manipulate arthropod reproduction

“…The question of whether mate preferences have evolved in CI-infected hosts has usually been addressed from the host’s perspective: under CI, there should be selection on hosts to preferentially mate with compatible mates (i.e., infected males with infected females, and uninfected females with uninfected males). While theory suggests that such CI-avoiding mate preferences can indeed evolve (Champion de Crespigny et al ., 2005), empirical evidence is scarce (Champion de Crespigny & Wedell, 2007; Hoffmann et al ., 1990; Cruz et al, 2024; but see Vala et al ., 2004).…”