Preference for isolated host plants facilitates invasion of Danaus chrysippus (Linnaeus, 1758) (Lepidoptera: Nymphalidae) by a bacterial male-killer Spiroplasma

Matrilinearly inherited endosymbiotic bacteria are estimated to occur in a third of all terrestrial arthropods. They include male killers, which are typically associated with organisms that lay their eggs in batches. Batch laying favours male-killing bacteria because infected female larvae can cannibalise dead brothers and do not have to compete with them for larval resources. This paper tackles the paradox of high male-killer infection rates in Danaus chrysippus (Linnaeus, 1758), a butterfly that lays its eggs singly rather than in batches, making the selective advantage of male killing for the bacterium hard to understand. The study was conducted in the Nairobi region of Kenya where two substantially allopatric but seasonally migratory semispecies of Danaus chrysippus overlap and hybridise. Within this hybrid zone, but apparently not outside it, D. chrysippus hosts the endosymbiotic male killer, Spiroplasma ixodetis. In Nairobi, this bacterium can infect up to 95% of females. Semispecies D. chrysippus chrysippus and its hybrid with D. chrysippus dorippus (form transiens) are heavily infected, unlike the parental pure D. chrysippus dorippus semispecies, which may be protected by a suppressor gene. We find that: (1) adult females oviposit preferentially on isolated host plants; (2) female larvae on isolated plants survive better than on plants growing in clumps; (3) female larvae survive in greater numbers on plants removed to the laboratory compared to plants left outside; (4) high Spiroplasma infection favours female survival; and (5) high egg/larval density adversely affects adult body size. We conclude that: (1) the butterflies' preference for isolated host plants creates high egg densities and hence enables invasion by Spiroplasma; (2) male killing favours female survival through cannibalism of male eggs and the extra food-plant resources so released; and (3) the butterfly's preference for isolated host plants may provide an enemy-free space that protects eggs and larvae from predators and parasitoids.