Male-killing in the Coccinellidae: testing the predictions

Abstract

Male-killing endosymbionts have been widely reported in the invertebrates and are highly prevalent in the Coccinellidae. The presence of male-killers can lead to extreme bias in host population sex ratios and may have important and far-reaching consequences for the life-history and evolution of their hosts. Male-killers may have direct and indirect effects on host fitness and reproductive behaviour, as well as affecting the host genome, either via strong selection pressure imposed by highly female-biased population sex ratios or by selective sweeps caused as a male-killer conferring an advantage to infected individuals spreads through a population. Criteria used to predict which species are liable to male-killer invasion, based on a variety of ecological factors, have been produced. In summary male-killers are predicted to occur in aphidophageous species, that lay eggs in clutches, show sibling egg consumption and are liable to neonatal larval mortality due to starvation. We assayed 30 species of Coccinellid for the presence of such male-killers to assess the predictive accuracy of the criteria. Male-killers were identified in 8 species in which they were predicted to occur and were absent from all 10 species predicted not to harbor them. Analysis of the remaining 12 species, where male-killers were predicted by the original criteria, but where they were not found, allowed us to identify areas where the criteria can be refined and improved. We conclude that whilst the original criteria give a reasonably accurate prediction, there are refinements and improvements, concerning details of host diet and life-history, which make them more robust, especially in the light of discoveries of male-killing suppressors and when incorporated give a better fit to our findings from field samples. Michael E. N. Majerus-deceased. Electronic supplementary material The online version of this article (

Population genetics of the predatory lady beetle Hippodamia convergens

“…However, no male-killing bacteria have been reported from H. convergens (Majerus, 2006;Weeks et al, 2003). Still, (Majerus and Majerus, 2012) predicted their occurrence or invasion based on H. convergens' oviposition behavior of laying eggs in clusters, the risk of first instar starvation, and sibling egg cannibalism by neonates. Augmentative releases of overwintering adult H. convergens collected from the Sierra Nevada Mountains in California have been conducted for over a century (see description of practices in Hagen (1962)).…”

Unbalanced polyandry in wild-caught ladybirds Harmonia axyridis (Coleoptera: Coccinellidae)

“…The highly biased sex ratio toward females observed during the breeding season may be explained by infection of the population by male-killing bacteria (Majerus and Majerus 2012) and/or differential winter mortality (Galvan et al 2008). In the previous season, there were on average 46 % of males (range 36-52 %) recorded during the migration to the overwintering site in the same population.…”

Two Strains of Male-Killing Wolbachia in a Ladybird, Coccinella undecimpunctata, from a Hot Climate

“…All known agents of early male-killing are bacterial, with these agents being taxonomically diverse (including Rickettsia [3], Flavobacteria [4], Spiroplasma , [5], [6], Wolbachia [7] and γ-Proteobacteria [8]. The diversity of the agents associated with male-killing sets the male-killing strategy apart from the other ultra-selfish manipulations of host reproduction, most of which are caused by Wolbachia [9].…”

“…The potential for sibling egg cannibalism has imposed selection for embryos to develop and hatch rapidly [13]. As a result, neonate larvae are poorly resourced and show high mortality from starvation when they fail to find and subdue their first aphid prey [9]. In egg clutches laid by females infected with male-killing bacteria, male eggs fail to hatch and so are available to be eaten by infected female siblings, which thereby gain significant extra resources before they disperse to find aphid prey.…”