Co-existence of hosts and sex ratio distorters in structured populations

Vertically transmitted parasites occur in several invertebrate species, and alter host reproduction by a variety of mechanisms, including sex ratio distortion via feminization. Efficient feminizers are predicted to drive homogenous host populations extinct due to the absence of males. However, group (interdemic) selection may enable host-parasite co-existence through extinction-colonization turnover of local subpopulations. Here we analyse the effects of feminizers on host metapopulations, in relation to the underlying mechanism of host sex determination. We examine host metapopulations with (a) fixed probabilistic sex ratio control, (b) female heterogamety (WZ/ZZ) and (c) male heterogamety (XX/XY) with and without YY viability. Under some circumstances, host and parasite can co-exist in metapopulations despite deterministic instability of local populations, in which case the parasite persists at lower frequency than predicted for homogenous populations. However, co-existence is sensitive to host sex determining mechanism. Long-term co-existence is unlikely in chromosomal systems, where sex ratio selection and novel mating type combinations result in the loss of female-determining alleles from infected host subpopulations. The consequent loss of uninfected females precludes stochastic parasite exclusion and thus prevents local population recovery. Hence, host-feminizer co-existence via interdemic selection requires intrinsic patch recovery in addition to recolonization from neighbouring subpopulations. We conclude that metapopulation structure can only buffer host populations against parasite-mediated extinction if female-determining alleles are retained in the host population.