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A Nicaraguan isolate of  Spodoptera frugiperda  multiple nucleopolyhedrovirus is being studied as a possible biological insecticide. This virus exists as a mixture of complete and deletion genotypes; the latter depend on the former for the production of an essential  per os  transmission factor ( pif1 ) in coinfected cells. We hypothesized that the virus population was structured to account for the prevalence of  pif1  defector genotypes, so that increasing the abundance of  pif1  produced by a cooperator genotype in infected cells would favor an increased prevalence of the defector genotype. We tested this hypothesis using recombinant viruses with  pif1  expression reprogrammed at its native locus using two exogenous promoters ( egt ,  p10 ) in the  pif2 / pif1  intergenic region. Reprogrammed viruses killed their hosts markedly faster than the wild-type and rescue viruses, possibly due to an earlier onset of systemic infection. Group success (transmission) depended on expression of  pif1 , but overexpression was prejudicial to group-specific transmissibility, both in terms of reduced pathogenicity and reduced production of virus progeny from each infected insect. The presence of  pif1 -overproducing genotypes in the population was predicted to favor a shift in the prevalence of defector genotypes lacking  pif1 -expressing capabilities, to compensate for the modification in  pif1  availability at the population level. As a result, defectors increased the overall pathogenicity of the virus population by diluting  pif1  produced by overexpressing genotypes. These results offer a new and unexpected perspective on cooperative behavior between viral genomes in response to the abundance of an essential public good that is detrimental in excess.

Expression of a Peroral Infection Factor Determines Pathogenicity and Population Structure in an Insect Virus