The Genetic Basis for Salivary Gland Barriers to Arboviral Transmission

SIMPLE SUMMARY: Mosquito salivary glands are infected with an arbovirus prior to entering saliva. The virus in the mosquito’s saliva can then infect a vertebrate host when the vector acquires its next bloodmeal. Salivary gland infection and escape barriers (SGIB and SGEB, respectively) have been identified that modulate arbovirus transmission. SGIB are manifest as the absence of virus in the salivary glands of mosquitoes having a disseminated infection, while SGEB are evident as an absence of virus in the saliva of mosquitoes even though salivary glands are infected. The interaction between Aedes aegypti and viruses is dynamic and related to the genetic background of each vector population and virus variant. There is little understanding of the genetic basis for SGIB and SGEB. Here, nested, half-sib families of Aedes aegypti were used to estimate genetic and environmental variances, in which daughters from an individual dam differ in their phenotype due to the sire. We found that SGIB has a strong genetic basis with dengue virus infections but not with Zika or chikungunya virus infections, in which all salivary glands became infected. SGEB has a moderate genetic basis for Zika or chikungunya infections but not with dengue virus infections. ABSTRACT: Arthropod-borne viruses (arboviruses) infect mosquito salivary glands and then escape to saliva prior to virus transmission. Arbovirus transmission from mosquitoes can be modulated by salivary gland infection barriers (SGIBs) and salivary gland escape barriers (SGEBs). We determined the influence of SGIBs and SGEBs by estimating the quantitative genetic contributions of Aedes aegypti half-sib families (Mapastepec, Mexico) infected with three dengue 2 (DENV2), two chikungunya (CHIKV), and two Zika (ZIKV) genotypes. We determined virus titer per salivary gland and saliva at seven days post-infection and virus prevalence in the half-sib population. CHIKV or ZIKV genotypes did not present SGIB, whereas DENV2 genotypes showed low rates of SGIB. However, virus titer and prevalence due to additive genetic factors in the half-sib family displayed a significant narrow-sense heritability (h(2)) for SGIB in two of the three DENV2 genotypes and one CHIKV and one ZIKV genotype. SGEBs were detected in all seven virus strains: 60–88% of DENV2 and 48–62% of CHIKV or ZIKV genotype infections. SGEB h(2) was significant for all CHIKV or ZIKV genotypes but not for any of the DENV2 genotypes. SGIBs and SGEBs exhibited classical gene-by-gene interaction dynamics and are influenced by genetic factors in the mosquito and the virus.