Genetic divergence between populations of feral and domestic forms of a mosquito disease vector assessed by transcriptomics

Abstract

Culex pipiens, an invasive mosquito and vector of West Nile virus in the US, has two morphologically indistinguishable forms that differ dramatically in behavior and physiology. Cx. pipiens form pipiens is primarily a bird-feeding temperate mosquito, while the sub-tropical Cx. pipiens form molestus thrives in sewers and feeds on mammals. Because the feral form can diapause during the cold winters but the domestic form cannot, the two Cx. pipiens forms are allopatric in northern Europe and, although viable, hybrids are rare. Cx. pipiens form molestus has spread across all inhabited continents and hybrids of the two forms are common in the US. Here we elucidate the genes and gene families with the greatest divergence rates between these phenotypically diverged mosquito populations, and discuss them in light of their potential biological and ecological effects. After generating and assembling novel transcriptome data for each population, we performed pairwise tests for nonsynonymous divergence (Ka) of homologous coding sequences and examined gene ontology terms that were statistically over-represented in those sequences with the greatest divergence rates. We identified genes involved in digestion (serine endopeptidases), innate immunity (fibrinogens and α-macroglobulins), hemostasis (D7 salivary proteins), olfaction (odorant binding proteins) and chitin binding (peritrophic matrix proteins). By examining molecular divergence between closely related yet phenotypically divergent forms of the same species, our results provide insights into the identity of rapidly-evolving genes between incipient species. Additionally, we found that families of signal transducers, ATP synthases and transcription regulators remained identical at the amino acid level, thus constituting conserved components of the Cx. pipiens proteome. We provide a reference with which to gauge the divergence reported in this analysis by performing a comparison of transcriptome sequences from conspecific (yet allopatric) populations of another member of the Cx. pipiens complex, Cx. quinquefasciatus.

Sex-specific gene expression in the mosquito Culex pipiens f. molestus in response to artificial light at night

“…The only other transcriptomic study of Cx. pipiens f. molestus to date found that the relationship between species was sufficiently close to obtain reliable mapping results [ 26 ]. Both species belong to the Cx.…”

Global evaluation of taxonomic relationships and admixture within the Culex pipiens complex of mosquitoes

“…As a supplement to publicly available data, we also sequenced the genomes of three additional Culex samples. One of these was a single adult female from a laboratory strain of molestus that derived from New York City, USA [43]. The second was an adult female pipiens, reared from a larva collected in an oviposition trap placed in a wooded area on the campus of Montclair State University in Passaic County, New Jersey, USA.…”

“…Among our pipiens and molestus samples, it is impossible to determine if many of the taxonomic designations are incorrect within the context of this study. Nonetheless, all eastern USA molestus samples were determined to be autogenic [43,53], as was the sample from Germany [41]. The molestus from the western USA and Russia were taxonomically assessed using molecular methods [42].…”

Olfaction, experience and neural mechanisms underlying mosquito host preference

“…A comparison of Cx. pipiens form pipiens and form molestus transcriptomes revealed that odorant-binding proteins were statistically overrepresented in the subset of genes with the highest divergence rates (Price and Fonseca, 2015). Thus, evolutionary changes to the olfactory periphery, even at the molecular level, can significantly impact host preference.…”

“…gambiae, has convergently evolved several ORs responsive to sulcatone (Carey et al, 2010), suggesting that host preference is driven by selection for OR profiles in the peripheral nervous system. To add to the complexity of peripheral nervous system 'players', the evolution of which can contribute to host-preference phenotypes, recent comparative proteomic and transcriptomic studies have revealed differences in the abundance of odorantbinding proteins of closely related mosquitoes with divergent host preferences (Rinker et al, 2013;Price and Fonseca, 2015;Iovinella et al, 2017). One example comes from comparisons of species in the An.…”