Genomic differentiation and intercontinental population structure of mosquito vectors Culex pipiens pipiens and Culex pipiens molestus

Abstract

Understanding the population structure and mechanisms of taxa diversification is important for organisms responsible for the transmission of human diseases. Two vectors of West Nile virus, Culex pipiens pipiens and Cx. p. molestus, exhibit epidemiologically important behavioral and physiological differences, but the whole-genome divergence between them was unexplored. The goal of this study is to better understand the level of genomic differentiation and population structures of Cx. p. pipiens and Cx. p. molestus from different continents. We sequenced and compared the whole genomes of 40 individual mosquitoes from two locations in Eurasia and two in North America. Principal Component, ADMIXTURE, and neighbor joining analyses of the nuclear genomes identified two major intercontinental, monophyletic clusters of Cx. p. pipiens and Cx. p. molestus. The level of genomic differentiation between the subspecies was uniform along chromosomes. The ADMIXTURE analysis determined signatures of admixture in Cx. p. pipens populations but not in Cx. p. molestus populations. Comparison of mitochondrial genomes among the specimens showed a paraphyletic origin of the major haplogroups between the subspecies but a monophyletic structure between the continents. Thus, our study identified that Cx. p. molestus and Cx. p. pipiens represent different evolutionary units with monophyletic origin that have undergone incipient ecological speciation. The advent of genomics has provided new insights into population divergence between incipient taxa, changing our vision about the mechanisms of adaptation and speciation 1. Experimental data demonstrate highly heterogenous patterns of population differentiation in various groups of organisms 2. In addition to the classical model of allopatric speciation, when incipient taxa are isolated geographically 3 , it becomes obvious that ecological speciation or the development of reproductive isolation between populations as a result of adaptation to different environments is feasible and common in nature 4-6. Understanding the population structure and the mechanisms of taxa diversification in the changing environment is extremely important if the studied organisms are related to the transmission of human diseases 7. Members of the Culex pipiens complex are globally distributed throughout Europe, Asia, America, Africa, and Australia and represent competent vectors of the lymphatic filariasis parasite and encephalitis viruses, including the widely spread West Nile virus 8-11. However, despite the fact that Cx. pipiens was the first mosquito species described by C. Linnaeus in his "Systema Naturae" 12 , mosquitoes from the Cx. pipiens complex still represent "one of the major outstanding problems in mosquito taxonomy" because the

Differential Gene Expression in the Heads of Behaviorally Divergent Culex pipiens Mosquitoes

“…Instead, there may be greater genetic variation in our AG populations relative to BG1, giving rise to more alternative splice sites. This is consistent with previous studies of genetic variation in these populations [30].…”

“…pipiens, collected from previously described above-ground form pipiens breeding and over-wintering sites and belowground form molestus breeding sites ( Table 1 and Table S1). Hereafter, we refer to these populations with respect to where they were collected rather than bioform nomenclature because it is known that gene flow can occur between the forms in North America [27,30]. We used a multi-day host choice assay to quantify the extent of variation in human and avian host preference among above-and below-ground Cx.…”

“…Form pipiens is thought to be predominately avian-seeking, while form molestus is thought to be mammalian-, and sometimes human-seeking [23][24][25]. In nature, the two forms can hybridize where populations come into contact with one another [26][27][28][29][30]. Molestus-pipiens F1 hybrids display indiscriminate feeding behaviors when tested in a laboratory setting, while progeny of F1s backcrossed to molestus or pipiens have host responses biased toward that of their non-hybrid parent, indicating a genetic basis for this trait [23].…”

The urban-adapted underground mosquito,Culex molestus, maintains exogenously influenced circadian rhythms despite an absence of photoperiodically induced dormancy

“…pipiens (e.g. Asgharian et al, 2015;Price and Fonseca, 2015;Aardema et al, 2020;Yurchenko et al, 2020). We first needed to determine which annotated Cx.…”

Autogenous and anautogenousCulex pipiensbioforms exhibit insulin-like peptide signaling pathway gene expression differences that are not dependent upon larval nutrition

“…The copyright holder for this preprint this version posted June 20, 2021. ; https://doi.org/10.1101/2021.06.20.449144 doi: bioRxiv preprint Kent et al, 2007;Yurchenko et al, 2020), the molecular mechanisms underlying their divergent reproductive strategies have not been identified.…”