Hybrid speciation in the Culex pipiens mosquito complex?

Mosquitoes are infamous for the challenges they present biologists attempting to classify distinct taxonomic groups. In a recent article, researchers try to answer some challenging questions on the taxonomy of the Culex pipiens species complex.

从历史上看,使用形态学特点tics created many instances where single ‘species’ were described as having broad ecological and behavioral variation, including variation in host preferences.

With the advent of molecular tools for surveying mosquito diversity, it has become clear that much of the ecological and behavioral diversity observed within mosquito species correlates with multiple, distinct genetic units.

Accurate cataloguing of variation in relation to taxonomic diversity is scientifically vital as it can facilitate a better understanding of enzootic cycles and disease transmission to humans or domesticated animals. For this reason, it is also equally important to understand the evolutionary processes that create and shape mosquito taxonomic diversity.

One group of mosquitoes with challenging taxonomic designations are those in theCulex pipiensspecies complex.

Currently, most researchers consider there to be six distinct taxa within this complex although what each of these taxa represents is of greater contention. Here I will treat them as discrete species for simplicity.

These taxa include the cosmopolitan Northern (Cx. pipiens) and Southern (Cx. quinquefasciatus) House Mosquitoes, the urban adapted ‘London Underground Mosquito’ (Cx. molestus), a Northeast Asian endemic taxon,Cx. pallens, and two Australian endemic taxa,Cx. australicus and Cx. globocoxitus. The mosquitoes within this complex are major vectors of West Nile virus and St. Louis encephalitis, among other pathogenic organisms.

Recently, my colleagues and I used publicly available next-generation sequencing data taken from twelve different studies to examine for the first time the genetic relationships among allsix members of the complex across their global distribution. In this study, we asked three specific questions:

1) How do the Australia endemic species relate to the other members of the complex?

2) Is the urban-adapted taxonCx. molestusmonophyletic?

3) Is the taxonCx. pallensa distinct evolutionary entity or rather does it arise from contemporary hybridization between other complex members?

These world maps show the collection locations of samples (small circles inside gray boxes) and the relative genetic ancestry proportions of three (a) or five (b) inferred populations (referred to as ‘K’ values). Each sample’s taxonomic designation was based on that reported in the literature. The proportion of each color in the large circles corresponds to the amount of taxon-associated genetic ancestry. Note the consistent combination of Cx. quinquefasciatus and Cx. pipiens genetic ancestry in the Cx. pallens samples from China the upper map (a; K=3), and the unique genetic ancestry of Cx. pallens from China in the lower map (b; K=5) (Aardema et al. 2020).

Using a combination of genetic clustering and phylogenetic analyses, we found clear evidence that the two Australian endemic taxa belong within the complex and most likely diverged fromCx. quinquefasciatusafter the split between it andCx. pipiens.

Our results also indicated thatCx. molestusfrom North America and from Europe are genetically distinct, and may have separate evolutionary origins. This result suggests that urban environments may have selected for themolestus-form in multiple locations independently and therefore thatmolestusispolyphyletic.

This finding contrasts withprevious workthat indicatedCx.molestushas just a single origin. However, our results also showed extensive genetic exchange among all members of the complex, and correspondingly the genetic signatures of evolutionary origins are obscured in these interbreeding populations.

Lastly, and perhaps most interestingly, we found that the taxonCx. pallensharbors a distinct genetic signature across a broad geographic area in Northern China that reveals its hybrid origins. Samples showed a consistent ancestry that was comprised of approximately 70%Cx. quinquefasciatusgenetic background and 30% of eitherCx. pipiensorCx. molestusgenetic background.

The close genetic similarity ofCx. pipiensandCx. molestusmade it impossible to differentiate which was the more likely parental taxon with theCx. pallensdata available to us. In addition to a consistent signature of genetic admixture, theCx. pallenssamples examined also had numerous genetic variants not seen in any of the other taxa, suggesting that contemporarily it is a distinct evolutionary entity.

The possibility that new and distinct taxa can arise through hybridization remains contentious, although evidence is increasingly revealing that it can occur and form new,reproductively isolated species.

Although very suggestive, our data is presently insufficient to state thatCx. pallensis a true hybrid taxon. If it is of hybrid origin but now evolutionarily distinct, we are left with another question to resolve.

Specifically,Cx. pallensis found predominately in temperate locations of Northeastern Asia and adult females enter diapause during the cold winter months. The other two extant taxa in theCx. pipienscomplex found in Asia areCx. quinquefasciatusandCx. molestus, neither of which has an ability to enterdiapause. If these two taxa historically hybridized to formCx. pallens,it remains unclear howCx. pallensdeveloped its ability to overwinter in a diapause state. An alternative explanation is that hybridization betweenCx. quinquefasciatusandCx. pipiensoriginally formedCx. pallens.

AsCx. pipiensdoes have an ability to diapause, this would resolve the mystery of whereCx. pallensobtained its diapause abilities. However, this hypothesis presents its own challenges asCx. pipiensis not presently found in east Asia.

Additional research will be necessary to determine how consistent the signature of hybrid origins is throughout the geographic range ofCx. pallens, the extent to which it is reproductively isolated from otherCulextaxa, and the origins of its diapause abilities.

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