Immigration and seasonal bottlenecks: High inbreeding despite high genetic diversity in an oscillating population of Culicoides sonorensis (Diptera: Ceratopogonidae)

Authors: Shults, Phillip; Cohnstaedt, Lee; ZHANG, XINMI - University Of California; GERRY, ALEC - University Of California; EYER, PIERRE-ANDRE - Texas A&M University; VARGO, EDWARD - Texas A&M University

Submitted to: Journal of Medical Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/12/2023
Publication Date: 7/7/2023
Citation: Shults, P.T., Cohnstaedt, L.W., Zhang, X., Gerry, A., Eyer, P., Vargo, E. 2023. Immigration and seasonal bottlenecks: High inbreeding despite high genetic diversity in an oscillating population of Culicoides sonorensis (Diptera: Ceratopogonidae). Journal of Medical Entomology. https://doi.org/10.1093/jme/tjad068.
DOI: https://doi.org/10.1093/jme/tjad068

Interpretive Summary: Populations are constantly changing and these changes can affect certain traits of a population. For example, populations with certain genes may be better at transmitting disease-causing pathogens. By monitoring the changes in genes over time, we were able to estimate what factors are influencing these changes in a population of biting midges. The high diversity of genes we observed suggests that new migrants are constantly moving this population. This high rate of movement could be a route by which disease is moved to new areas. We also found that this population was resistant to negative effects of inbreeding and suggests several ways in which this could be possible. Finally, we were able to gain valuable logistical information that will aid in the success of future population level studies in biting midges.

Technical Abstract: Populations are often compared across geographic scales in an attempt to determine their connectivity by assessing their levels of genetic differentiation. However, fewer studies aim at analyzing the temporal genetic changes that occur within populations. Numerous vector species of mosquitos and biting midges are characterized by an oscillating population density, which may potentially affect their dispersal ability, selection, and the amount of genetic diversity within populations over time. Here, we used a monthly collected population of Culicoides sonorensis in California over a three-year timeframe to investigate short-term (intra-annual) and long-term (inter-annual) temporal variations in genetic diversity. This biting midge species is the primary vector of several viruses affecting both wildlife and livestock. We found no significant genetic differentiation between the monthly or yearly collections of adults in this study, and no correlation between population density and the level of inbreeding. However, we showed that repeated episodes of low adult population densities are associated with recurring bottleneck events. Interestingly, we also found a high number of private and rare alleles, which suggests a constant influx of migrants from adjacent populations. Overall, we showed that the high number of migrants maintains a high level of genetic diversity by introducing new alleles to the population, while this increased diversity is potentially counterbalanced by recurrent bottleneck events and high inbreeding, purging unfit alleles each year. Our results therefore highlight the temporal influences of population structure and genetic diversity in C. sonorensis, as well as provides vital insight into the sampling efforts required to genetically characterize other Culicoides populations.