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  • Review Article
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Population bottlenecks and founder effects: implications for mosquito-borne arboviral emergence

Abstract

Transmission of arthropod-borne viruses (arboviruses) involves infection and replication in both arthropod vectors and vertebrate hosts. Nearly all arboviruses are RNA viruses with high mutation frequencies, which leaves them vulnerable to genetic drift and fitness losses owing to population bottlenecks during vector infection, dissemination from the midgut to the salivary glands and transmission to the vertebrate host. However, despite these bottlenecks, they seem to avoid fitness declines that can result from Muller’s ratchet. In addition, founder effects that occur during the geographic introductions of human-amplified arboviruses, including chikungunya virus and Zika virus, can affect epidemic and endemic circulation, as well as virulence. In this Review, we discuss the role of genetic drift following population bottlenecks and founder effects in arboviral evolution and spread, and the emergence of human disease.

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Fig. 1: Infection and transmission of arthropod-borne viruses by mosquitoes and bottlenecks.
Fig. 2: The impacts of founder effects and population bottlenecks on the evolution of human-amplified arthropod-borne viruses.
Fig. 3: Phylogenetic tree of CHIKV.
Fig. 4: Phylogenetic tree of ZIKV.

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Acknowledgements

Research in the authors’ laboratories is supported by National Institutes of Health (NIH) grants AI120942 and AI121452 (to S.C.W.) and AI145918 (to N.V.).

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Glossary

Zoonotic

Infections that spill over from non-human animals to humans.

Enzootic

Ancestral, often continuous, transmission cycles of zoonotic arboviruses involving wild animals serving as amplification and/or reservoir hosts.

Anthropophilic mosquitoes

Mosquitoes with a preference for and typically a tendency to bite humans.

Mutant swarms

A population of RNA viruses with numerous, randomly derived mutations resulting from low-fidelity RNA replication (lack of proofreading). Mutant swarms are also termed quasispecies when they are selected and evolve as populations rather than as individual genetic variants.

Quasispecies

A diverse RNA (virus) population that contains many mutants closely related to a master sequence (usually the most abundant) and selected as a population, rather than as individuals, during its evolution.

Population bottlenecks

Major reductions in the population size of organisms, often used in the context of near-extinction events. Population bottlenecks result in a loss in genetic diversity and can also fix mutations at random. Population bottlenecks also represent a form of genetic drift.

Genetic drift

Random changes in the genetic make-up of a population due to chance, random sampling. Drift can dominate the evolution of a virus when population sizes remain small, reducing the efficiency of selection and genetic diversity.

Founder effects

The loss of genetic variation, sometimes resulting in the fixation of random mutations. Founder effects occur when a new population is established by a small number of individuals (founder population) randomly derived from a larger ancestral population. Founder effects represent a form of genetic drift.

Muller’s ratchet

The step-wise fixation following population bottlenecks of random mutations, which are typically deleterious, resulting in a decline in fitness that is difficult to restore in the absence of efficient recombination.

Vector competence

The intrinsic ability of an arthropod to become infected and transmit a pathogen.

Epistasis

Interactions of genes or mutations such that one can suppress the effect of another on a phenotype.

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Weaver, S.C., Forrester, N.L., Liu, J. et al. Population bottlenecks and founder effects: implications for mosquito-borne arboviral emergence. Nat Rev Microbiol 19, 184–195 (2021). https://doi.org/10.1038/s41579-020-00482-8

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