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Population bottlenecks and founder effects: implications for mosquito-borne arboviral emergence. ​

Literature Information ​

DOI10.1038/s41579-020-00482-8
PMID33432235
JournalNature reviews. Microbiology
Impact Factor103.3
JCR QuartileQ1
Publication Year2021
Times Cited50
Keywordspopulation bottlenecks, founder effects, mosquito-borne viruses, genetic drift, human disease
Literature TypeJournal Article, Research Support, N.I.H., Extramural, Review
ISSN1740-1526
Pages184-195
Issue19(3)
AuthorsScott C Weaver, Naomi L Forrester, Jianying Liu, Nikos Vasilakis

TL;DR ​

This review explores how genetic drift and founder effects during population bottlenecks in arthropod vectors influence the evolution and spread of arboviruses, such as chikungunya and Zika virus, while allowing them to avoid fitness declines associated with Muller's ratchet. The findings highlight the importance of these genetic dynamics in shaping epidemic patterns and virulence in human diseases caused by arboviruses.

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population bottlenecks · founder effects · mosquito-borne viruses · genetic drift · human disease

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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Primary Questions Addressed ​

  1. How do population bottlenecks specifically influence the genetic diversity of arboviruses in mosquito vectors?
  2. What are the mechanisms by which founder effects can alter the virulence of newly introduced arboviruses in human populations?
  3. In what ways can understanding genetic drift in arboviruses inform strategies for controlling mosquito-borne diseases?
  4. How do environmental factors interact with population bottlenecks and founder effects to shape the emergence of arboviral epidemics?
  5. What role do vector competence and host immunity play in the dynamics of arboviral transmission following population bottlenecks?

Key Findings ​

Research Background and Objectives ​

Arthropod-borne viruses (arboviruses) are primarily transmitted through arthropod vectors, such as mosquitoes and ticks, and pose significant public health risks due to their ability to cause epidemics in humans. This review focuses on understanding how population bottlenecks and founder effects influence the evolution and spread of arboviruses, particularly those that have undergone geographic expansions leading to human disease outbreaks, such as chikungunya and Zika viruses.

Main Methods/Materials/Experimental Design ​

The review synthesizes findings from various studies that investigate the genetic and evolutionary dynamics of arboviruses during their transmission cycles. Key methods include:

  1. Genetic Analysis: Phylogenetic studies to trace the evolution and spread of arboviruses.
  2. Experimental Infection Studies: Evaluating how arboviruses navigate bottlenecks during mosquito infection and dissemination.
  3. Population Genetics: Assessing genetic drift and founder effects using sequencing data from infected hosts and vectors.

The following flowchart summarizes the main processes discussed in the review:

Mermaid diagram

Key Results and Findings ​

  1. Population Bottlenecks: Arboviruses face significant bottlenecks during each stage of their transmission cycle, leading to reduced genetic diversity and potential fitness declines.
  2. Genetic Drift: High mutation rates coupled with small population sizes can lead to genetic drift, which may fix deleterious mutations, particularly during founder events when a small number of viral particles initiate new infections.
  3. Founder Effects: Geographic introductions of arboviruses often result in founder effects, where the new population may carry random mutations that affect virulence and transmission efficiency.
  4. Adaptive Evolution: Despite these challenges, some arboviruses demonstrate remarkable stability and adaptability, maintaining fitness through rapid population turnover and selection of high-fitness variants.

Main Conclusions/Significance/Innovation ​

The review emphasizes the importance of understanding genetic drift and founder effects in the context of arboviral emergence. These factors can significantly influence the epidemiology of arboviruses and their potential to cause outbreaks. The findings highlight the need for enhanced surveillance and modeling to predict and manage arboviral threats effectively.

Research Limitations and Future Directions ​

  1. Limitations: The review primarily synthesizes existing literature and may not encompass all recent findings or the full complexity of arboviral interactions with vectors and hosts.
  2. Future Directions: Further research is needed to:
    • Explore the mechanisms of viral adaptation to different hosts and environments.
    • Investigate the role of the mosquito microbiome in vector competence.
    • Develop predictive models for arboviral emergence based on genetic and environmental factors.

In conclusion, the insights gained from understanding the genetic dynamics of arboviruses during their transmission cycles can inform public health strategies to mitigate the risks posed by these pathogens.

References ​

  1. Chikungunya Virus Strains Show Lineage-Specific Variations in Virulence and Cross-Protective Ability in Murine and Nonhuman Primate Models. - Rose M Langsjoen;Sherry L Haller;Chad J Roy;Heather Vinet-Oliphant;Nicholas A Bergren;Jesse H Erasmus;Jill A Livengood;Tim D Powell;Scott C Weaver;Shannan L Rossi - mBio (2018)
  2. Rapid fitness losses in mammalian RNA virus clones due to Muller's ratchet. - E Duarte;D Clarke;A Moya;E Domingo;J Holland - Proceedings of the National Academy of Sciences of the United States of America (1992)
  3. Venezuelan equine encephalitis virus in the mosquito vector Aedes taeniorhynchus: infection initiated by a small number of susceptible epithelial cells and a population bottleneck. - Darci R Smith;A Paige Adams;Joan L Kenney;Eryu Wang;Scott C Weaver - Virology (2008)
  4. A Zika virus envelope mutation preceding the 2015 epidemic enhances virulence and fitness for transmission. - Chao Shan;Hongjie Xia;Sherry L Haller;Sasha R Azar;Yang Liu;Jianying Liu;Antonio E Muruato;Rubing Chen;Shannan L Rossi;Maki Wakamiya;Nikos Vasilakis;Rongjuan Pei;Camila R Fontes-Garfias;Sanjay Kumar Singh;Xuping Xie;Scott C Weaver;Pei-Yong Shi - Proceedings of the National Academy of Sciences of the United States of America (2020)
  5. First Report of Aedes aegypti Transmission of Chikungunya Virus in the Americas. - Esteban E Díaz-González;Tiffany F Kautz;Alicia Dorantes-Delgado;Iliana R Malo-García;Maricela Laguna-Aguilar;Rose M Langsjoen;Rubing Chen;Dawn I Auguste;Rosa M Sánchez-Casas;Rogelio Danis-Lozano;Scott C Weaver;Ildefonso Fernández-Salas - The American journal of tropical medicine and hygiene (2015)
  6. Inter- and intra-host sequence diversity reveal the emergence of viral variants during an overwintering epidemic caused by dengue virus serotype 2 in southern Taiwan. - Hui-Ying Ko;Yao-Tsun Li;Day-Yu Chao;Yun-Cheng Chang;Zheng-Rong T Li;Melody Wang;Chuan-Liang Kao;Tzai-Hung Wen;Pei-Yun Shu;Gwong-Jen J Chang;Chwan-Chuen King - PLoS neglected tropical diseases (2018)
  7. Viral RNA-dependent RNA polymerase mutants display an altered mutation spectrum resulting in attenuation in both mosquito and vertebrate hosts. - K Lane Warmbrod;Edward I Patterson;Tiffany F Kautz;Adam Stanton;Dedeke Rockx-Brouwer;Birte K Kalveram;Kamil Khanipov;Saravanan Thangamani;Yuriy Fofanov;Naomi L Forrester - PLoS pathogens (2019)
  8. Spread of yellow fever virus outbreak in Angola and the Democratic Republic of the Congo 2015-16: a modelling study. - Moritz U G Kraemer;Nuno R Faria;Robert C Reiner;Nick Golding;Birgit Nikolay;Stephanie Stasse;Michael A Johansson;Henrik Salje;Ousmane Faye;G R William Wint;Matthias Niedrig;Freya M Shearer;Sarah C Hill;Robin N Thompson;Donal Bisanzio;Nuno Taveira;Heinrich H Nax;Bary S R Pradelski;Elaine O Nsoesie;Nicholas R Murphy;Isaac I Bogoch;Kamran Khan;John S Brownstein;Andrew J Tatem;Tulio de Oliveira;David L Smith;Amadou A Sall;Oliver G Pybus;Simon I Hay;Simon Cauchemez - The Lancet. Infectious diseases (2017)
  9. Chikungunya in the Americas. - Isabelle Leparc-Goffart;Antoine Nougairede;Sylvie Cassadou;Christine Prat;Xavier de Lamballerie - Lancet (London, England) (2014)
  10. Insect-Specific Viruses: A Historical Overview and Recent Developments. - Christopher M Roundy;Sasha R Azar;Shannan L Rossi;Scott C Weaver;Nikos Vasilakis - Advances in virus research (2017)

Literatures Citing This Work ​

  1. Current Status of Chikungunya in India. - - Frontiers in microbiology (2021)
  2. Multilocus Genotyping of 'Candidatus Phytoplasma solani' Associated with Rubbery Taproot Disease of Sugar Beet in the Pannonian Plain. - Živko Ćurčić;Andrea Kosovac;Jelena Stepanović;Emil Rekanović;Michael Kube;Bojan Duduk - Microorganisms (2021)
  3. Lineage Divergence and Vector-Specific Adaptation Have Driven Chikungunya Virus onto Multiple Adaptive Landscapes. - Rubing Chen;Jessica A Plante;Kenneth S Plante;Ruimei Yun;Divya Shinde;Jianying Liu;Sherry Haller;Suchetana Mukhopadhyay;Scott C Weaver - mBio (2021)
  4. Investigation of Biological Factors Contributing to Individual Variation in Viral Titer after Oral Infection of Aedes aegypti Mosquitoes by Sindbis Virus. - Peter Hodoameda;Linus Addae;Rollie J Clem - Viruses (2022)
  5. Glycosaminoglycan binding by arboviruses: a cautionary tale. - Maria D H Alcorn;William B Klimstra - The Journal of general virology (2022)
  6. Genetic Drift and Purifying Selection Shaped Mitochondrial Genome Variation in the High Royal Jelly-Producing Honeybee Strain (Apis mellifera ligustica). - Chuan Ma;Ruoyang Hu;Cecilia Costa;Jianke Li - Frontiers in genetics (2022)
  7. Impact of structural dynamics on biological functions of flaviviruses. - Karin Stiasny;Iris Medits;Lena Roßbacher;Franz X Heinz - The FEBS journal (2023)
  8. Vector-Borne Viral Diseases as a Current Threat for Human and Animal Health-One Health Perspective. - Wojciech Socha;Malgorzata Kwasnik;Magdalena Larska;Jerzy Rola;Wojciech Rozek - Journal of clinical medicine (2022)
  9. Mitochondrial Genome Contributes to the Thermal Adaptation of the Oomycete Phytophthora infestans. - Lin-Lin Shen;Abdul Waheed;Yan-Ping Wang;Oswald Nkurikiyimfura;Zong-Hua Wang;Li-Na Yang;Jiasui Zhan - Frontiers in microbiology (2022)
  10. Heterogeneity of Rift Valley fever virus transmission potential across livestock hosts, quantified through a model-based analysis of host viral load and vector infection. - Hélène Cecilia;Roosmarie Vriens;Paul J Wichgers Schreur;Mariken M de Wit;Raphaëlle Métras;Pauline Ezanno;Quirine A Ten Bosch - PLoS computational biology (2022)

... (40 more literatures)

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