Trends in Parasitology
Volume 36, Issue 1, January 2020, Pages 39-51
Journal home page for Trends in Parasitology

Review
Mosquito Age Grading and Vector-Control Programmes

https://doi.org/10.1016/j.pt.2019.10.011Get rights and content

Highlights

  • New guidelines on evaluating vector-control tools highlight the need for entomological-based measures that predict epidemiological outcomes.

  • Mosquito survivorship is the key variable in epidemiological models of vector-borne disease, but existing morphological measures of age are technically demanding, subjective, and have little utility for arbovirus vectors.

  • Emerging techniques in spectroscopy and existing transcriptional approaches may overcome many of the problems of conventional morphological techniques but their true utility has yet to be tested.

  • Future studies on age grading must focus on the ability of the new technologies to estimate the age of wild-caught adults and provide convincing field validations, replicated across field sites. This will require blinded trials against existing correlates of age (e.g., parity, infection, or the recapture rates of released mosquitoes).

An ability to characterize the age of mosquito populations could provide cost-effective and compelling entomological evidence for the potential epidemiological impacts of vector control. The average age of a mosquito population is the most important determinant of vectorial capacity and the likelihood of disease transmission. Yet, despite decades of research, defining the age of a wild-caught mosquito remains a challenging, impractical, and unreliable process. Emerging chemometric and existing transcriptional approaches may overcome many of the limitations of current morphological techniques, but their utility in terms of field-based monitoring programmes remains largely untested. Herein, we review the potential advantages and disadvantages of new and existing age-grading tools in an operational context.

Section snippets

New Regulatory Requirements and the Importance of Ageing Mosquito Populations

The increasing incidence of mosquito-borne diseases, such as dengue, chikungunya, and Zika, the failure of vaccine development programmes, and stalled efforts to reduce the global malaria burden have underscored the continuing requirement for new, effective vector-control tools and accelerated research and development efforts on this topic. New interventions include the release of Wolbachia-infected mosquitoes to block virus transmission [1] or sterilize vectors [2], genetic manipulations that

Recognizing a Need for a Reliable Age-Grading Method

Classifying a mosquito’s chronological age by examining qualitative or quantitative changes in its reproductive morphology is one of the oldest and most widely acknowledged methods of age grading. Its adoption was driven by its apparent technical simplicity: dissection tools, a steady pair of hands, and a light microscope were all that was required. The simplest of these microscopy techniques, the ovary tracheation method, distinguishes whether a female mosquito is nulliparous (has not laid

Transition to the Biochemical Age

The identification of age-dependent changes to particular biochemical signals in mosquitoes marked a move from subjective, dissection-based approaches to the adoption of contemporary analytical methods. Two classes of biochemicals, shown to vary with age, include the pteridines (pigments common in the wings and eyes of insects) and cuticular hydrocarbons, common in the mosquito integument.

Although initial studies isolated individual pteridines using high-pressure liquid chromatography (HPLC),

Genes and Proteins

Transcriptional profiling provided the next potential advance in mosquito age grading [23,51]. This measures gene expression using reverse transcriptase quantitative PCR (RT-qPCR), and it may be used to explore correlations between the transcription products of multiple genes and age-dependent expression patterns. Age-responsive genes identified in the model insect Drosophila melanogaster were used to find related homologues in Ae. aegypti mosquitoes whose expression subsequently proved to be

Chemometrics: NIRS and MIRS

In the last decade, one of the most widely reported innovations for differentiating a variety of mosquito traits (age, species, and infection) has been the use of NIRS and MIRS. NIRS measures the absorption of organic compounds within a sample using an electromagnetic spectrum in the near-infrared region (350–2500 nm) [28], and subsequent chemometric analysis may detect compositional differences between samples according to the near-infrared energy absorbed [27]. The derived spectra are

Areas for Consideration

A major challenge for contemporary analytical methods of mosquito age prediction is to develop models that are robust to the variance induced by field environments. Currently only a handful of studies have attempted to validate emerging chemometric [64] and molecular [22,32,50,55] approaches against wild-caught adult mosquitoes. Most proof-of-principle studies restrict themselves to validating models against established laboratory colonies or field-sourced larvae reared to adults [28,61,62].

Concluding Remarks

Calls for the rigorous evaluation of vector-control programmes have become louder in response to emerging pandemics of arboviral diseases (dengue, chikungunya, Zika), the continued commitment to malaria elimination across diverse habitats, and the strategic priorities of the new WHO Global Vector Control Response [10]. Unfortunately, the tools that we have for characterizing the entomological drivers of transmission are limited and, although the need for standard measures of the components of

Acknowledgements

G.J.D., O.T.W.O., and T.S.C. were supported by USAID grant AID-OAA-F-16-00094. T.S.C. received additional support from the UK Medical Research Council (MRC) grant MR/P01111X/1.

Glossary

Age grading
a method of determining the age structure of a target population by analysing morphological, biochemical, or genetic factors that are age-related (chronologically or physiologically).
Chemometrics
the use of mathematical and statistical methods to design optimal models for the interpretation of chemical data. It is the basis for interpreting hydrocarbon signatures, gene expression, or NIRS/MIRS outputs for the purposes of mosquito age grading.
Daily survival probability
the probability

References (77)

  • G.M. Vazquez-Prokopec

    Combining contact tracing with targeted indoor residual spraying significantly reduces dengue transmission

    Sci. Adv.

    (2017)
  • C. Garrett-Jones

    Prognosis for interruption of malaria transmission through assessment of the mosquito's vectorial capacity

    Nature

    (1964)
  • WHO

    Global Vector Control Response 2017–2030

    (2016)
  • WHO

    The Evaluation Process for Vector Control Products

    (2017)
  • S.E. Bellan

    The importance of age dependent mortality and the extrinsic incubation period in models of mosquito-borne disease transmission and control

    PLoS One

    (2010)
  • S.A. Gourley

    Eradicating vector-borne diseases via age-structured culling

    J. Math. Biol.

    (2007)
  • H.M. Gilles

    Essential Malariology

    (1993)
  • L.E. Hugo

    Vector competence of Australian Aedes aegypti and Aedes albopictus for an epidemic strain of Zika virus

    PLoS Negl. Trop. Dis.

    (2019)
  • I. Dia

    Bionomics of Anopheles gambiae Giles, An. arabiensis Patton, An. funestus Giles and An. nili (Theobald) (Diptera: Culicidae) and transmission of Plasmodium falciparum in a Sudano-Guinean zone (Ngari, Senegal)

    J. Med. Entomol.

    (2003)
  • J.V.B. Dis

    Life table analysis of Anopheles gambiae (Diptera: Culicidae) in relation to malaria transmission

    J. Vector Borne Dis.

    (2009)
  • P. McDonald

    Population characteristics of domestic Aedes aegypti (Diptera: Culicidae) in villages on the Kenya Coast I. Adult survivorship and population size

    J. Med. Entomol.

    (1977)
  • L.E. Muir et al.

    Aedes aegypti survival and dispersal estimated by mark-release-recapture in northern Australia

    Am. J. Trop. Med. Hyg.

    (1998)
  • J.D. Charlwood

    ‘We like it wet’: a comparison between dissection techniques for the assessment of parity in Anopheles arabiensis and determination of sac stage in mosquitoes alive or dead on collection

    PeerJ

    (2018)
  • L.E. Hugo

    Adult survivorship of the dengue mosquito Aedes aegypti varies seasonally in central Vietnam

    PLoS Negl. Trop. Dis.

    (2014)
  • P.E. Cook

    The use of transcriptional profiles to predict adult mosquito age under field conditions

    Proc. Natl. Acad. Sci. U. S. A.

    (2006)
  • T.K. Joy

    Aging field collected Aedes aegypti to determine their capacity for dengue transmission in the southwestern United States

    PLoS One

    (2012)
  • M.G. Jiménez

    Prediction of mosquito species and population age structure using mid-infrared spectroscopy and supervised machine learning

    Wellcome Open Res.

    (2019)
  • B. Lambert

    Monitoring the age of mosquito populations using near-infrared spectroscopy

    Sci. Rep.

    (2018)
  • V.S. Mayagaya

    Non-destructive determination of age and species of Anopheles gambiae sl using near-infrared spectroscopy

    Am. J. Trop. Med. Hyg.

    (2009)
  • M. Sikulu

    Near-infrared spectroscopy as a complementary age grading and species identification tool for African malaria vectors

    Parasit. Vectors

    (2010)
  • L.E. Hugo

    Investigation of cuticular hydrocarbons for determining the age and survivorship of Australasian mosquitoes

    Am. J. Trop. Med. Hyg.

    (2006)
  • T.S. Detinova

    Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria

    Monogr. Ser. World Health Organ.

    (1962)
  • C.M. Degener

    Evaluation of the effectiveness of mass trapping with BG-sentinel traps for dengue vector control: a cluster randomized controlled trial in Manaus, Brazil

    J. Med. Entomol.

    (2014)
  • M.L. Desena

    Potential for aging female Aedes aegypti (Diptera: Culicidae) by gas chromatographic analysis of cuticular hydrocarbons, including a field evaluation

    J. Med. Entomol.

    (1999)
  • C.E. Gunning

    Efficacy of Aedes aegypti control by indoor ultra low volume (ULV) insecticide spraying in Iquitos, Peru

    PLoS Negl. Trop. Dis.

    (2018)
  • V. Polovodova

    The determination of the physiological age of female Anopheles by the number of gonotrophic cycles completed

    Medskaya. Parazit.

    (1949)
  • M.T. Gillies et al.

    A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in North-Eastern Tanzania

    Bull. Entomol. Res.

    (1965)
  • L.E. Hugo

    Evaluations of mosquito age grading techniques based on morphological changes

    J. Med. Entomol.

    (2008)
  • 3

    These authors made equal contributions

    View full text