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Diapause and Quiescence: Dormancy Mechanisms That Contribute to The Diniz et al. Parasites & Vectors (2017) 10:310 DOI 10.1186/s13071-017-2235-0 REVIEW Open Access Diapause and quiescence: dormancy mechanisms that contribute to the geographical expansion of mosquitoes and their evolutionary success Diego Felipe Araujo Diniz1, Cleide Maria Ribeiro de Albuquerque2, Luciana Oliveira Oliva2, Maria Alice Varjal de Melo-Santos1 and Constância Flávia Junqueira Ayres1* Abstract Mosquitoes are insects belonging to the order Diptera and family Culicidae. They are distributed worldwide and include approximately 3500 species, of which about 300 have medical and veterinary importance. The evolutionary success of mosquitoes, in both tropical and temperate regions, is due to the various survival strategies these insects have developed throughout their life histories. Of the many adaptive mechanisms, diapause and quiescence, two different types of dormancy, likely contribute to the establishment, maintenance and spread of natural mosquito populations. This review seeks to objectively and coherently describe the terms diapause and quiescence, which can be confused in the literature because the phenotypic effects of these mechanisms are often similar. Keywords: Culicidae, Seasonality, Metabolism, Adaptation, Dispersion, Disease transmission Background Mosquitoes, especially from the genera Anopheles, Mosquitoes are arthropods that can cause considerable Aedes and Culex, include vectors for three major groups nuisance and affect human health worldwide [1, 2]. They of human pathogens: parasites from the genus Plas- are among the most prolific and invasive species, con- modium, which cause malaria; filarial worms from the tributing to the spread of endemic diseases [3, 4]. These genera Wuchereria and Brugia; and many arboviruses, in- organisms are present in most places on the planet, from cluding the agents of dengue, yellow fever, chikungunya, the Arctic to the most remote desert oases, except Ant- zika and others [12–14]. Estimates by the World Health arctica due to its extremely low temperatures. Thus, Organization (WHO) indicate that diseases transmitted by mosquitoes are widely diverse and can easily be found in mosquitoes are among the major causes of morbidity and a wide variety of habitats, including forested, rural and mortality in developing countries [15], and high densities urban environments [2, 5]. of mosquitoes severely challenge vector control programs These insects have been intensely studied since the [16]. The explosive growth of natural mosquito popula- end of the nineteenth century due to their ability to act tions is strongly related to the survival and dispersion as hosts for many pathogens, including helminths, pro- strategies that some species have acquired over the course tozoans and arboviruses, that cause disease in humans of their evolutionary history [17]. and other vertebrates [2, 6]. However, only 10% of the Dormancy is a biological trait that may play an import- approximately 3500 mosquito species are medically rele- ant role in the maintenance of natural populations and vant [1, 7–11]. refers to a physiological phenomenon characterised by the interruption or reduction of metabolic activity in an * Correspondence: [email protected] organism. In mosquitoes, dormancy can occur at differ- 1Entomology Department, Aggeu Magalhães Institute, Oswaldo Cruz ent stages of the life-cycle [18]. Diapause and quiescence Foundation, Av. Professor Moraes Rego, s/n – Cidade Universitária, Recife, PE, represent different types of dormancy found in many Brazil Full list of author information is available at the end of the article species of mosquitoes. In this review, these terms are © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Diniz et al. Parasites & Vectors (2017) 10:310 Page 2 of 13 analysed for their conceptual principles and their re- The first studies on diapause in mosquitoes coincided spective delayed developmental effects; in addition, the with early studies of seasonality, diapause and photoperiod mosquito species found to exhibit these phenomena will in other insects [17]. Early reviews on the topic were per- be noted. formed by Lees [32], Danilevskii [33], Tauber et al. [31] and Danks [20]. Studies at the time were motivated by the Insect dormancy and its various types mosquito’s hematophagous habit, which is linked to its Dormancy is a physiological phenomenon defined as a ability to transmit the causative agents of several diseases state of suspended development or suppressed metabolic such as malaria, filariasis, and many arbovirus infections activity in an organism [19]. Dormancy can occur in (yellow fever, Western equine, St. Louis and Japanese en- both plants and animals; in insects, it can manifest in cephalitis, and West Nile fever) [34]. the embryonic (pharate larvae), immature (larvae and Diapause is common in insects and other arthropods, pupae) and adult stages [18]. This phenomenon can be especially in areas with harsh winters. Many aspects of triggered by climactic signals, especially the photoperiod diapause are critical for understanding the transmission for temperate climate insects and relative humidity for cycle of vector-borne diseases, as this survival strategy tropical insects. This adaptation seeks to promote sur- contributes to the maintenance, establishment, growth vival during and after unfavourable environmental con- and dispersion of natural vector populations after the ditions and is known in the literature as heterodynamic end of an unfavourable season to their development development [20]. In 1869, the term dormancy was first [29]. The process of diapause seeks to reactivate devel- described as a period of inactivity caused by low temper- opment via external signals that control the genetic fac- atures by the French researcher Duclaux, who was tors underlying the dormant phenotype. This can occur studying silkworms (Bombyx mori) [20, 21]. According in several phases of the life-cycle, but most often only to a literature review by Danks [20] on the definitions one developmental stage enters diapause [34]. and terminology of dormancy in insects, dormancy is di- vided into two major categories: diapause and quies- What is the environmental signal that induces diapause cence. The terms diapause and quiescence have been in mosquitoes? reported to be synonymous in the literature [8, 22–27], Species exhibiting the phenotypic plasticity to undergo but these survival strategies arise from distinct signalling diapause have the required information encoded in their pathways even though the strategies have the same goal: genomes. The major stimuli inducing diapause in nat- to ensure survival during and after environmental stress. ural populations are changing photoperiod (short days Mosquitoes belong to one of the most well-adapted and long nights) and gradual decreases in temperature taxa in the insect group; they are present across most of [31, 35–40]. Mosquito species that use photoperiod to the planet, they occupy diverse niches and are potential signal diapause include Aedes albopictus, Aedes atropal- disease vectors [2]. Diapause and quiescence are well pus, Aedes sollicitans, Aedes taeniorhynchus, Culex characterised in several stages of the mosquito life-cycle. pipiens and Culex restuans [38, 39, 41–44]. In the embryonic phase, for example, both strategies Preparation for diapause occurs in mosquitoes when have the same effect: the inhibition of larval hatching. pupae and/or adult females, which are thought to be the Conversely, only diapause drives dormancy in the larval determining stages for this biological trait, are stimulated and adult stages of mosquitoes [28]. by exposure to the seasonal changes that typically occur during transitions between a favourable and unfavour- Diapause in mosquitoes able season [29, 39, 45–47]. For Ae. albopictus, for in- Diapause is a well-studied seasonal survival strategy and stance, induced females develop their offspring for is influenced by several factors, such as the species- diapause, which in turn present low metabolism in each specific ecological interactions, biogeography, life history life-cycle stage during the winter [48, 49]. However, for and physiology of many insects [29]. The etymology of Cx. pipiens, the induced pupae females express diapause the word “diapause” comes from the Greek diapausis when they become adults [50]. Therefore, this ecological (pause), derived from the verb diapauein, which means adaptation is indispensable for coordinating the growth, to stop or to decrease activity at a time of constant ac- development and reproduction of mosquito species tion [30]. Biologically, Tauber et al. [31] defined the dia- found in temperate zones [29]. pause phenomenon as a dynamic state of low metabolic activity that is genetically determined and mediated by Ecophysiological phases of diapause neurohormones that phenotypically affect individuals by The phenomenon of diapause consists of three ecophysi- decreasing morphogenesis, blocking reproduction
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