Review article

Implications of diet on mosquito life history traits and pathogen transmission

Laura Carvajal-Lagoa, María Jos e Ruiz-Lo peza, Jordi Figuerolaa,c,*, Josué

Martínez-de la Puentea,b,c

a Departamento de Ecología de Humedales, Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas, CSIC, Spainb Departamento de Parasitología, Facultad de Farmacia, Campus Universitario de Cartuja, Universidad de Granada, 18071 Granada, Spain c CIBER de Epidemiología y Salud Pública (CIBERESP), Spain

* Corresponding author. Departamento de Ecología de Humedales, Estacio n Biolo gica de Don ana - CSIC, Calle Am erico Vespucio 26, 41092 Sevilla, Spain. E-mail address: jordi@ebd.csic.es (J. Figuerola).

Keywords:

Mosquito diet ArbovirusFeeding behaviour Pathogen infection Vectorial capacity

ABSTRACT

The environment, directly and indirectly, affects many mosquito traits in both the larval and adult stages. The availability of food resources is one of the key factors influencing these traits, although its role in mosquito fitness and pathogen transmission remains unclear. Larvae nutritional status determines their survivorship and growth, having also an impact on adult characteristics like longevity, body size, flight capacity or vector competence. During the adult stage, mosquito diet affects their survival rate, fecundity and host-seeking behaviour. It also affects mosquito susceptibility to infection, which may determine the vectorial capacity of mosquito populations. The aim of this review is to critically revise the current knowledge on the effects that both larval and adult quantity and quality of the diet have on mosquito life history traits, identifying the critical knowledge gaps and proposing future research lines. The quantity and quality of food available through their lifetime greatly determine adult body size, longevity or biting frequency, therefore affecting their competence for pathogen transmission. In addition, natural sugar sources for adult mosquitoes, i.e., specific plants providing high metabolic energy, might affect their host-seeking and vertebrate biting behaviour. However, most of the studies are carried out under laboratory conditions, highlighting the need for studies of feeding behaviour of mosquitoes under field conditions. This kind of studies will increase our knowledge of the impact of diets on pathogen transmission, helping to develop successful control plans for vector-borne diseases.

1. Introduction

Emerging infectious diseases (EIDs) represent an important human health concern with devastating consequences for human and animal populations (WHO, 2017). It is estimated that around 22%–28% of EIDs events from 1940 to 2004 correspond to vector-borne diseases (Jones et al., 2008). At present they cause around 700,000 deaths annually and important economic costs (WHO, 2020). Mosquitoes are one of the more important disease vectors. They transmit numerous parasites and other pathogens, like viruses of the families Flaviviridae, causing Dengue, West Nile fever, yellow fever or Zika, and Togaviridae including Chi- kunguya and Mayaro viruses (Weger-Lucarelli et al., 2018; Wiggins et al., 2018). In addition, mosquitoes are the vectors of parasites like malarial parasites, and filarial worms (e.g. Dirofilaria) (Tolle, 2009). Mosquitoes of the genera Aedes, Anopheles and Culex are considered the primary vectors of these pathogens (Paupy et al., 2009; Kilpatrick and Randolph, 2012). For example, Aedes aegypti and Aedes albopictus are the main vectors of Dengue, Yellow fever, Chikungunya and Zika viruses, which have caused sporadic infections in Europe, but important out- breaks in Africa, Asia, and South America in the last decades with dra- matic consequences (Rezza et al., 2007; Kilpatrick and Randolph, 2012; Mayer et al., 2017). Because of the absence of effective vaccines for most of these diseases, the control of vector populations is gaining importance as the most effective method of disease prevention (Müller et al., 2010a, 2010b; Imam et al., 2014; Wang et al., 2017; Sissoko et al., 2019). To successfully control these vector-borne pathogens, it is critical to improve our understanding of the factors potentially affecting mosquito life history traits and their vectorial capacity (Linenberg et al., 2016; Kang et al., 2017).

Vector competence is the ability of a vector to transmit a disease (Beerntsen et al., 2000; Cohuet et al., 2010). It is governed mainly by intrinsic genetic related factors that determine the ability of the vector to become infected and to successfully transmit the pathogen to a new vertebrate host (Hardy et al., 1983). However, extrinsic factors may also affect vector competence, for example by affecting gene expression and consequently mosquito phenotype (Ferreira et al., 2020). In contrast, vectorial capacity is a broad term that reflects the efficiency of vector-borne pathogen transmission. It depends not only on vector competence but is also influenced by environmental, behavioural and biochemical factors that may affect vector, host and pathogen populations and their interactions (Beerntsen et al., 2000; Cohuet et al., 2010). Numerous intrinsic (Sheldon and Verhulst 1996; Delhaye et al., 2016) and extrinsic factors (Lambrechts et al., 2006; Araújo et al., 2012; Lef`evre et al., 2013; Couret et al., 2014; Sangare et al., 2014; Linenberg et al., 2016) affect mosquito capacity for the transmission of pathogens (Fig. 1). One of the most relevant extrinsic factors is mosquito diet, because of its effects on development, longevity and competence for pathogen transmission by mosquitoes (Muturi et al., 2011; Linenberg et al., 2016; Weger-Lucarelli et al., 2018; Paige et al., 2019). Moreover, diet determines the contact rate between mosquitoes and susceptible vertebrate hosts, consequently increasing the possibility of pathogen

dissemination (Straif and Beier, 1996; Canyon et al., 1999; Gary and Foster, 2001). Nevertheless, it is currently unclear how mosquito diet influences different mosquito traits. The aim of this article is to review the impact of diet through different life stages of mosquitoes on different traits that may affect their importance for the transmission of pathogens. In addition, we will also review how differences in diet affect mosquito-pathogen interactions. Search for papers dealing with mosquitoes and diet was done in Web of Knowledge, Scopus, Pubmed and Google scholar and by checking the references cited in papers dealing with the topic, but without following PRISMA guidelines.

2. Impacts of diet during the larval stage of mosquitoes

Mosquito larvae feed on different organic elements depending on their abundance in the field, like microorganisms (bacteria or protozoa), unicellular and filamentous algae, small metazoans (i.e. crustaceans) and non-living materials like dust organic detritus (Merritt et al., 1992). Larvae acquire essential compounds from these sources including car- bohydrates, amino acids, and fat for their development and to store necessary energetic reserves for metamorphosis into adults (Timmermann and Briegel, 1999; Briegel et al., 2001; Ng’habi et al., 2008). Mosquitoes feed in the larval stages but not as pupae. Therefore, they depend on the resources acquired as larvae to develop as healthy adults (Barker and Reisen, 2019). Most research about the effects of diet on mosquito traits has been focused on the study of the mosquito larval stage (Dodson et al., 2011; Muturi et al., 2011; Yoshioka et al., 2012; Jannat and Roitberg, 2013; Linenberg et al., 2016; Paige et al., 2019; Souza et al., 2019), while less attention has been paid to the adult phase.

Variations in the availability of food for larvae influence different traits of adult mosquitoes like body size (Briegel, 1990; Takken et al., 1998; Ng’habi et al., 2008; Yoshioka et al., 2012; Lang et al., 2018; Souza et al., 2019), longevity or survivorship (Araújo et al., 2012; Moller-Jacobs et al., 2014; Vantaux et al., 2016a; Sasmita et al., 2019), flight activity (Klowden et al., 1988; Takken et al., 1998) or their vector competence to different pathogens (Muturi et al., 2011; Linenberg et al., 2016; Weger-Lucarelli et al., 2018; Paige et al., 2019). Published evi- dence derived from experiments on Anopheles gambiae and Anopheles darlingi, where adult mosquitoes derived from larvae grown with a high food quantity had larger body sizes and higher survival rates than in- dividuals grown with less food (Ng’habi et al., 2008; Araújo et al., 2012). Ae. aegypti females emerged from highly-nutritive conditions in the larval stage presented a large body size associated with a higher proportion of metabolic reserves (Briegel, 1990). This greater body condition increased their feeding capacity on vertebrate hosts and reproductive success (Briegel, 1990). Not only the quantity but also the quality of larval diet might affect mosquito’ fitness (Paige et al., 2019; Souza et al., 2019). Depending on the type of larval diet used with Anopheles coluzzii, different adult mosquito traits were impacted, like body size and survival, the midgut microbiota and the prevalence and intensity of Plasmodium berghei infection (Linenberg et al., 2016). An experiment testing the effects of various types of larval diets and tem- peratures in Ae. aegypti males detected significant effects on the development and

survival of larvae, and adult longevity, but no differences in mating capacity (Sasmita et al., 2019). Undernutrition caused by limited access to food may extend the lifespan of a considerable number of animal species (Mair and Dillin, 2008), including mosquitoes like Ae. aegypti (Joy et al., 2010). In Culex quinquefasciatus, adult males lived longer when fed a low-food larval diet, but females lived longer when fed a high-food larval diet (Vrzal et al., 2010). However, other fitness traits might be altered to compensate for this change in access to energy, such as fecundity (Joy et al., 2010).

Fig. 1. Schematic summary of some extrinsic and intrinsic factors affecting larva and adult mosquito’s traits. In larval phase, environment (like temperature or use of larvicides), larval competition and food availability determine traits such as devel- opment time, survival and teneral reserves, while during the adult phase they may impact on their body size, longevity, etc. As adults, environmental conditions (tempera- ture, insecticides and others), diet (sugar- plants and vertebrate blood) and intrinsic mosquito traits (largely related to their larval condition) might determine their longevity, survival, gut microbiota or vector competence and vectorial capacity, among others. Figure created with Biorender.

Differences in larval traits may be due to a differential develop- mental rate

depending on nutritional resources. For example, in exper- iments with An. darlingi larvae fed with different quantities of ground fish food, the group with the highest amount supplied developed faster and presented an increased larval survivorship (Araújo et al., 2012). For Ae. aegypti (Muturi et al., 2011; Zirbel et al., 2018) and Culex tarsalis (Dodson et al., 2011) it was reported a longer larvae development time under starvation and limited access to food treatments. In addition, Ae. aegypti larvae kept on a bacteria or microalgae-based diets had a reduced development rate and survivorship than larvae kept on a yeast-based diet (Souza et al., 2019). However, contradictory results have been also reported. This is the case of a study on Ae. aegypti larvae where authors reported a faster development when combining a high density of larvae (80 individuals) and a low diet level (1%) of a mixture solution (beef liver powder, tuna meal and vitamin combined on water) (Couret et al., 2014). Thus, under these conditions, there is a rapid development time from hatch to emergence compared with those larvae with a higher diet level (4–8%) and same density level (Couret et al., 2014). In An. gambiae and An. coluzzii fed with the highest amount of Tetramin® baby fish food, larvae had a more rapid development but lower survivorship than their poor-nourished counterparts (Vantaux et al., 2016a, 2016b). These outcomes expose the controversy regarding the effects that diet has on larval traits during development and may be due to other factors affecting the developmental time of the larvae and the amount of nu- trients available to them, such as larval competition (Walsh et al., 2011; Hauser et al., 2020). Various authors have indirectly investigated the role of reduced availability of nutritional resources by increasing the competition between mosquito larvae during development (Gilles et al., 2011; Yoshioka et al., 2012; Jannat and Roitberg, 2013). For example, no effects on Ae. albopictus larvae survival was found when they were subjected to different nutrition and competitive stress treatments (Yoshioka et al., 2012). In the field, habitats with fewer conspecific larvae and higher proportion of organic food sources are mostly selected by adult females as oviposition sites (Yoshioka et al., 2012). This observation suggests that larval density and food limitation may affect mosquito development. In fact, increasing larvae competition was associated with a reduced adult body size (Sumanochitrapon et al., 1998; Alto et al., 2005; Yoshioka et al., 2012; Jannat and Roitberg, 2013; Hauser et al., 2020) and survival until adulthood (Gilles et al., 2011; Walsh et al., 2011; Jannat and Roitberg, 2013). Other factors could also explain the negative effects of larval competition on the development and survival of mosquitoes. For example, a physical crowding effect (Dye, 1982; Roberts, 1998; Roberts and Kokkinn, 2010) or the produc- tion of growth retardant factors (GRF) that delay pupation (Moore and Fisher, 1969; Ikeshoji and Mulla, 1970; Kuno and Moore, 1975; Reisen, 1975), although the scarcity of larval food was proposed as the principal reason to the production of these GRF (Moore and Whitacre, 1972).

In summary, these studies provide compelling evidence of the effect of larval diet on traits developed both during larval and adult stages of mosquitoes. Nevertheless, conclusions obtained in studies conducted under laboratory conditions should be interpreted with caution as some of the conditions linked to ex-situ rearing may affect the observed associations. For example, larval

environment had important effects on size and fitness of adult mosquitoes (Schneider et al., 2004; Ng’habi et al., 2008; Vantaux et al., 2016a). However, important environmental parameters, like temperature and larvae competition, fluctuate in the field and this variability is hard to reproduce under laboratory condi- tions. Furthermore, larvae reared in the laboratory usually obtain higher nutritional reserves because are kept in ideal conditions. Female mosquitoes reared in the laboratory to mimic the nutritional conditions experienced in the wild survived less than those reared under standard laboratory conditions, but the opposite was found for males (Vrzal et al., 2010). The progeny of field collected Aedes vexans (Klowden et al., 1988) and Aedes triseriatus (Mather and DeFoliart 1983) develop greater body size when reared under laboratory conditions. In addition, the effects may not be linear and perhaps are only apparent over certain nutrition thresholds, potentially explaining apparent contradictory results between studies.

3. Impacts of diet during the adult stage of mosquitoes

Adult mosquitoes ingest plant-derived sugars like nectar (floral and extra-floral) (Foster, 1995; Gary and Foster, 2004; Vrzal et al., 2010). There is also evidence of sugar feeding on honeydew (Foster, 1995; Gary and Foster, 2004; Impoinvil et al., 2004), flowers (Manda et al., 2007b; Müller et al., 2011), pollen (Eischen and Foster, 1983), plant–tissues (Schlein and Muller, 1995; Müller and Schlein, 2005; Gu et al., 2011; Qualls et al., 2013), damaged seedpods (Müller et al., 2010c; Yu et al., 2016) or, even, on sweet fluids present in some home waste items (Dieng et al., 2017). In the field, different sugars are nutritional sources for mosquitoes of both sexes including carbohydrate like glucose, sucrose, and fructose (Foster, 1995; Manda et al., 2007a; Kessler et al., 2015). The total concentration of sugars present in certain plants was positively correlated with the survival rate and reproductive success (i.e. ovipo- sition) of mosquitoes feeding on them (Manda et al., 2007a). Conse- quently, mosquito fitness may be increased by selectively feeding on some plant species under natural conditions (Manda et al., 2007a; Gu et al., 2011; Yu et al., 2016). Adults of An. gambiae (Gary and Foster, 2004; Impoinvil et al., 2004; Manda et al., 2007b), Anopheles arabiensis (Gouagna et al., 2014), Ae. albopictus (Müller et al., 2010c; 2011; Qualls et al., 2013), Ae. aegypti (Peach et al., 2019; Sissoko et al., 2019) and Culex pipiens (Müller and Schlein, 2005) prefer to feed on particular components from specific plant species. For instance, An. gambiae feed primarily on flowers of many perennial plants in Kenya (Manda et al., 2007b); Ae. aegypti mosquitoes feed on flowers and fruits in urban en- vironments (Sissoko et al., 2019); Ae. albopictus and Anopheles sergentii feed on seed pods and plant tissue (Müller et al., 2010c; Gu et al., 2011). A recent study showed that male An. coluzzii feeding on papayas sur- vived longer and had a higher mating rate than those feeding on bananas (Nignan et al., 2020).

Plant-derived food is the unique source of energy for males and the primary source for females (Okech et al., 2003; Sissoko et al., 2019), likely representing the first food for both sexes after emergence (Foster, 1995; Foster and Takken, 2004). Female mosquitoes of the family Culicidae are blood-feeders (Manda et al., 2007a; Stone and Foster, 2013). Although amino acids are also present in great quantity in

the nectar of some plants (Baker and Baker, 1973), these mosquito species obtain amino acids necessary for the development of eggs and ovaries from vertebrate blood (Clements, 1956; Stone and Foster, 2013). When amino acids are consumed together with carbohydrates in high pro- portion, they lengthen the lifespan of some insects (Vrzal et al., 2010). Therefore, even though females ingest blood during the gonotrophic cycle (the period of time from host seeking, blood-feeding and egg production to oviposition (Barker and Reisen, 2019), they may still need to feed from sugar plants and nectar to obtain energy for basic mainte- nance (Foster, 1995). This may provide enough energy to promote survival (Vrzal et al., 2010), fecundity (Briegel, 1990) and flight activity (Briegel et al., 2001; Scaraffia and Wells, 2003).

The need to develop novel tools for vector control in areas with active circulation of relevant mosquito-borne pathogens led to an increasing interest on adult mosquito diet (Fikrig et al., 2017, 2020; Sissoko et al., 2019). For example, using attractive toxic sugar baits (a technique known as ATSB) on flowers and fruits of different plant spe- cies on which adults of Culex, Aedes and Anopheles species feed frequently (Müller et al., 2010b; Beier et al., 2012; Sissoko et al., 2019). However, most of the evidence is derived from laboratory experiments, while there are few direct observations in natural (Mogi and Miyagi, 1989; Müller and Schlein, 2005; Manda et al., 2007b; Müller et al., 2011) and semi-natural conditions (Abdel-Malek, 1964).

3.1. Flight capacity of adult mosquitoes and host-seeking based on their diet

Metabolic reserves accumulated during the larval stage (i.e. the teneral reserves) (Timmermann and Briegel, 1999) provide limited flight capacity for the newly emerged adults. Thus, they need to quickly obtain the first meal to allow survivorship and flight (Briegel et al., 2001). Depending on larval nutritional conditions, adults present vari- able quantities of glycogen, proteins and lipids that can be mobilized to allow survivorship, flight and host-seeking activity (Timmermann and Briegel, 1999; Vrzal et al., 2010). Flying is a costly activity for mosquitoes. It has been suggested that mosquitoes feed on carbohy- drates after emergence to support flight because they completely use the teneral reserves of glycogen in the first days after emergence (Briegel et al., 2001). In contrast, lipid and protein reserves are not always consumed (Nayar and Handel, 1971; Briegel, 1990). Large females from well-nourished larvae typically had more metabolic reserves than their small counterparts (Takken et al., 1998; Vrzal et al., 2010). In Ae. aegypti females exposed to a suboptimal larval nutrition, reduced body size was associated with a reduced ability to find vertebrate hosts (Nasci, 1986; Klowden et al., 1988; Briegel, 1990) and an increase in single-host blood-meals during one gonotrophic cycle (Farjana and Tuno, 2013). In adult mosquitoes, carbohydrates from nectar and honeydew have been studied as energy sources for flying in Aedes taeniorhynchus (Nayar and Sauerman, 1971) and An. gambiae (Gary and Foster, 2001, 2004). In the case of Ae. taeniorhynchus, females were supplied five days after emergence with an aqueous mixed solution 20% of test carbohydrate plus 5% sorbose (acting as phagostimulant) (Nayar and Sauerman,

1971). Mainly glucose, followed by sucrose and fructose, provided the greatest speed of flight after their ingestion, indicating their direct uti- lization (Nayar and Sauerman, 1971). Therefore, the sugar oxidation of carbohydrates gives the required energy for flight and plays a key role in flight capacity of newly emerged adults (Nayar and Handel, 1971; Nayar and Sauerman, 1971; Foster, 1995; Briegel et al., 2001). Interestingly, in the case of adult Ae. aegypti females, free amino acid proline present in hemolymph can also be used as fuel for their flight activity (Scaraffia and Wells, 2003).

Host seeking and biting behaviour after emergence is also influenced by both larval and adult diet (Klowden et al., 1988; Yee and Foster, 1992; Hancock and Foster, 1997; Gunathilaka et al., 2019). In experi- ments with Culex nigripalpus in an air-flow olfactometer, some adult mosquitoes chose to feed on plant-sugar and others on bird-blood (Hancock and Foster, 1997). Nutrition status previous to experiment determined their choice; while unfed females preferred feeding on honey rather than birds, sucrose-fed females preferred feeding on birds (Hancock and Foster, 1997). Recent emerged An. gambiae adults rapidly fed on sugar-plant to survive independently of their sex (Foster and Takken, 2004). However, five days later females switch to blood-feeding, obtaining the energy required for host-seeking activity from previous sugar-feeding (Foster and Takken, 2004). Thus, mosquito females require an initial sugar meal soon after emergence for self-maintenance, and later they can shift their feeding preferences to energetically support other activities such as reproduction. When female mosquitoes cannot get enough sugar from plants or the energy provided by carbohydrates is low, biting frequency on vertebrate increases (Fos- ter, 1995), increasing the likelihood of taking an infected-meal. This raised feeding rate on vertebrates was reported in some laboratory studies with the malaria vector An. gambiae (Straif and Beier, 1996; Gary and Foster, 2001) and the yellow fever mosquito Ae. aegypti (Canyon et al., 1999). In these experiments, mosquitoes that fed only on blood increased their biting frequency compared with diets based both on vertebrate blood and sugar. When various types of sugars were compared, sucrose was the preferred sugar providing the highest energy reserves and longevity rates (Kessler et al., 2015). In fact, increased biting behaviour was also reported when females fed on glucose instead of sucrose. To compensate for the low energetic of glucose, which only might allow basic flight activity, females would increase their host-seeking activity and biting behaviour (Kessler et al., 2015).

Depending on the time of the day, mosquitoes search for sugar-plant meals or perform a host-seeking activity (Yee and Foster, 1992). Cx. quinquefasciatus and Aedes triseriatus increased their search for a host before feeding on sugar plants in the evening, whereas in the morning Cx. quinquefasciatus presented host-seeking behaviour but not sugar-plant feeding (Yee and Foster, 1992). In the laboratory, the deprivation or intermittent access to sugar may enhance the blood-feeding activity of mosquitoes (Straif and Beier, 1996; Braks et al., 2006; Westby et al., 2016). This increase in host contacts due to the scarcity of sugar-plant meals might turn into a high probability of transmission of vector-borne diseases (Gary and Foster, 2001). Although this extreme has been studied in laboratory

conditions, it is still poorly studied under field conditions (Sissoko et al., 2019). Higher metabolic reserves in large females lead to longer flights that increase the possi- bility of encountering more hosts (Nasci, 1986). As a result, flight ac- tivity associated to mosquito nutritional status in both larval and adult stages may have epidemiological consequences. In urban habitats where arbovirus outbreaks are common, the intensity of Ae. aegypti searching for a host depends on the abundance or scarceness of sugar meals (Sis- soko et al., 2019). Therefore, the absence of preferred plants may pro- long gonotrophic cycles and reduce female necessity of human blood, consequently reducing pathogen transmission (Gary and Foster, 2001; Gu et al., 2011).

3.2. Nutritional status of mosquitoes and its effects on longevity

As stated before, some species of plants proportionate more nutri- tional energy (i.e. sugars) than others to mosquitoes. Mosquitoes have thus developed a preference to feed on these plants. Laboratory and field studies show that feeding on preferred plants results in a higher lifespan (Manda et al., 2007a; Gu et al., 2011; Yu et al., 2016). For example, An. gambiae that had access to preferred plants, such as Tecoma stans and Senna didymobotrya, showed longer survivorship and laid more eggs than mosquitoes that fed on other plant species (Manda et al., 2007a). An. sergentii (Gu et al., 2011) and Cx. pipiens pallens (Yu et al., 2016) mosquitoes exhibited higher longevity rates when feeding on the plants they prefer than when feeding in areas without these plants. Consequently, mosquitoes are more likely to feed on specific plants to obtain compounds which supply them with the highest energy and enhance their fitness (Gouagna et al., 2014). Nonetheless, despite the need and benefits of feeding on plant sugars, their diets will be short of some nutritional components. As example, Cx. quinquefasciatus females that fed on carbohydrates and amino acids had a 5% longer lifespan than females that fed only on carbohydrates (Vrzal et al., 2010).

Under laboratory conditions, researchers have used various sub- stances to feed adult mosquitoes including glucose, fructose or sucrose at different concentrations ranging from 1% to 50% (Briegel et al., 2001; Gary and Foster, 2001; 2004; Okech et al., 2003; Impoinvil et al., 2004; Braks et al., 2006; Vaidyanathan et al., 2008; Ng’habi et al., 2008; Qualls et al., 2013; Takken et al., 2013; Guti errez-Lo pez et al., 2019). Some authors used other sources such as 10% corn syrup (Straif and Beier, 1996) or fruit juices and honey (Imam et al., 2014). These different concentrations and substances may impact the life history traits of mosquitoes differently. However, studies comparing what is the impact of feeding different sugar concentrations on mosquito life history are scarce. As seen in laboratory experiments, the incorporation of sugar from plants as well as vertebrate blood in mosquito diet increases their longevity (Nayar and Sauerman, 1971; Gary and Foster, 2001; Braks et al., 2006). For example, Ae. aegypti females with single or no access to blood-meals survived 30–40% longer than females with weekly access to blood (Joy et al., 2010). In the case of Ae. albopictus survivorship also increased when feeding on blood and 10% sucrose solution diet (Xue et al., 2010). An. gambiae females with access to blood and feeding on 10% corn syrup solution

lived on average 3 days longer than those without sugar (Straif and Beier, 1996). In a semi-field study conducted with females of this species, individuals lived 33 days when fed with blood and sugar (6% glucose solution), 29 days when fed with sugar and 14 days when fed with blood alone (Okech et al., 2003). In addition, the effect of the mosquito diet during the adult stage may revert its nutri- tional status from the previous phase. For example, Culex and Aedes mosquitoes reared under nutrient-deprived larval conditions have longer survival when they accessed a rich adult diet (Vrzal et al., 2010; Xue et al., 2010).

Finally, diet may also have synergistic effects on other variables such as immune system development that may affect mosquito’s fitness and their response to exposure and transmission of different pathogens (Muturi et al., 2011; Ponton et al., 2013; Sangare et al., 2014). The ef- fects of adult diet on the longevity of mosquitoes may have a consid- erable impact on the transmission of vector-borne diseases because vector survival plays a key role in vectorial capacity by increasing the transmission of vector-borne pathogens (Smith and McKenzie, 2004; Smith et al., 2012).

4. The effect of diet on mosquito - pathogen interactions

It is widely recognized that pathogens can alter their vector and final hosts’ fitness in many ways, although the underlying mechanisms are not completely understood (Hurd et al., 2005). After the ingestion of an infected blood meal, pathogens develop inside the mosquito’s body to reach the salivary glands, where they accumulate until new blood feeding events happens (Girard et al., 2004; Valkiunas, 2005). Then, female mosquitoes transfer pathogens to a new host through their saliva, and depending on vector’s species preferences they will feed on different species of vertebrates (Takken and Verhulst, 2013; Martínez-de la Puente et al., 2015). Factors like vector longevity and nutritional status (Lambrechts et al., 2006; Vaidyanathan et al., 2008; V ezilier et al., 2012; Ponton et al., 2013; Lalubin et al., 2014; Linenberg et al., 2016), mos- quito immune condition (Sheldon and Verhulst, 1996; Koella and Sørensen, 2002; Hillyer, 2010; Muturi et al., 2011; Delhaye et al., 2016) or contact rates between mosquitoes and infected vertebrates (Cohuet et al., 2010) may have large impacts on pathogen transmission because they affect estimates of vectorial capacity as suggested in several Plasmodium-Anopheles assemblages (Araújo et al., 2012; Takken et al., 2013; Shapiro et al., 2016; Vantaux et al., 2016a).

Nutrition deprivation might increase the susceptibility to arbovirus infection on Ae. aegypti (Nasci and Mitchell, 1994; Muturi et al., 2011) and Ae. triseriatus (Grimstad and Walker, 1991). In other words, larvae reared under starvation conditions might result in adults more suscep- tible to infection when exposed to pathogens. This is because these larvae invest the available energy in survival and development instead of defence and immunity (Muturi et al., 2011; Moller-Jacobs et al., 2014). Large adults from well-nourished larvae usually possess more metabolic reserves than their small counterparts (Takken et al., 1998; Vrzal et al., 2010). These reserves allow them to fight against parasites and avoid its infection cost in

comparison with smaller females (Vai- dyanathan et al., 2008; Ponton et al., 2013). For instance, nutrient-deprived larvae of Ae. triseriatus had a large vectorial capacity for La Crosse Virus (Grimstad and Walker, 1991). Ae. aegypti adults with low access to nutrients during the larval stage showed an increased infection rate when exposed to Sindbis virus in comparison to adults metamorphosed from larvae with optimal access to nutrients (Muturi et al., 2011). Moreover, Ae. aegypti adults derived from larvae from treatments with low-insect detritus related to a high nitrogen percent presented the greatest rates of infection and dissemination of Zika virus (Paige et al., 2019). The impact of nutritional deprived diets of mosquito larvae on their vectorial capacity through the effects of body size in adults was reported using different mosquito-pathogen assemblages (Table 1). However, we do not know much about the effects of larvae diet on the susceptibility to infection in adult mosquitoes since the studies have provided contradictory results. To help clarify this issue, further analysis of the effects of larval diet on the susceptibility of mosquitoes to pathogen infection need to be carried out. In general, the conditions used in these studies are non-natural (Ferguson and Read, 2002a), thus not necessarily representing range of conditions found in the wild. Alongside to the effects derived from nutritional deprived conditions of larvae, the interaction between mosquito-pathogen species might have substantial consequences for their susceptibility to infection and vectorial capacity.

In the adult stage after pathogen infections, the development of pathogens in mosquitoes and subsequent consequences (e.g. effects on vectorial capacity related to longevity) can be determined by mosquito nutritional status as some studies suggested (Table 2). A longer mosquito’s lifespan allows pathogens to develop inside the vector, and an increase in the number of infective bites on hosts increasing pathogen transmission (Ferguson and Read, 2002b). This is the case for avian Plasmodiumspp.inCx.pipiensmosquitoes(V ezilieretal.,2012). Regarding the effects of diet on susceptibility to infections, dissemina- tion and transmission rates, different results have also been reported (Vaidyanathan et al., 2008; Gu et al., 2011; Westby et al., 2016). For instance, Cx. pipiens pipiens adults fed with different concentrations of sucrose (ranging from 2% to 40%) did not differ in their susceptibility to West Nile virus infection (Vaidyanathan et al., 2008). Despite that, those fed on the lower doses of sucrose (2% and 10%) transmitted the virus better than individuals fed on a 40% sucrose diet (Vaidyanathan et al., 2008). Ae.

albopictus that were deprived during 72 h from feeding on 20% sucrose solution did not show an increase of La Crosse virus infection compared with no food deprived ones (Westby et al., 2016).

The life cycle of pathogens in vectors differs between organisms, and mosquitoes use different immunological pathways to fight against in- fections (Barillas-Mury et al., 2000; Koella and Sørensen, 2002; Hillyer, 2010; Muturi et al., 2011; Telang et

al., 2011; Ariani et al., 2015; Del- haye et al., 2016). These immunological responses are energetically costly. As a result, a trade-off with energetic resources available for other functions is expected to occur (Sheldon and Verhulst, 1996; Fer- guson and Read, 2002a; Hurd et al., 2005), especially on fecundity and survival (Ferguson et al., 2006; V ezilier et al., 2012; Delhaye et al., 2016; Vantaux et al., 2016a). For example, An. coluzzi females infected by P. falciparum and those exposed but no infected, presented a reduced survival rate when sugar was unavailable after an infectious blood meal (Sangare et al., 2014). Similarly, differences in survival of wild trapped Cx. pipiens naturally infected by avian Plasmodium parasites and unin- fected mosquitoes were only apparent when keep in the laboratory on a low glucose concentration diet (2%) but not when kept on a higher glucose concentration diet (6%, Lalubin et al., 2014). In An. stephensi infected with the rodent malaria parasites Plasmodium yoelii mortality was higher in mosquitoes with 2% glucose solution diet in comparison with those fed on 4% or 6% glucose solutions (Lambrechts et al., 2006). The differences in mortality between 2% and 4–6% diets were also significant in control non infected mosquitoes, but the interaction be- tween infection status and glucose concentration indicated that mor- tality of infected mosquitoes was disproportionally high in low glucose conditions (Lambrechts et al., 2006). In the case of An. gambiae, the type of diet (blood or sugar) did not influence oocyst infection rate after feeding on humans infected by P. falciparum. However, female mosquitoes that received two instead of a single bloodmeal before exposure to infected blood presented higher oocyst infection rates (Okech et al., 2004). An. gambiae feeding on sugar-rich plants had the highest survivorship and lowest biting rates, decreasing the vectorial capacity of females (Stone et al., 2012). However, other field experi- ments with An. sergentii (Gu et al., 2011; Beier et al., 2012) and meso- cosm experiments with An. gambiae (Ebrahimi et al., 2019) concluded that vectorial capacity increased when feeding in sugar-rich plants. This contradiction is due to the higher densities and survival rates of mosquitoes in rich-sugar environment among experiments (Beier et al., 2012), although daily biting rates presented no significative results (Ebrahimi et al., 2019) or were greater than in poor-sugar sites (Gu et al., 2011). This summarizes the contradictory results of studies analyzing the contribution of sugar-rich plants to vectorial capacity, and showing that some assemblages are more favourable to pathogen transmission than others (Hien et al., 2016). For example, when compared to mosquitoes fed on 5% glucose solution, feeding on Thevetia neriifolia plants reduced P. falciparum transmission up to 30%. In contrast, feeding on Barleria lupilina and Lannea microcarpa transmission increased 40% and 30%, respectively (Hien et al., 2016). In consequence, there is still much to understand about the potential effects of natural variation in adult diet on vector’s susceptibility to pathogen infections and their vectorial capacity.

In summary, an impact of parasite infection on longevity and fecundity of mosquitoes is expected, especially in nutritionally stressed mosquitoes (Lambrechts et al., 2006; Lalubin et al., 2014; Sangare et al., 2014). The vectorial capacity is determined by a great variety of intrinsic traits, largely affected by extrinsic factors, including the nutritional status. In epidemiological models, the

basic reproductive number (R0) is the most widely used estimate of vectorial capacity. R0 is described as the total number of secondary infections from an original infected host (Smith et al., 2012). It is a complex rate determined by several parameters which differ depending on the vector-host system and others that are strongly influenced by environment. In models for malaria transmission, R0 is determined by factors including the daily vector survival rate, the pathogen development time inside vector or the probability of mosquitoes to be infected after taking an infected blood meal (MacDonald, 1956). These factors may largely be affected by the nutritional status of mosquitoes (Gary and Foster, 2001; Sangare et al., 2014; Kessler et al., 2015).

5. Knowledge gaps and future research lines

A major caveat in understanding the effect of diet on mosquito life cycle is that often mosquitoes are reared in the laboratory under optimal conditions, and experiments do not include a relevant number of factors that affect mosquitoes in the field (Dodson et al., 2012; Kang et al., 2017). For example, the developmental time of larvae is an important factor to consider when understanding how the phenotype of adult insects varies under different habitat conditions (Muturi et al., 2011; Yoshioka et al., 2012; Couret et al., 2014). Another factor is the diet used in the experiments. Different artificial diets are commonly used by re- searchers although their composition and effects are not completely identified. These diet regimens are commonly composed of a variety of essential (amino acids, water-soluble vitamins, nucleotides and choles- terol) and beneficial compounds like sugar (glucose, sucrose or a mixture of both) or agarose (optimizes drinking as diet is often liquid) (Merritt et al., 1992). Commonly used larval diets are based on ground or dried fish food (Sumanochitrapon et al., 1998; Araújo et al., 2012; Jannat and Roitberg, 2013) and Tetramin Baby® fish food (Foster and Takken, 2004; Okech et al., 2004; Takken et al., 2013; Vantaux et al., 2016a, 2016b; Hauser et al., 2020) that may differ in their effects on mosquitoes. This was demonstrated by Linenberg et al. (2016) in a comparative study with two common diets used in the laboratory based in fish-pellets (Dr. Clarke’s Pool Pellets and Nishikoi Fish-Pellets) and other based on fish-flakes (Tetramin® Fish-Flakes). In this study, larvae of An. coluzzii fed with the pellet diets grow and developed faster than those fed with fish-flakes, despite their similar protein and fat content. These results may be based on unknown concentrations and components of the diets, as commercial diets sometimes lack information for some ingredients. In the case of Ae. aegypti males, both carbohydrate-rich and protein-rich larval diets in combination with different temperatures affected several life-history traits of mosquitoes (Sasmita et al., 2019). Part of the problem is also the scarcity of information about feeding preferences and larvae behaviour in the field (Merritt et al., 1992; Fos- ter, 1995) when establishing laboratory conditions expecting to simulate real situations (Kang et al., 2017). Recent contributions of larval nutrient stoichiometry (Paige et al., 2019) and a study of effects of mi- croorganisms present in organic field detritus (Souza et al., 2019) are helping to clarify this issue. Characterizing realistic ranges of variation in diet composition in the field is necessary.

As for adults, accurate information of the ecological consequences for energy from plant sugar in adult stage is lacking. Mosquitoes tend to feed on plants with the greatest proportion of sugar in their flowers or stems (Manda et al., 2007b; Ebrahimi et al., 2019) that supply them a high level of metabolic energy (Gouagna et al., 2014). The modification of a natural plant-vector assemblage, such as by the introduction of invasive plants with a major nectar-production, may lead to an increase in the vectorial capacity of mosquitoes (Ebrahimi et al., 2019). However, the potential for reducing vectorial capacity and probably mosquito survival through manipulation of plant species composition remains untested. Future studies should focus on how relevant sugar diet is on adult stage life cycle, and how this could affect their fitness and vectorial capacity by altering survival and biting behaviour.

In addition, the effects of mosquito diet on mosquito-pathogen in- teractions may be indirectly driven by other factors such as mosquito gut microbiota. It has been recently postulated that midgut microbiota in- creases the fitness of mosquitoes by preventing pathogen infections (Dong et al., 2009; Ramirez et al., 2012; Z el e et al., 2012; Linenberg et al., 2016). For example, adults of An. coluzzi grown with a low-caloric diet when larvae harboured lower quantities of Enterobacteriaceae in their midgut microbiota and presented a higher intensity and prevalence of Plasmodium berghei infection after exposure to the pathogen (Linen- berg et al., 2016). Nevertheless, effects of diet on gut microbiota are largely unknown. Overall, midgut microbiota has been investigated in infected or uninfected mosquitoes of species like Cx. pipiens (Z el e et al., 2012; Martínez-de la Puente et al., 2021), An. gambiae (Dong et al., 2009) and several species of Aedes (Ramirez et al., 2012; Muturi et al., 2016). However, the effects that variation of nutritional status can produce in their resistance to infection has not been considered. Therefore, it is necessary to analyse the interaction between diet and gut microbiota and the direct and indirect effects on vectorial capacity mediated by gut microbiota.

6. Concluding remarks

Different factors may have a major incidence in mosquito-borne disease transmission. In recent years, an increasing number of studies help to clarify the role of access to nutrients on both larval and adult mosquito’s traits. These studies also help the study of disease ecology, as they focus primarily on the potential consequences for vector-borne pathogens transmission. However, the majority of the factors studied have been tested in isolation ignoring the potential synergistic in- teractions between them, which could potentially explain the differ- ences in the results. In addition, despite recent studies, there is still little information available on the mechanisms underlying the effect of adult diet on the vectorial capacity of mosquitoes. Longevity, body size and biting frequency of infected mosquitoes have a large impact on pathogen transmission dynamics, traits that are greatly influenced by the avail- ability of food. Future research on adult nutrition of mosquitoes should consider natural variation in diet quantity and composition in order to improve our understanding of the impact on vectorial capacity. Overall, understanding better the nutritional needs of vectors will allow us to develop new approaches to fight against vector-borne pathogens.

Funding

This study was funded by the project PGC2018-095704-B-I00 from the Spanish Ministry of Science and Innovation. M.J.R-L was supported by the program H2020 -MSCA-IF (H2020-MSCA–IF–2017-795537- TransWNV). This study was partially funded by a 2017 Leonardo Grant for Researchers and Cultural Creators, BBVA Foundation to J.M.-d.l.P. The BBVA Foundation accepts no responsibility for the opinions, state- ments and contents included in the project and/or the results thereof, which are entirely the responsibility of the authors.

Author contributions

L.C-L wrote the first original draft of the manuscript and subsequent versions with considerable assistance from J.M.-d.l.P., M.J.R-L and J.F. All authors contributed to manuscript revision.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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