Mosquito community composition shapes virus prevalence patterns along anthropogenic disturbance gradients

A major challenge in understanding the emergence of infectious disease is to identify the driving factors responsible for changes in infectious disease dynamics. New infectious diseases mostly emerge in tropical regions that have undergone strong ecological and economic change (Swei et al., 2020). Tropical rainforests are terrestrial ecosystems with a high biodiversity, constituting a habitat with a diverse range of hosts and pathogens. This high host richness likely corresponds to a high pathogen richness as each host is likely to carry its own specific pathogens (Dunn et al., 2010). Pristine rainforests are subject to large scale anthropogenic land use transformation leading to increased contact among humans, wildlife, and pathogens (Keesing et al., 2010; Olival et al., 2017). Disturbed habitats often show a drastic decline in biodiversity or turnover of host species community composition, which is accompanied by an increase of species that are resilient to disturbance, so-called generalist species. How changes in community composition influence pathogen prevalence in target hosts is still unclear and a matter of scientific debate (Randolph and Dobson, 2012).

In this context, the dilution effect hypothesis postulates that a high diversity of different host species dilutes the prevalence of a specific pathogen in intact ecosystems as the density of competent hosts (hosts that contribute to pathogen transmission and maintenance) is diluted by the presence of non-competent hosts. Biodiversity loss increases the infection prevalence of this specific pathogen in the disturbance-resilient, competent host species (Ostfeld, 2017). Prerequisites for the occurrence of a dilution effect are the presence of species that differ in their susceptibility for a particular pathogen and a lower risk of extinction of competent hosts under habitat disturbance. This may then lead to a higher relative frequency of competent host species in modified habitats (Halliday et al., 2017; Joseph et al., 2013; Ostfeld and Keesing, 2012). Hence, in the case of zoonotic pathogens, the disease risk for humans is increased (Ostfeld, 2017; Gibb et al., 2020). Studies confirming the dilution effect hypothesis focused on pathogens known to cause outbreaks in humans and livestock (e.g. West Nile virus [WNV], Sin Nombre virus, and Borrelia spp.) and use generalist species as hosts (Allan et al., 2009; Clay et al., 2009; Ostfeld and Keesing, 2000; Khalil et al., 2016). However, it seems that this effect cannot be generalized and that diverse mechanisms regulate infectious disease transmission dynamics in a host-, pathogen-, and situation-dependent manner (Guo et al., 2019; Johnson et al., 2015b). Some studies observed a contrary effect for WNV, Usutu virus, and Borellia spp., where the infection rate or density of infected hosts increased with biodiversity, referred to as amplification effect (Levine et al., 2017; Ruyts et al., 2016; Roiz et al., 2019).

These conflicting results indicate that biodiversity loss has complex impacts on disease risk and effects can be heterogeneous and scale-dependent (Johnson et al., 2015b; Keesing et al., 2006; McLeish et al., 2017; Salkeld et al., 2013). Partial views on single host species or single pathogens cannot reveal general mechanisms. Existing studies either focused only on pathogen discovery aside from an ecological context or on one specific pathogen in a specific host across different habitats (Clay et al., 2009; Ostfeld and Keesing, 2000; Levine et al., 2017; Shi et al., 2016). Studies with a wider scope analyzing community composition of entire host groups and assessing the genetic diversity of their pathogens in undisturbed and disturbed habitats are lacking and would be paramount for a comprehensive understanding of biodiversity-infection relationships. To this end, analyzing species interactions is crucial for a mechanistic understanding of the factors governing emerging infectious diseases (Johnson et al., 2015a).

Here, we provide a comprehensive analysis combining fields of community ecology and virology to understand how viral richness depends on host richness, and which role host–habitat associations play for viral abundance patterns using viruses that naturally infect mosquitoes in a natural system. Habitat alterations such as agricultural development and urbanization promote thriving of disease-transmitting mosquito species (Burkett-Cadena and Vittor, 2018; Lee et al., 2020; Perrin et al., 2022; Perrin et al., 2023; Schrama et al., 2020), but it is less clear how such changes in mosquito species disassembly affect the abundance and prevalence of viruses. From the limited amount of available studies, these mostly focused on the effects of land use change on one specific virus (Ferraguti et al., 2021; Gardner et al., 2014; Martínez-de la Puente et al., 2018). In addition to the vertebrate-pathogenic arthropod-borne viruses (arboviruses), for example, dengue virus (DENV), yellow fever virus (YFV), and Zika virus (ZIKV) (Gould et al., 2017; Weaver et al., 2018a), mosquitoes can also be infected with so-called insect-specific viruses (ISVs), which cannot infect vertebrates due to several host restriction barriers, for example, sensitivity to higher (body) temperatures and inability to replicate in vertebrate cells (Blitvich and Firth, 2015; Marklewitz et al., 2015). All arbovirus taxa are embedded in a much greater phylogenetic diversity of ISVs, which suggests that arboviruses evolved from ancestral arthropod-restricted viruses (Blitvich and Firth, 2015; Marklewitz et al., 2015; Halbach et al., 2017; Junglen, 2016). The mode of transmission of most ISVs in nature remains largely unknown but is suggested to rely on direct transmission. For some insect-specific flaviviruses, vertical transmission to the progeny was described and is considered to play an important role for virus maintenance in nature (Blitvich and Firth, 2015; Bolling et al., 2012; Cook et al., 2006; Lutomiah et al., 2007). Additional transmission mechanisms of ISVs may include shared food sources, ectoparasites, or venereal transmission (reviewed in Halbach et al., 2017; Agboli et al., 2019; Meki et al., 2021). It has been shown that at least some flavi-, mesoni, and bunyaviruses are expectorated during feeding, which may provide a route for horizontal virus transmission (Birnberg et al., 2020; Gaye et al., 2020; Newton et al., 2020; Ramírez et al., 2018). However, transmission dynamics may differ among virus species and viral families and data are lacking describing the maintenance and transmission of ISVs related to arboviruses (Meki et al., 2021). Knowledge of the natural transmission of ISVs has been mainly studied for entomopoxviruses and baculoviruses, which infect other insects than mosquitoes (Ma et al., 2021). Due to their high abundance in natural mosquito populations, ISVs can serve as model systems to study how changes in mosquito species assembly affect associated virus abundance.

In a preliminary analysis, we had demonstrated that the prevalence of three ISVs, isolated from mosquitoes sampled along an anthropogenic disturbance gradient in Côte d’Ivoire, West Africa, increased from pristine to disturbed habitat types (Junglen et al., 2009b; Zirkel et al., 2011). Subsequently, a plenitude of previously unknown RNA viruses was identified in these samples establishing novel species, genera, and even families (Marklewitz et al., 2015; Zirkel et al., 2011; Hermanns et al., 2017; Hermanns et al., 2014; Junglen et al., 2009a; Junglen et al., 2017; Kallies et al., 2014; Marklewitz et al., 2011; Marklewitz et al., 2013; Quan et al., 2010; Zirkel et al., 2013; Schuster et al., 2014). To this end, we established broad-range generic PCR assays for all viruses identified previously in these samples, as well as for all major virus taxa containing arthropod-associated viruses. With this, we aimed to assess the viral genetic diversity along with the prevalence patterns of each detected virus in an entire family of hosts (Culicidae) sampled across habitat types. We expect a higher species diversity in mosquitoes of the family Culicidae in habitats of low or no disturbance and predict a turnover in mosquito species composition along the disturbance gradient concomitant with an increase in disturbance-resilient mosquito species and their viruses. We thus hypothesize that habitat perturbation and subsequent changes in community composition influence virus abundance patterns and most likely transmission dynamics. This multi-host and multi-taxa study provides insight into common and distinct micro-evolutionary patterns of virus emergence and geographic spread at the interface of pristine and modified landscapes.

In this study, we analyzed the interplay between host community composition, habitat disturbance, and virus prevalence in a multi-host and multi-taxa approach. We characterized the genetic diversity of RNA viruses (multi-taxa) in an entire family of hosts (Culicidae; multi-host), which were sampled along an anthropogenic disturbance gradient. We subsequently studied prevalence patterns of all detected viruses per habitat type, as well as mosquito community composition per habitat type. We discovered an exceptionally high diversity of 49 distinct viruses, of which 34 were previously unknown members of seven different RNA virus families. We demonstrated that the majority of these viruses occurred at low minimum infection rates (MIRs) of 0.22–1.97 infected mosquitoes per 1000 tested mosquitoes. Nine viruses occurred more frequently across the disturbance gradient, of which five increased in prevalence from pristine to disturbed habitat types. We could show that the detection rates of these viruses corresponded to the abundance patterns of their specific mosquito host species. Importantly, the differences in virus prevalence were driven by the number of hosts present in a specific habitat type and not by changes in host infection rates. This interplay was named abundance effect. These data show that host community composition critically influences virus prevalence that has direct impact on our understanding of infectious disease emergence mechanisms.

The majority of the detected viruses grouped with ISVs in phylogenetic analyses, suggesting that vertebrates do not participate in their amplification and maintenance cycles. However, the novel viruses Cimo peribunyavirus I and II formed a monophyletic clade that shared a most recent common ancestor with viruses of the genera Orthobunyavirus and Pacuvirus. Orthobunyaviruses are arboviruses that infect a great variety of vertebrates including humans (Hughes et al., 2020). Pacuviruses were isolated from rodents and phlebotomine sandflies in Brazil (Aitken et al., 1975; Rodrigues et al., 2014). Thus, the amplification cycle of Cimo peribunyavirus I and II may involve vertebrates and may be more complex than that of the other detected viruses. Further research is necessary to assess the host range of Cimo peribunyavirus I and II. The ISVs detected here were previously unknown, and it is thus not known whether they are viral symbionts of mosquitoes or pathogenic viruses. Since these represent previously unknown viruses, no study investigating whether they induce symptoms of disease and/or influence life history traits of mosquitoes has been conducted. Either way, the study provides data for a better understanding of factors influencing the viral community composition of mosquitoes. Although the microbiome of invertebrates is widely unexplored, it has been shown that the microbiome of mosquitoes can have a negative effect on its vector competence (the ability of mosquitoes to transmit human- and livestock pathogenic viruses). In consequence, even if the viruses detected in this study would be symbionts of mosquitoes, they may affect the transmission efficiency of pathogenic viruses and affect spillover events of pathogenic arboviruses from sylvatic to urban cycles. Nevertheless, studying abundance patterns and geographic spread of ISVs in the light of habitat disturbance and shifts in host community composition can provide valuable insight into infectious disease dynamics, at least for directly transmitted viruses. Mosquito-borne viruses are among the major global health concerns, and the recent spread and epidemics caused by Zika and chikungunya viruses have exemplified that there is an urgent need to understand viral emergence processes (Weaver et al., 2018a). Using mosquito-specific viruses as model viruses has many advantages as these viruses are more frequently found than arboviruses and no vertebrate host is required for virus maintenance and amplification, which makes links between host community composition and virus abundance patterns easier to identify. Mosquitoes and their viruses are an ideal system to study such effects as this allows studying infectious disease dynamics in an entire family of hosts, which can be tested in high numbers.

Our observed virus prevalence patterns are in agreement with several studies stating a heterogeneous effect of biodiversity on pathogen prevalence or disease risk (Randolph and Dobson, 2012; Salkeld et al., 2013). Biodiversity can influence disease risk by different mechanisms like host regulation, changes in encounter rates or transmission rates, leading to an amplifying or diluting net effect (Keesing et al., 2006). Areas with a high host richness likely harbor a high pathogen richness that might act as a source pool of novel diseases upon habitat change and increased contact to humans (Dunn et al., 2010; Keesing et al., 2010). We observed the highest virus richness in intermediately disturbed and primary rainforest habitats supporting that biodiverse habitats are also rich in pathogens. However, highest viral prevalence rates were observed in villages and at camp sites, further supporting that intact or intermediately disturbed ecosystems also contain well-balanced spectra of viruses.

For those arboviruses that are transmitted by a generalist mosquito species and use a competent host profiting from disturbance, a dilution effect can occur at local scales (Halliday et al., 2017; Ostfeld and Keesing, 2012). Several studies observed a dilution effect for WNV with either increasing non-passerine or total bird diversity (Allan et al., 2009; Ezenwa et al., 2006; Swaddle and Calos, 2008) while others reported no protective effect of avian species richness on WNV prevalence (Levine et al., 2017; Loss et al., 2009). For tick-borne encephalitis virus, a dilution effect with increasing density of incompetent deer hosts was observed at local scale (Cagnacci et al., 2012). Likewise, the prevalence of the directly transmitted hantavirus sin nombre virus is reduced at sites with higher rodent diversity as the persistence of the main host species (deer mouse) is reduced at diverse sites (Clay et al., 2009). A similar pattern was observed in our sampling for the five viruses GOLV, HEBV, FERV, Spilikins virus, and CAVV belonging to four different families (Phenuiviridae, Peribunyaviridae, Phasmaviridae, and Mesoniviridae). All these viruses used mosquitoes of the species C. nebulosus as primary host, which seemed to profit from disturbance and increased in abundance in disturbed versus pristine habitats (38% vs. 3%).

The ecological mechanisms leading to changes in mosquito community composition due to anthropogenic disturbance are presently poorly understood. Environmental changes, including land use changes, but also changes in the host species composition have been suggested to act as drivers of vector-borne diseases, including important arboviral diseases like dengue (Patz et al., 2000; Takken and Verhulst, 2013; Young et al., 2017). Yet, very few studies have focused on C. nebulosus. It has been reported as a sylvatic species in Nigeria, Benin, and Mozambique (Abílio et al., 2020; Agwu et al., 2016; Lingenfelser et al., 2010), but to the best of our knowledge this is the first study showing an increasing abundance of C. nebulosus in modified ecosystems. The possible reasons for the varying mosquito community compositions in the different habitat types might be the availability of suitable larval habitat sites and food sources, the abundance of predators, as well as differences in temperature and humidity (Ferraguti et al., 2016; Roiz et al., 2015; Thongsripong et al., 2013).

The prevalence of the five viruses associated with C. nebulosus was reduced in the diverse habitat types where the abundance of incompetent mosquito hosts increased and C. nebulosus was rarely found. It is striking that this effect was observed for five taxonomically different viruses infecting the same host species. This effect was not observed for closely related viruses using other mosquito species as host that did not increase in abundance in disturbed habitats. These data suggest that the adaptability of mosquito hosts to changed environments plays a more important role for the increase in prevalence of associated viruses than the phenotypic or genetic characteristics of these viruses. A similar observation was made by another study, which showed that the virome composition of three mosquito species captured along a rural to urban disturbance gradient in Thailand was defined primarily by the mosquito host species rather than the geographic location and that ISVs display a relatively narrow host range (Thongsripong et al., 2021).

Contrary effects can be caused by scale-dependent effects or depending on additive or substitutive community assemblies (Johnson et al., 2015b). Additionally, the most competent host can either increase or decline with disturbance, leading either to a dilution or amplification effect, respectively (Halliday et al., 2017). In our investigated sample set, two viruses (Cimo phenuivirus II, family Phenuiviridae, and Cimo flavivirus I, family Flaviviridae) with higher prevalence in pristine than in disturbed habitats were detected. As observed for the five viruses mentioned above (GOLV, HEBV, FERV, Spilikins virus, and CAVV), virus prevalence rates were closely linked to abundance rates of host mosquito species. Cimo phenuivirus II and Cimo flavivirus I were associated with Uranotaenia and Coquillettidia mosquitoes that declined in abundance in disturbed habitat types. An explanation of why such an effect is rarely found could be that model pathogens selected in the field of disease ecology are usually zoonotic pathogens that infect humans in disturbed habitats and are known to cause outbreaks. Thus, there may exist a bias towards those pathogens that thrive in disturbed habitat types. Pathogens that are rarely found in disturbed habitats may never be selected for disease ecology studies. Notably, the vast majority of detected virus species showed low infection rates without any evidence for effects of mosquito community changes on their abundance. These findings for 40 (out of 49) distinct viruses infecting different mosquito species suggest that host community disassembly does only influence a small fraction of the pathogen population. These examples underline why an unbiased multi-host and multi-taxa approach is crucial to uncover host community effects on pathogen prevalence patterns.

In other studies focusing on plant, vector-borne, indirectly and directly transmitted pathogens, the composition of the host community rather than total biodiversity was a predictor for pathogen distribution (Randolph and Dobson, 2012; McLeish et al., 2017). For example, (i) a low diversity of grassland plant species diversity was associated with a higher abundance of fungal plant pathogens (Mitchell et al., 2002), (ii) the disease and infection risk of populations of wild pepper (chiltepin) with different viruses increased with the level of human management, which was associated with decreased species diversity and host genetic diversity, and increased host plant density (Pagán et al., 2012), and (iii) the prevalence of four generalist aphid-vectored pathogens (barley and cereal yellow dwarf viruses) increased in grass host plants as local host richness declined, indicating that virus incidence in the focal host species is affected by the composition of the entire host community rather than by dependence on species diversity (Mitchell et al., 2002; Pagán et al., 2012; Lacroix et al., 2014). This is in agreement with the strong observed association between the prevalence of a certain virus and the abundance of its main mosquito host species in our study.

We detected novel strains of two previously characterized viruses, PCLV and Anopheles flavivirus, in A. aegypti and Anopheles gambiae mosquitoes, respectively, corresponding to previous findings of these viruses in these mosquito species in Asia and Africa (Chandler et al., 2014; Fauver et al., 2016; Zhang et al., 2018). This further supports the specific associations between certain viruses and mosquitoes on a broader geographical scale.

Mosquitoes harbor a diverse natural virome that can influence subsequent virus infections (Hall et al., 2016; Junglen and Drosten, 2013). We observed four frequently co-occurring viruses in C. nebulosus mosquitoes (GOLV, HEBV, FERV, and CAVV) that also grew together in cell culture, while in contrast the two C. decens-associated viruses, Cimo rhabdovirus I and JONV, were rarely detected together. This could hint, on the one hand, at synergistic interactions and, on the other hand, at superinfection exclusion between different ISVs in mosquitoes. For several ISVs in the genera Flavivirus and Alphavirus, an interference with related arboviruses was observed (Bolling et al., 2012; Nasar et al., 2015; Hobson-Peters et al., 2013). A better knowledge of the virome of different mosquito species as well as studies on mutual interference might help to assess vector competence and possibilities of geographic spread.

Virus detection in mosquito homogenates independent of virus isolation extents potential virus findings but has the limitation that exogenous and integrated viruses can be discovered. The detection of likely integrated sequences derived from flavi- and rhabdoviruses in our mosquito sample is in agreement with frequent previous findings of NIRVS from these families in mosquito genomes (Fort et al., 2012; Katzourakis et al., 2010; Lequime and Lambrechts, 2017; Whitfield et al., 2017). NIRVS are more closely related to ISVs than to arboviruses, probably limiting their influence on vector competence. The transovarial transmission of ISVs might increase the chance of germline integrations (Palatini et al., 2017; Olson and Bonizzoni, 2017). NIRVS can be transcriptionally active and might play a role in immunity against related viruses by producing piRNAs (Fort et al., 2012; Lequime and Lambrechts, 2017; Whitfield et al., 2017; Ter Horst et al., 2019).

Collectively, our data show that only some viruses of a huge viral community benefited from ecosystem disturbance. This effect was found for five viruses (GOLV, HEBV, FERV, Spilikins virus, and CAVV) and was determined by abundance patterns of their mosquito hosts, which profited from habitat disturbance and strongly increased in numbers from pristine to disturbed habitats. In contrast, we also detected two viruses (Cimo phenuivirus II and Cimo flavivirus I) that were associated with mosquito hosts specific to primary habitat types. Detection rates of the associated viruses were also closely linked to host abundance, and these viruses were found with higher frequencies in the primary and secondary rainforest. However, our analyses have also shown that virus prevalence is not always a consequence of the abundance of host species in a certain area. The prevalence pattern of JONV did not follow the abundance pattern of C. decens mosquitoes and its abundance seems to be determined by unknown mechanisms, possibly by superinfection exclusion mediated by Cimo rhabdovirus I. The study of prevalence patterns of a broad genetic diversity of RNA viruses and their associated hosts allowed us to seek for general mechanisms influencing emergence and geographic spread of mosquito-associated viruses. No general dilution or amplification effect was observed. Instead, we identified changes in mosquito community composition causing an increase or decrease in the main host species as the most important factor determining virus prevalence patterns, an effect named abundance effect. Remarkably, host infection rates were not affected by higher host abundance in our study.

The viral sequence fragments and genomes as well as the potential non-retroviral integrated RNA virus sequences (NIRVS) were assigned the GenBank accession numbers MZ202249–MZ202305 and MZ399697–MZ399709, respectively.

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Author details

1. Kyra Hermanns

   Institute of Virology, Charité - Universitätsmedizin Berlin, corporate member of Free University Berlin, Humboldt-Universtiy Berlin, and Berlin Institute of Health, Berlin, Germany

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Writing - original draft, Writing – review and editing

   Competing interests

   No competing interests declared

2. Marco Marklewitz

   Institute of Virology, Charité - Universitätsmedizin Berlin, corporate member of Free University Berlin, Humboldt-Universtiy Berlin, and Berlin Institute of Health, Berlin, Germany

   Contribution

   Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

3. Florian Zirkel

   Institute of Virology, University of Bonn Medical Centre, Berlin, Germany

   Present address

   Biotest AG, Dreieich, Germany

   Contribution

   Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

4. Anne Kopp

   Institute of Virology, Charité - Universitätsmedizin Berlin, corporate member of Free University Berlin, Humboldt-Universtiy Berlin, and Berlin Institute of Health, Berlin, Germany

   Contribution

   Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

5. Stephanie Kramer-Schadt

   1. Department of Ecological Dynamics, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
   2. Institute of Ecology, Technische Universität Berlin, Berlin, Germany

   Contribution

   Formal analysis, Visualization, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9269-4446

6. Sandra Junglen

   Institute of Virology, Charité - Universitätsmedizin Berlin, corporate member of Free University Berlin, Humboldt-Universtiy Berlin, and Berlin Institute of Health, Berlin, Germany

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Writing - original draft, Writing – review and editing

   For correspondence

   sandra.junglen@charite.de

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3799-6011

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