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Communication

Sex Ratio Distortion of Aedes aegypti (L.) in El Salvador: Biocontrol Implications for Seasonally Dry Urban Neotropical Environments

by
Anna M. Groat-Carmona
1,*,
Maryory A. Velado Cano
2,
Ana M. González Pérez
3 and
Víctor D. Carmona-Galindo
3,4
1
Division of Sciences and Mathematics, School of Interdisciplinary Arts and Sciences, University of Washington Tacoma, 1900 Commerce Street, Tacoma, WA 98402, USA
2
Departamento de Ingeniería de Procesos y Ciencias Ambientales, Universidad Centroamericana “José Simeón Cañas”, Blvd. Los Próceres, Antiguo Cuscatlán, La Libertad 05001, El Salvador
3
Laboratorio de Entomología de Vectores, Centro de Investigación y Desarrollo en Salud, Universidad de El Salvador, San Salvador, San Salvador 01168, El Salvador
4
Biology Department, Natural Sciences Division, University of La Verne, 1950 Third Street, La Verne, CA 91750, USA
*
Author to whom correspondence should be addressed.
Diversity 2025, 17(4), 257; https://doi.org/10.3390/d17040257
Submission received: 11 February 2025 / Revised: 28 March 2025 / Accepted: 2 April 2025 / Published: 5 April 2025
(This article belongs to the Special Issue Ecology and Diversity of Diptera in the Tropics)
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Abstract

:
Vector-borne diseases (VBDs) remain a major public health burden, particularly in tropical and subtropical regions. Aedes aegypti mosquitoes are primary vectors of several VBDs, and understanding their population dynamics is critical for developing effective control strategies. This study investigates seasonal sex ratio variation in A. aegypti populations within urban environments of El Salvador’s seasonally dry neotropical biomes. Using data from an ongoing surveillance program, we analyzed the temporal distribution of male and female mosquitoes across eight sampling events. Our results reveal significant deviations from the expected 1:1 sex ratio, with a pronounced female bias during the dry season and a shift toward parity in the wet season. These findings suggest that environmental and anthropogenic factors influence sex ratio dynamics, potentially affecting reproductive success and population persistence. The observed sex ratio distortion has important implications for vector ecology and biocontrol, emphasizing the need to incorporate seasonal and urban ecological variation into vector management strategies. Integrating these ecological insights into biocontrol programs could enhance the effectiveness of interventions aimed at reducing VBD transmission in seasonally dry tropical regions.

1. Introduction

Vector-borne diseases (VBDs), including malaria and dengue, are major global health challenges caused by microbial pathogens transmitted primarily by arthropods. Annually, VBDs account for over 700,000 deaths, with the disease burden disproportionately affecting underdeveloped nations in tropical and subtropical regions [1]. The global distribution of VBDs is shaped by a complex interplay of demographic, ecological, environmental, and social factors. More than half of the world’s population is at risk of infection by at least one vector-borne pathogen, with mosquitoes and ticks responsible for the majority of VBD cases [1]. Human activities—including global trade and travel, urbanization, changes in land use, and population growth—combined with climate change (e.g., increased temperatures, altered weather patterns, and changes in seasonal rainfall) have expanded the distribution of many vectors [2,3]. These factors are likely to accelerate the future spread of VBDs [1,4,5,6].
There are over 2500 mosquito species worldwide, with species from the genera Anopheles (subfamily Anophelinae), Culex (subfamily Culicinae), and Aedes (subfamily Culicinae) being the primary vectors of VBDs. Female mosquitoes acquire pathogens through blood meals necessary for ovulation. Vertical transmission can occur when infected females transmit pathogens to their offspring via their eggs, although the epidemiological significance of this transmission mode varies among arboviruses [7]. Once infected, mosquitoes remain infectious for life and are capable of transmitting pathogens to susceptible hosts during subsequent blood-feeds [4,5,8].
Among mosquito vectors, Aedes aegypti L. (Diptera: Culicidae) is responsible for the transmission of significant public health pathogens, including Yellow Fever, Zika, Chikungunya, and Dengue. These mosquitoes exhibit strong anthropophilic behavior, preferring to reside in human dwellings, feed primarily on human hosts, and oviposit in dark-colored, man-made water containers [1,4,5,9,10].
A. aegypti mosquitoes were introduced to the Americas in the 1600s via the transatlantic slave trade and subsequently spread globally through shipping routes [3,5,11]. Eradication efforts led by the Pan American Health Organization in the mid-20th century temporarily reduced A. aegypti populations [12]. However, reintroductions occurred through international trade, transportation networks, and human migration [4,11,13]. Presently, A. aegypti populations in the Americas exhibit higher genetic diversity compared to those in Africa or Asia [2,3], with notable variability observed in El Salvador. Studies have identified at least two genetically distinct groups in El Salvador [13]. This genetic variability is critical for developing biocontrol strategies, as different strains exhibit variation in insecticide resistance and vector competence, underscoring the importance of localized surveillance efforts [14].
The maintenance of a balanced female-to-male sex ratio (1:1) is fundamental for population dynamics in sexually reproducing species [15]. Several mechanisms contribute to sex ratio parity, including Fisher’s principle, which posits that natural selection favors a balanced sex ratio due to the selective advantage of producing the rarer sex [16,17]. Environmental factors can differentially affect male and female development, survival, and reproduction, leading to sex ratio distortions [18,19]. Sex ratio distortion in mosquito populations, particularly in A. aegypti, can reflect underlying evolutionary adaptations to environmental conditions and selective pressures [20,21].
Limited data exist on sex ratios within A. aegypti populations outside biocontrol interventions. Some evidence suggests sex ratio imbalances in tree-hole dwelling Aedes species, such as A. triseriatus and A. albopictus [22,23]. These biases, generally skewed towards males, exhibit seasonal and geographic variation, primarily documented in temperate regions like the United States and Europe [21,23,24]. Effective biocontrol strategies require comprehensive knowledge of pathogen dynamics, vector behavior, and environmental factors influencing transmission [25,26,27].
In addition to ecological and environmental drivers, sex ratio distortion may also result from molecular mechanisms, including endosymbiont-mediated reproductive interference (e.g., Wolbachia-induced cytoplasmic incompatibility), genetic incompatibilities, and sex-linked meiotic drive systems, which have been documented across various arthropod taxa [28,29,30]. While such mechanisms remain understudied in A. aegypti within tropical dry environments, they may interact with environmental conditions to influence population-level sex ratios.
El Salvador’s tropical dry forests [31,32] provide a unique context for studying these dynamics. These forests, characterized by deciduous and gallery forests [33], are highly sensitive to climatic variability. Changes in temperature and precipitation influence vegetation composition, arthropod distribution, and ecosystem dynamics [34,35]. Human reliance on water storage during droughts creates suitable larval habitats for A. aegypti, sustaining populations near human dwellings [36]. A. aegypti is a key vector species whose population dynamics are shaped by both seasonal climatic changes and anthropogenic factors [5,37]. Characterizing these dynamics is essential for understanding vector ecology in tropical dry environments, especially within the Central American Dry Corridor [33,34].
Given the paucity of data on A. aegypti sex ratios in seasonally dry tropical environments, our study addresses this critical gap by examining how drought and climate variability influence population dynamics in El Salvador. Using metadata from the Salvadoran Ministry of Health and the Centro de Investigación y Desarrollo en Salud (CENSALUD) at the University of El Salvador, we hypothesized that seasonality influences sex ratio biases. Our study aims to enhance the understanding of vector–pathogen dynamics and inform context-dependent biocontrol strategies within the Central American Dry Corridor (CADC).

2. Materials and Methods

2.1. Climate Data

To corroborate the seasonality of the tropical environment under investigation, we collected temperature and precipitation data for San Salvador, El Salvador. These data were derived from the CHELSA V2.1 database for the period between 1981 and 2010 [38]. The climate data were further used to determine the Köppen–Geiger classification [31] and the Holdridge Life Zone [32].

2.2. Site Description

Mosquito larvae were collected from urban environments within rural hamlets of El Salvador. These hamlets feature a unique blend of traditional and modern elements, complemented by diverse vegetation cover [37]. The sites typically combine small-scale agricultural activities with residential zones. The vegetation includes cultivated crops, ornamental plants, and native flora. Residents maintain gardens with fruit trees, flowering plants, and vegetables, while shade trees and hedges are commonly planted around homes and community spaces. Patches of natural vegetation, such as native trees and shrubs, are interspersed within and around these hamlets [37].

2.3. Collection of Mosquito Larvae

This study used data collected through a long-standing mosquito surveillance program coordinated by CENSALUD. Sampling was conducted opportunistically as funding and field capacity allowed, and not all sites were sampled uniformly across time.
Mosquito larvae were hand-collected during the morning and afternoon on eight sampling dates (March 2021 to September 2022) using a 30 mL plastic transfer pipette (General Mills; Minnesota, U.S.A.). Collections were made from peridomiciliary concrete water basins, locally known as pilas. These pilas are used for household cleaning and washing and are typically kept filled with water year-round in El Salvador (Figure 1).
At each sampling site, larvae were collected from a single peridomiciliary pila, rather than pooled from multiple sources, to maintain consistency in larval environmental conditions. Collected larvae were transported in pila-derived water within aerated 750 mL plastic bottles (repurposed from commercially available water bottles) to the CENSALUD laboratories. Upon arrival, larvae were transferred to plastic tray bins (27 cm × 15 cm × 9.5 cm; 4 L capacity; Dollarama; Montréal, Canada) containing 1 L of dechlorinated tap water. They were reared at temperatures ranging from 25.5 °C to 28.6 °C, with 57% relative humidity, under a 10:14 h light:dark photoperiod. Larvae were fed conventional dry cat food pellets (Nestlé Purina PetCare Company; St Louis, Missouri) daily until they reached adulthood (approximately 5 to 14 days). Adult mosquitoes were transferred to 30 cm × 30 cm × 30 cm fabric-mesh cages using a standard mouth aspirator (constructed in-house from locally available materials).
Adults were euthanized by freezing at −20 °C and their species level was identified using the Rueda [39] taxonomic key under a stereomicroscope (35× total magnification; Leica Microsystems; Wetzlar and Mannheim, Germany). A total of 576 adult A. aegypti mosquitoes were selected, representing four departments, seven municipalities, and eight hamlets across El Salvador (Table 1).

2.4. Determination of Sex

Sex determination of adult A. aegypti mosquitoes was performed using external morphological characteristics under a stereomicroscope at 35× magnification (Figure 2) [40,41]. Multiple sexually dimorphic features were assessed in tandem to ensure accurate identification, even in specimens with minor physical damage.
The proboscis was evaluated first: females exhibited a long, slender, and straight labium adapted for skin penetration and blood-feeding, while males had a slightly shorter and more flexible labium, adapted for nectar-feeding. The maxillary palps, located lateral to the proboscis, were distinctly longer and more plumose in males, contrasting with the short, less setose palps observed in females.
Antennae were also highly diagnostic. Males possessed bushy, plumose antennae, with long fibrillae extending from each flagellomere, enhancing their ability to detect female wingbeat frequencies. In contrast, females exhibited pilose antennae, with shorter and sparser fibrillae.
The terminal abdominal segments were assessed for genitalia differences. Female terminalia presented a broad, bluntly rounded 7th–8th abdominal segment, while male mosquitoes displayed a more tapered abdomen terminating in claspers (gonostyli), which are part of the external genitalia used in copulation.
In combination, these traits—proboscis length, palp morphology, antennal structure, and terminalia—allowed for accurate sex determination in all specimens used in this study.

2.5. Statistical Analyses

Sex ratio deviations from the expected 1:1 male-to-female (M:F) ratio in A. aegypti mosquitoes were evaluated using a one-factor Chi-Square analysis. Percent sampling abundance for both male and female mosquitoes was calculated relative to the total number of A. aegypti collected. The expected sampling distribution was determined by evenly distributing the total sampling abundance (100%) across the eight sampling events (12.5% per event).

3. Results

The climate diagram of San Salvador, El Salvador (Figure 2), based on long-term climatic averages from 1981 to 2010, provides a baseline for understanding the typical dry and wet seasonal cycles in this biome. Exact sampling dates and locations from 2021 to 2022 can be interpreted within the context of these broader seasonal patterns (Table 1). The climate diagram revealed a distinct seasonal pattern, with a dry season lasting approximately six months (November to April) and a wet season spanning six months (May to October). During the wet season, soil water saturation persisted for at least five months (Figure 3). The Köppen–Geiger classification confirmed this region as a tropical wet and dry climate (As/Aw), characterized by dry winters and summers [31]. Additionally, the Holdridge Life Zone classification identified this area as a tropical dry forest [32].
The sex ratio of A. aegypti mosquitoes significantly deviated from parity during the sampling period (χ2 = 108.2, p < 0.001). This deviation favored female mosquitoes, with fewer males collected during the dry season (March). However, the sex ratio shifted during the wet season (June to October), approaching parity between male and female mosquitoes (Figure 4).
The proportion of male A. aegypti mosquitoes relative to the total number sampled also differed significantly from the expected proportional abundance (χ2 = 42.5, p < 0.001). Our data suggest that male abundance remained consistently below the expected value throughout both the dry and wet seasons (Figure 5). Similarly, the proportion of female A. aegypti mosquitoes relative to the total sample size differed significantly from the expected proportional abundance (χ2 = 43.0, p < 0.001). Notably, there were more females than expected during the dry season (March), while female abundance fell below the expected proportion during the wet season (June to September) (Figure 4).
Collectively, our meta-analysis of data collected by CENSALUD on behalf of the Salvadoran Ministry of Health provides evidence of a seasonal shift in A. aegypti sex ratios. These data reflect sampling dates and locations where field activities were feasible through the CENSALUD surveillance program, during which we observed a consistent pattern of higher female abundance during the dry season in highly urbanized environments within El Salvador.

4. Discussion

Our meta-analysis reveals significant temporal variability in sex ratio distortion across A. aegypti populations. We observed a consistent seasonal shift toward female-biased populations during the dry season (Figure 4), which contrasts with male-biased patterns commonly reported in tree-hole dwelling Aedes species, such as A. triseriatus and A. albopictus [21,22,23,24]. While sex ratio deviation has been well-documented in those species, this phenomenon has not previously been demonstrated in container-breeding mosquitoes like A. aegypti. The observed distortions may reflect adaptive responses to seasonal pressures: increased female emergence during the dry season could optimize reproductive output when larval competition is reduced, whereas male-biased ratios during the wet season may enhance mating opportunities through sexual selection for larger males [4,20,21,22]. These findings expand our ecological understanding of Aedes sex ratio dynamics and reinforce the importance of integrating sex ratio surveillance into public health interventions, particularly those relying on population structures to guide biocontrol efforts [42].
This study mined data from an ongoing community-based surveillance program coordinated by CENSALUD, where mosquito collections are conducted intermittently as funding permits. As a result, sampling efforts were not uniformly distributed across sites or months. While this limits our ability to generalize findings across all regions of El Salvador, it provides valuable site- and time-specific insights into local sex ratio distortions that may inform future hypothesis-driven surveillance and control strategies. Inconsistent funding and limited infrastructure for mosquito surveillance programs in Central America—particularly in the Northern Triangle—contribute to gaps in data availability and generalizability. These same limitations are emblematic of the systemic neglect that characterizes many vector-borne diseases in the region. We hope that this study, while based on a constrained dataset, may help inform and advocate for more robust and sustained surveillance efforts moving forward.
Our sampling strategy—collecting larvae from a single pila per site—ensured consistency in larval environmental conditions, allowing us to control for microhabitat-level variation. However, this design may limit the generalizability of our findings, as it does not capture intra-hamlet heterogeneity in container types, water quality, or mosquito breeding dynamics. Additionally, the modest sample sizes in this pilot study reflect data mining from an opportunistically funded surveillance program, rather than a comprehensive, year-round sampling effort. While these limitations constrain the statistical generalizability of our findings, the observed female-biased patterns—especially during the dry season—align with independent field observations reported by the World Mosquito Program in El Salvador (personal communication). This convergence lends external validity to our findings and supports the need for further hypothesis-driven research on Aedes sex ratio dynamics in seasonally dry tropical regions.
Male Aedes eggs typically hatch early in the rainy season, and male larvae develop faster than females [4,24]. However, adult males have significantly shorter lifespans (8–10 days) compared to females (4–6 weeks, depending on environmental conditions). Male-biased sex ratios in Aedes mosquitoes have been linked to sexual selection, where larger males are better able to compete for early-emerging, nulliparous females during the rainy season [21]. This dynamic can shift toward parity as the rainy season progresses and favor smaller, late-emerging males [22]. In contrast, our data from seasonally dry tropical forest environments show that A. aegypti sex ratios approach parity during the rainy season (Figure 4), deviating from observations in temperate regions. These findings underscore the variability in sex ratio distortion across Aedes species and geographic regions, which is a crucial consideration for vector control strategies [5,43].
Recent biocontrol strategies have incorporated molecular approaches such as genetically engineered mosquitoes and Wolbachia-infected A. aegypti, which interfere with pathogen development and reproduction [5,6,7,44]. Sterile insect techniques (SITs) rely on the release of sterilized males to suppress wild populations [45,46,47], though their short lifespan limits effectiveness beyond a single breeding cycle [5]. Wolbachia-based strategies offer more sustainable control by inducing cytoplasmic incompatibility, shortening the female lifespan, and increasing resistance to arboviruses and Plasmodium [48,49]. However, their success depends on local ecological dynamics—including seasonal shifts in sex ratios—and compatibility between the genetic backgrounds of released and wild populations [5,10,50]. In Brazil, the failure of Wolbachia to persist was attributed to a lack of pre-existing pyrethroid resistance in released mosquitoes, underscoring the importance of matching resistance profiles [13,14]. Our findings of persistent female-biased sex ratios —especially during the dry season—highlight the need to account for regional variation in sex ratio dynamics, which may influence the timing, efficacy, and public reception of Wolbachia-based interventions [51].
While our study was not designed to uncover the mechanistic basis of the sex ratio distortion in A. aegypti, recent research in other arthropods has highlighted several potential molecular pathways. These include sex chromosome meiotic drive, endosymbionts like Wolbachia, and temperature-dependent sex determination [28,52,53]. The role of these mechanisms in shaping seasonal patterns of sex ratio distortion remains poorly understood in container-breeding Aedes mosquitoes. However, they may interact with environmental and anthropogenic drivers to influence vector population structure and mating dynamics.
Our findings highlight the dynamic nature of A. aegypti populations in seasonally dry neotropical biomes. This underscores the need for vector control strategies that adapt to seasonal sex ratio shifts. Field scientists from the World Mosquito Program (El Salvador) have observed female-biased sex ratios during drought conditions, which revert to parity in the rainy season [21,22]. These observations (Figure 4 and Figure 5) are consistent with our data. However, the reduced success of Wolbachia infections during the dry season (World Mosquito Program: El Salvador, personal communication) suggests that releases should coincide with the rainy season to optimize propagation.
Mixed success rates of Wolbachia-based biocontrol in Latin America may be related to unexpected, region-specific sex ratio distortions [51]. Additionally, Wolbachia-infected mosquitoes released in Brazil lacked genetic resistance to local pyrethroid-based insecticides, highlighting the importance of matching the genetic profiles of lab-reared and wild populations [13,14]. This highlights the importance of considering regional differences in vector ecology and insecticide resistance when designing biocontrol strategies [2,3].
Effective implementation of biocontrol measures also requires transparent public education [54]. In El Salvador, a recent Wolbachia release coincided with a national red alert for dengue, causing public misconceptions about the program’s efficacy [55,56]. Sustained public service announcements (PSAs) are essential to clarify the role, effectiveness, and limitations of these measures [57,58].
Our analysis of long-term climatic patterns (Figure 3) confirms a pronounced seasonal cycle in El Salvador, with a six-month dry season (November to April) followed by a six-month wet season (May to October). In high-density urban settings, water storage practices—such as the use of pilas—are especially prevalent during the dry season and inadvertently maintain larval habitats for A. aegypti [13,59]. These anthropogenic behaviors sustain vector populations when female abundance peaks (Figure 4 and Figure 5). At the same time, reduced floral resource availability during the dry season may contribute to lower male survivorship, compounding seasonal sex ratio distortion through both ecological and resource-based constraints.
The seasonal variation in sex ratios observed across sites underscores the ecological plasticity of A. aegypti, a key consideration in the design and implementation of vector control programs [10,13]. Developing effective biocontrol strategies—particularly in seasonally dry tropical biomes—requires the integration of local vector ecology, climatic seasonality, and human behavioral patterns [37]. Incorporating sex ratio surveillance into these efforts will be critical, especially for biocontrol tools that rely on male release (e.g., Wolbachia-infected or sterile insect techniques) [60,61]. Our findings contribute to a growing understanding of A. aegypti functional diversity across neotropical urban landscapes. By linking seasonal sex ratio distortion to ecological and anthropogenic drivers, we highlight the importance of site-specific baseline data for adaptive vector control planning [34,62]. Further investigation is needed to assess the epidemiological relevance of dry-season female-biased populations, particularly within the Central American Dry Corridor (CADC), where climate extremes and water insecurity may intensify VBD risk.

5. Conclusions

Our study demonstrates that A. aegypti populations in seasonally dry urban environments of El Salvador exhibit marked sex ratio distortions influenced by both seasonal and anthropogenic factors. The consistent female-biased ratios observed during the dry season, and the return to near-parity during the wet season, suggest adaptive responses to fluctuating environmental conditions. These findings enhance our understanding of mosquito population dynamics and hold important implications for vector control efforts—particularly those involving Wolbachia-based releases and sterile insect techniques.
Incorporating sex ratio variability into biocontrol programs may improve efficacy by aligning intervention timing with seasonal population dynamics. Our results also underscore the need for effective public education and communication strategies to address misconceptions about biocontrol efforts. Future research should examine the epidemiological consequences of female-biased sex ratios and assess the genetic compatibility of lab-reared and wild mosquito populations to optimize interventions across the Central American Dry Corridor and comparable tropical biomes.
By linking ecological, climatic, and anthropogenic factors to vector ecology, this study contributes valuable insights to the broader understanding of Diptera biology and provides a foundation for adaptive, resilient strategies to mitigate vector-borne diseases under global climate change.

Author Contributions

Conceptualization, A.M.G.-C., M.A.V.C., A.M.G.P. and V.D.C.-G.; methodology, A.M.G.P.; software, V.D.C.-G.; validation, A.M.G.-C., M.A.V.C., A.M.G.P. and V.D.C.-G.; formal analysis, V.D.C.-G.; investigation, A.M.G.-C., M.A.V.C., A.M.G.P. and V.D.C.-G.; resources, A.M.G.-C., M.A.V.C., A.M.G.P. and V.D.C.-G.; data curation, A.M.G.P. and V.D.C.-G.; writing—original draft preparation, A.M.G.-C., M.A.V.C., A.M.G.P. and V.D.C.-G.; writing—review and editing, A.M.G.-C., M.A.V.C., A.M.G.P. and V.D.C.-G.; visualization, A.M.G.-C., M.A.V.C., A.M.G.P. and V.D.C.-G.; supervision, A.M.G.-C., M.A.V.C., A.M.G.P. and V.D.C.-G.; project administration, A.M.G.-C., M.A.V.C., A.M.G.P. and V.D.C.-G.; funding acquisition, A.M.G.-C., M.A.V.C., A.M.G.P. and V.D.C.-G. All authors have read and agreed to the published version of the manuscript.

Funding

A.M.G.-C. was funded through the Core Fulbright U.S. Scholar program (El Salvador, 12440-ES) at the United States Department of State.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author [A.M.G.-C.] upon reasonable request.

Acknowledgments

We would like to express our sincere gratitude to the Salvadoran Ministry of Health for their invaluable support of scientific endeavors that contribute to a better understanding of the population dynamics of disease vectors.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. World Health Organization. Vector-Borne Diseases. Available online: https://www.who.int/news-room/fact-sheets/detail/vector-borne-diseases (accessed on 28 November 2023).
  2. Brown, J.E.; McBride, C.S.; Johnson, P.; Ritchie, S.; Paupy, C.; Bossin, H.; Lutomiah, J.; Fernandez-Salas, I.; Ponlawat, A.; Cornel, A.J.; et al. Worldwide patterns of genetic differentiation imply multiple ‘domestications’ of Aedes aegypti, a major vector of human diseases. Proc. Biol. Sci. 2011, 278, 2446–2454. [Google Scholar] [CrossRef] [PubMed]
  3. Brown, J.E.; Evans, B.R.; Zheng, W.; Obas, V.; Barrera-Martinez, L.; Egizi, A.; Zhao, H.; Caccone, A.; Powell, J.R. Human impacts have shaped historical and recent evolution in Aedes aegypti, the dengue and yellow fever mosquito. Evolution 2014, 68, 514–525. [Google Scholar] [CrossRef] [PubMed]
  4. Facchinelli, L.; Badolo, A.; McCall, P.J. Biology and Behaviour of Aedes aegypti in the Human Environment: Opportunities for Vector Control of Arbovirus Transmission. Viruses 2023, 15, 636. [Google Scholar] [CrossRef] [PubMed]
  5. Guzman, M.G.; Gubler, D.J.; Izquierdo, A.; Martinez, E.; Halstead, S.B. Dengue infection. Nat. Rev. Dis. Primers 2016, 2, 16055. [Google Scholar] [CrossRef]
  6. Wilson, A.L.; Courtenay, O.; Kelly-Hope, L.A.; Scott, T.W.; Takken, W.; Torr, S.J.; Lindsay, S.W. The importance of vector control for the control and elimination of vector-borne diseases. PLoS Negl. Trop. Dis. 2020, 14, e0007831. [Google Scholar] [CrossRef]
  7. Gubler, D.J.; Ooi, E.E.; Vasudevan, S.; Farrar, J. Dengue and Dengue Hemorrhagic Fever, 2nd ed.; CABI: Wallingford, UK, 2014. [Google Scholar]
  8. Pimenta, P.F.; Touray, M.; Miller, L. The journey of malaria sporozoites in the mosquito salivary gland. J. Eukaryot. Microbiol. 1994, 41, 608–624. [Google Scholar] [CrossRef]
  9. Ngugi, H.N.; Mutuku, F.M.; Ndenga, B.A.; Musunzaji, P.S.; Mbakaya, J.O.; Aswani, P.; Irungu, L.W.; Mukoko, D.; Vulule, J.; Kitron, U.; et al. Characterization and productivity profiles of Aedes aegypti (L.) breeding habitats across rural and urban landscapes in western and coastal Kenya. Parasites Vectors 2017, 10, 331. [Google Scholar] [CrossRef]
  10. Wilke, A.B.B.; Vasquez, C.; Carvajal, A.; Moreno, M.; Fuller, D.O.; Cardenas, G.; Petrie, W.D.; Beier, J.C. Urbanization favors the proliferation of Aedes aegypti and Culex quinquefasciatus in urban areas of Miami-Dade County, Florida. Sci. Rep. 2021, 11, 22989. [Google Scholar] [CrossRef]
  11. Powell, J.R.; Tabachnick, W.J. History of domestication and spread of Aedes aegypti—A review. Mem. Inst. Oswaldo Cruz 2013, 108, 11–17. [Google Scholar] [CrossRef]
  12. Slosek, J. Aedes aegypti mosquitoes in the Americas: A review of their interactions with the human population. Soc. Sci. Med. 1986, 23, 249–257. [Google Scholar] [CrossRef]
  13. Joyce, A.L.; Torres, M.M.; Torres, R.; Moreno, M. Genetic variability of the Aedes aegypti (Diptera: Culicidae) mosquito in El Salvador, vector of dengue, yellow fever, chikungunya and Zika. Parasites Vectors 2018, 11, 1–14. [Google Scholar]
  14. Ocampo, C.B.; Wesson, D.M. Population dynamics of Aedes aegypti from a dengue hyperendemic urban setting in Colombia. Am. J. Trop. Med. Hyg. 2004, 71, 506–513. [Google Scholar] [PubMed]
  15. Charnov, E.L. The Theory of Sex Allocation; Princeton University Press: Princeton, NJ, USA, 1982. [Google Scholar]
  16. Fisher, R.A. The Genetical Theory of Natural Selection: A Complete Variorum Edition; Oxford University Press: Oxford, UK, 1999. [Google Scholar]
  17. Edwards, A.W.F. Natural Selection and the Sex Ratio: Fisher’s Sources. Am. Nat. 1998, 151, 564–569. [Google Scholar] [CrossRef] [PubMed]
  18. Barrett, S.C.; Yakimowski, S.B.; Field, D.L.; Pickup, M. Ecological genetics of sex ratios in plant populations. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010, 365, 2549–2557. [Google Scholar] [CrossRef]
  19. Vergés, A.; Paul, N.A.; Steinberg, P.D. Sex and life-history stage alter herbivore responses to a chemically defended red alga. Ecology 2008, 89, 1334–1343. [Google Scholar] [CrossRef]
  20. Hamilton, W.D. Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science 1967, 156, 477–488. [Google Scholar] [CrossRef]
  21. Hawley, W. Population Dynamics of Aedes sierrensis. In Ecology of Mosquitoes: Proceedings of a Workshop; Lounibos, L.P., Rey, J.R., Frank, J.H., Eds.; Florida Medical Entomology Laboratory: Vero Beach, FL, USA, 1985; pp. 167–184. [Google Scholar]
  22. Lounibos, L.P.; Escher, R.L. Sex ratios of mosquitoes from long-term censuses of Florida tree holes. J. Am. Mosq. Control Assoc. 2008, 24, 11–15. [Google Scholar] [CrossRef]
  23. Unlu, I.; Farajollahi, A.; Rochlin, I.; Crepeau, T.N.; Strickman, D.; Gaugler, R. Differences in male-female ratios of Aedes albopictus (Diptera: Culicidae) following ultra-low volume adulticide applications. Acta Trop. 2014, 137, 201–205. [Google Scholar] [CrossRef]
  24. Yates, M. The biology of the tree-hole breeding mosquito Aedes geniculatus (Olivier)(Diptera: Culicidae) in southern England. Bull. Entomol. Res. 1979, 69, 611–628. [Google Scholar]
  25. Groat-Carmona, A.M.; Orozco, S.; Friebe, P.; Payne, A.; Kramer, L.; Harris, E. A novel coding-region RNA element modulates infectious dengue virus particle production in both mammalian and mosquito cells and regulates viral replication in Aedes aegypti mosquitoes. Virology 2012, 432, 511–526. [Google Scholar] [CrossRef]
  26. Ross, P.A.; Callahan, A.G.; Yang, Q.; Jasper, M.; Arif, M.A.K.; Afizah, A.N.; Nazni, W.A.; Hoffmann, A.A. An elusive endosymbiont: Does Wolbachia occur naturally in Aedes aegypti? Ecol. Evol. 2020, 10, 1581–1591. [Google Scholar] [CrossRef] [PubMed]
  27. Simberloff, D. Risks of biological control for conservation purposes. BioControl 2012, 57, 263–276. [Google Scholar] [CrossRef]
  28. Werren, J.H.; Baldo, L.; Clark, M.E. Wolbachia: Master manipulators of invertebrate biology. Nat. Rev. Microbiol. 2008, 6, 741–751. [Google Scholar] [CrossRef] [PubMed]
  29. Jaenike, J. Sex Chromosome Meiotic Drive. Annu. Rev. Ecol. Evol. Syst. 2001, 32, 25–49. [Google Scholar] [CrossRef]
  30. Hurst, G.D.; Jiggins, F.M. Male-killing bacteria in insects: Mechanisms, incidence, and implications. Emerg. Infect. Dis. 2000, 6, 329–336. [Google Scholar] [CrossRef]
  31. Beck, H.E.; Zimmermann, N.E.; McVicar, T.R.; Vergopolan, N.; Berg, A.; Wood, E.F. Present and future Köppen-Geiger climate classification maps at 1-km resolution. Sci. Data 2018, 5, 180214. [Google Scholar] [CrossRef]
  32. Holdridge, L.R. Determination of World Plant Formations from Simple Climatic Data. Science 1947, 105, 367–368. [Google Scholar] [CrossRef]
  33. Bullock, S.H.; Mooney, H.A.; Medina, E. Seasonally Dry Tropical Forests; Cambridge University Press: Cambridge, UK, 1995. [Google Scholar]
  34. Dexter, K.G.; Pennington, R.T.; Oliveira-Filho, A.T.; Bueno, M.L.; Silva de Miranda, P.L.; Neves, D.M. Inserting Tropical Dry Forests into the Discussion on Biome Transitions in the Tropics. Front. Ecol. Evol. 2018, 6, 104. [Google Scholar] [CrossRef]
  35. Pablo-Cea, J.D.; Velado-Cano, M.A.; Noriega, J.A. A first step to evaluate the impact of ecotourism on biodiversity in El Salvador: A case study using dung beetles in a National Park. J. Ecotour. 2021, 20, 51–69. [Google Scholar]
  36. Trewin, B.J.; Kay, B.H.; Darbro, J.M.; Hurst, T.P. Increased container-breeding mosquito risk owing to drought-induced changes in water harvesting and storage in Brisbane, Australia. Int. Health 2013, 5, 251–258. [Google Scholar] [CrossRef]
  37. Choi, J.; Carmona-Galindo, V.; Paredes, G.R.; Marín Recinos, M.F.; de Abrego, V.C. An exploration of land use and poverty as an integrative model for mitigating Chagas disease in El Salvador. BIOS 2020, 91, 125–132. [Google Scholar] [CrossRef]
  38. Karger, D.N.; Conrad, O.; Böhner, J.; Kawohl, T.; Kreft, H.; Soria-Auza, R.W.; Zimmermann, N.E.; Linder, H.P.; Kessler, M. Climatologies at high resolution for the earth’s land surface areas. Sci. Data 2017, 4, 170122. [Google Scholar] [CrossRef] [PubMed]
  39. Rueda, L.M. Pictorial keys for the identification of mosquitoes (Diptera: Culicidae) associated with dengue virus transmission. Zootaxa 2004, 589, 1–60. [Google Scholar]
  40. de Araújo, H.R.C.; Kojin, B.B.; Capurro, M.L. Sex determination and Aedes population control. Parasites Vectors 2018, 11, 644. [Google Scholar] [CrossRef]
  41. Shettima, A.; Joseph, S.; Ishak, I.H.; Abdul Raiz, S.H.; Abu Hasan, H.; Othman, N. Evaluation of Total Female and Male Aedes aegypti Proteomes Reveals Significant Predictive Protein–Protein Interactions, Functional Ontologies, and Differentially Abundant Proteins. Insects 2021, 12, 752. [Google Scholar] [CrossRef]
  42. Robinson, A.S. Sex-ratio manipulation in relation to insect pest control. Annu. Rev. Genet. 1983, 17, 191–214. [Google Scholar] [CrossRef]
  43. Benelli, G.; Jeffries, C.L.; Walker, T. Biological Control of Mosquito Vectors: Past, Present, and Future. Insects 2016, 7, 52. [Google Scholar] [CrossRef]
  44. Gubler, D.J. The partnership for dengue control—A new global alliance for the prevention and control of dengue. Vaccine 2015, 33, 1233. [Google Scholar] [CrossRef]
  45. Benedict, M.Q.; Robinson, A.S. The first releases of transgenic mosquitoes: An argument for the sterile insect technique. Trends Parasitol. 2003, 19, 349–355. [Google Scholar] [CrossRef]
  46. Hendrichs, J.; Robinson, A. Sterile insect technique. In Encyclopedia of Insects; Academic Press: Amsterdam, The Netherlands, 2009; pp. 953–957. [Google Scholar]
  47. Lance, D.; McInnis, D. Biological basis of the sterile insect technique. In Sterile Insect Technique; CRC Press: Boca Raton, FL, USA, 2021; pp. 113–142. [Google Scholar]
  48. Moreira, L.A.; Iturbe-Ormaetxe, I.; Jeffery, J.A.; Lu, G.; Pyke, A.T.; Hedges, L.M.; Rocha, B.C.; Hall-Mendelin, S.; Day, A.; Riegler, M. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 2009, 139, 1268–1278. [Google Scholar] [CrossRef]
  49. Walker, T.; Moreira, L.A. Can Wolbachia be used to control malaria? Mem. Inst. Oswaldo Cruz 2011, 106, 212–217. [Google Scholar] [PubMed]
  50. Zhang, D.; Lees, R.S.; Xi, Z.; Bourtzis, K.; Gilles, J.R. Combining the sterile insect technique with the incompatible insect technique: III-robust mating competitiveness of irradiated triple Wolbachia-infected Aedes albopictus males under semi-field conditions. PLoS ONE 2016, 11, e0151864. [Google Scholar]
  51. Garcia, G.d.A.; Sylvestre, G.; Aguiar, R.; da Costa, G.B.; Martins, A.J.; Lima, J.B.P.; Petersen, M.T.; Lourenço-de-Oliveira, R.; Shadbolt, M.F.; Rašić, G. Matching the genetics of released and local Aedes aegypti populations is critical to assure Wolbachia invasion. PLoS Negl. Trop. Dis. 2019, 13, e0007023. [Google Scholar]
  52. Lindholm, A.K.; Dyer, K.A.; Firman, R.C.; Fishman, L.; Forstmeier, W.; Holman, L.; Johannesson, H.; Knief, U.; Kokko, H.; Larracuente, A.M.; et al. The Ecology and Evolutionary Dynamics of Meiotic Drive. Trends Ecol. Evol. 2016, 31, 315–326. [Google Scholar] [CrossRef]
  53. Pen, I.; Weissing, F.J. Sex-ratio optimization with helpers at the nest. Proc. Biol. Sci. 2000, 267, 539–543. [Google Scholar] [CrossRef]
  54. Carmona-Galindo, V.; Carmona, T.; Carmona-Valdivieso, D. El papel del pez chimbolo (Poeciliopsis gracilis Heckel 1848) en el biocontrol de zancudos y la recuperación de servicios ecosistémicos en los ríos urbanos de El Salvador. El Salv. Cienc. Tecnol. 2018, 23, 23–27. [Google Scholar]
  55. Cea, M. Concluyen las liberaciones de zancudos con Wolbachia en Santa Ana. La Prensa Gráfica, 9 June 2024. [Google Scholar]
  56. Alemán, M. Decretan Alerta Roja por el Aumento de Casos de Dengue en El Salvador; Associated Press: New York, NY, USA, 2024. [Google Scholar]
  57. Padmanaban, D. Can mass-produced mosquitoes slow dengue’s spread? Harvard Public Health, 15 August 2023. [Google Scholar]
  58. Cea, M. Alabi: Liberaciones de zancudos con Wolbachia no tienen relación con alza de dengue. La Prensa Gráfica, 25 July 2024. [Google Scholar]
  59. Fernández, D.; Montañez, A.; Sarmanto, N. Diagnóstico de la Prestación de los Servicios de Agua Potable y Alcantarillado en El Salvador; Comisión Económica para América Latina y el Caribe (CEPAL): Santiago, Chile, 2023; 25p. [Google Scholar]
  60. Benelli, G. Managing mosquitoes and ticks in a rapidly changing world—Facts and trends. Saudi J. Biol. Sci. 2019, 26, 921–929. [Google Scholar] [CrossRef]
  61. Ferraguti, M.; Martínez-de La Puente, J.; Roiz, D.; Ruiz, S.; Soriguer, R.; Figuerola, J. Effects of landscape anthropization on mosquito community composition and abundance. Sci. Rep. 2016, 6, 29002. [Google Scholar]
  62. Kache, P.A.; Santos-Vega, M.; Stewart-Ibarra, A.M.; Cook, E.M.; Seto, K.C.; Diuk-Wasser, M.A. Bridging landscape ecology and urban science to respond to the rising threat of mosquito-borne diseases. Nat. Ecol. Evol. 2022, 6, 1601–1616. [Google Scholar] [CrossRef]
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Figure 1. Examples of peridomiciliary cement water basins (pilas) and plastic water storage containers. These containers are kept filled with water year-round and are commonly used for washing and cleaning in hamlets across El Salvador.
Figure 1. Examples of peridomiciliary cement water basins (pilas) and plastic water storage containers. These containers are kept filled with water year-round and are commonly used for washing and cleaning in hamlets across El Salvador.
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Figure 2. Sexual dimorphism in A. aegypti. The female (left) has an elongated proboscis and shorter palps, while the male (right) has a shorter proboscis, feathery palps, and bushier antennae. Abdominal differences are also visible.
Figure 2. Sexual dimorphism in A. aegypti. The female (left) has an elongated proboscis and shorter palps, while the male (right) has a shorter proboscis, feathery palps, and bushier antennae. Abdominal differences are also visible.
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Figure 3. Climate diagram of San Salvador, El Salvador (1981–2010), showing average monthly changes in precipitation (blue line) and temperature (orange line). The diagram also displays the average annual temperature (°C), elevation above sea level (m), and total annual precipitation (mm). These long-term climate norms reflect the characteristic seasonal dynamics of seasonally dry tropical forests in the region. Yellow shading indicates periods of water deficit, where the temperature curve exceeds the precipitation curve. Light blue shading represents periods of water excess, where precipitation exceeds temperature. Dark blue shading highlights months with precipitation above 100 mm, indicating likely soil water saturation.
Figure 3. Climate diagram of San Salvador, El Salvador (1981–2010), showing average monthly changes in precipitation (blue line) and temperature (orange line). The diagram also displays the average annual temperature (°C), elevation above sea level (m), and total annual precipitation (mm). These long-term climate norms reflect the characteristic seasonal dynamics of seasonally dry tropical forests in the region. Yellow shading indicates periods of water deficit, where the temperature curve exceeds the precipitation curve. Light blue shading represents periods of water excess, where precipitation exceeds temperature. Dark blue shading highlights months with precipitation above 100 mm, indicating likely soil water saturation.
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Figure 4. Temporal changes in A. aegypti mosquito male-to-female (M:F) sex ratios (solid blue line) in El Salvador, compared to the expected 1:1 ratio (dashed red line).
Figure 4. Temporal changes in A. aegypti mosquito male-to-female (M:F) sex ratios (solid blue line) in El Salvador, compared to the expected 1:1 ratio (dashed red line).
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Figure 5. Temporal changes in the observed distribution of male (green line) and female (orange line) A. aegypti mosquitoes in El Salvador, compared to the expected distribution (dashed red line), which was calculated as the total sampling abundance averaged across eight sampling events (12.5%).
Figure 5. Temporal changes in the observed distribution of male (green line) and female (orange line) A. aegypti mosquitoes in El Salvador, compared to the expected distribution (dashed red line), which was calculated as the total sampling abundance averaged across eight sampling events (12.5%).
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Table 1. Sampling dates, locations, numbers of Aedes aegypti mosquitoes successfully reared from field-collected larvae and examined for sex determination, and M:F sex ratios collected across four departments, seven municipalities, and eight hamlets in El Salvador.
Table 1. Sampling dates, locations, numbers of Aedes aegypti mosquitoes successfully reared from field-collected larvae and examined for sex determination, and M:F sex ratios collected across four departments, seven municipalities, and eight hamlets in El Salvador.
DateDepartmentMunicipalityHamletLocation
(Latitude and Longitude)		No. SamplesM:F
Ratio
14 March
2021		UsulutanEreguayquinUnnamed13°20.5880′ N 88°23.3880′ W18729:100
28 June
2022		MorazanSan CarlosBarrio El Centro13°38′48.5″ N 88°05′47.4″ W5018:25
2 July
2022		MorazanJocoroBarrio San Sebastian13°36′56.3″ N 88°01′21.3″ W4823:25
6 July
2021		San MiguelSan Rafael OrienteBarrio San Benito13°22.8290′ N 88°21.2050′ W8933:100
16 July
2022		MorazanJocoroLas Marias Centro13°37′08.1″ N 87°58′56.1″ W521:1
28 July
2022		La UnionSanta Rosa de LimaEl Limón13°36′25.8″ N 87°55′47.3″ W501:1
7 September
2022		La UnionPasaquinaSanta Clara13°35′12.4″ N 87°46′47.2″ W5017:20
20 September
2022		La UnionSan José la FuenteBarrio El Calvario13°33′33.2″ N 87°54′16.4″ W5017:20
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MDPI and ACS Style

Groat-Carmona, A.M.; Velado Cano, M.A.; González Pérez, A.M.; Carmona-Galindo, V.D. Sex Ratio Distortion of Aedes aegypti (L.) in El Salvador: Biocontrol Implications for Seasonally Dry Urban Neotropical Environments. Diversity 2025, 17, 257. https://doi.org/10.3390/d17040257

AMA Style

Groat-Carmona AM, Velado Cano MA, González Pérez AM, Carmona-Galindo VD. Sex Ratio Distortion of Aedes aegypti (L.) in El Salvador: Biocontrol Implications for Seasonally Dry Urban Neotropical Environments. Diversity. 2025; 17(4):257. https://doi.org/10.3390/d17040257

Chicago/Turabian Style

Groat-Carmona, Anna M., Maryory A. Velado Cano, Ana M. González Pérez, and Víctor D. Carmona-Galindo. 2025. "Sex Ratio Distortion of Aedes aegypti (L.) in El Salvador: Biocontrol Implications for Seasonally Dry Urban Neotropical Environments" Diversity 17, no. 4: 257. https://doi.org/10.3390/d17040257

APA Style

Groat-Carmona, A. M., Velado Cano, M. A., González Pérez, A. M., & Carmona-Galindo, V. D. (2025). Sex Ratio Distortion of Aedes aegypti (L.) in El Salvador: Biocontrol Implications for Seasonally Dry Urban Neotropical Environments. Diversity, 17(4), 257. https://doi.org/10.3390/d17040257

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