Darker eggs of mosquitoes resist more to dry conditions: Melanin enhances serosal cuticle contribution in egg resistance to desiccation in Aedes, Anopheles and Culex vectors.

Luana C Farnesi,Gustavo L Rezende,Helena C M Vargas,Denise Valle,Pedro L Oliveira

doi:10.1371/journal.pntd.0006063

Abstract

Mosquito vectors lay their white eggs in the aquatic milieu. During early embryogenesis water passes freely through the transparent eggshell, which at this moment is composed of exochorion and endochorion. Within two hours the endochorion darkens via melanization but even so eggs shrink and perish if removed from moisture. However, during mid-embryogenesis, cells of the extraembryonic serosa secrete the serosal cuticle, localized right below the endochorion, becoming the third and innermost eggshell layer. Serosal cuticle formation greatly reduces water flow and allows egg survival outside the water. The degree of egg resistance to desiccation (ERD) at late embryogenesis varies among different species: Aedes aegypti, Anopheles aquasalis and Culex quinquefasciatus eggs can survive in a dry environment for ≥ 72, 24 and 5 hours, respectively. In some adult insects, darker-body individuals show greater resistance to desiccation than lighter ones. We asked if egg melanization enhances mosquito serosal cuticle-dependent ERD. Species with higher ERD at late embryogenesis exhibit more melanized eggshells. The melanization-ERD hypothesis was confirmed employing two Anopheles quadrimaculatus strains, the wild type and the mutant GORO, with a dark-brown and a golden eggshell, respectively. In all cases, serosal cuticle formation is fundamental for the establishment of an efficient ERD but egg viability outside the water is much higher in mosquitoes with darker eggshells than in those with lighter ones. The finding that pigmentation influences egg water balance is relevant to understand the evolutionary history of insect egg coloration. Since eggshell and adult cuticle pigmentation ensure insect survivorship in some cases, they should be considered regarding species fitness and novel approaches for vector or pest insects control.

Highlights

Mosquitoes of the genera Aedes, Anopheles and Culex transmit pathogens that are the causative agents of diverse diseases such as yellow fever, dengue, chikungunya, Zika and West Nile viruses, malaria and lymphatic filariasis [1,2,3,4,5,6,7]
The egg resistance to desiccation (ERD), defined as the capacity of an egg to sustain its viability outside the water [29,30], varies among mosquito species at the end of embryogenesis (Fig 1C) [19]
In order to directly evaluate the relationship between melanization and ERD without any other confounding factor, we took advantage of a mutant strain of the species An. quadrimaculatus, which shows a significant melanization deficit: the GORO strain

Summary

Introduction

Mosquitoes of the genera Aedes, Anopheles and Culex transmit pathogens that are the causative agents of diverse diseases such as yellow fever, dengue, chikungunya, Zika and West Nile viruses, malaria and lymphatic filariasis [1,2,3,4,5,6,7]. Blocking mosquito life cycle is an effective way to hamper disease transmission [8]. Mosquitoes lay their eggs in water pools, some of which are temporary [2]. Water passes freely through their eggshells during early embryogenesis and drying these water collections leads to egg desiccation, preventing its development. At this stage mosquito eggshell is composed of a brittle exochorion and a smooth transparent endochorion [2,9]. Throughout this work the eumelanin will be named "melanin"

Results

Discussion

Conclusion