Mosquito Sensory Systems

Abstract

In this chapter, we will highlight recent progress in describing the current state of our understanding of the diverse array of sensory pathways across the family Culicidae. These will include both contact (gustatory) and volatile (olfactory)-based chemosensory systems as well as auditory, mechanosensory, thermosensory and visual modalities. We will discuss both the cellular and the molecular basis underlying these senses as well as how they control the lifecycle, behaviour and vectorial capacity of mosquitoes. We will discuss the impact of recent data derived from next-generation sequencing to our understanding of the evolution and function of these diverse sensory systems.

Introduction

In light of their role as vectors for the transmission of a range of important human and animal diseases, mosquitoes represent one of the greatest worldwide threats to global health. In fact, mosquitoes might well be considered the most dangerous animals on the planet. Anopheles gambiae and other Anopheline mosquitoes spread malaria, which is the most prevalent insect-borne disease worldwide. Each year, Plasmodium falciparum and other malaria pathogens infect hundreds of millions and cause the death of hundreds of thousands of people (Enayati and Hemingway, 2010, Guinovart et al., 2006). Arboviruses (arthropod-borne viruses) represent another significant class of mosquito-borne pathogens. Of these, dengue virus, which is responsible for both dengue fever and dengue haemorrhagic fever (DF/DHF), is rapidly emerging as a significant worldwide problem since it appeared on the public health landscape after the World War II (Bhatt et al., 2013). While DF/DHF was first described in the 18th century, today upwards of ~ 500,000,000 people are infected with dengue virus annually by the highly invasive Aedes aegypti mosquito, which is the main vector for this and other arboviruses (Bhatt et al., 2013). Together with other Aedine mosquitoes Ae. aegypti also transmits a wide range of arboviruses, including the causative agents for Chikungunya, Yellow and Zika fevers. In addition to their immediate symptomatic effects on infected individuals, which range from aches, fever to broad haemorrhagic episodes and death, public health agencies are increasingly becoming aware of a diverse range of very serious postinfection pathologies that include birth defects such as microcephaly, neurological conditions such as Guillain–Barre syndrome and many others (Cao-Lormeau et al., 2016, Chang et al., 2016).

Diseases spread by mosquitoes are not restricted to the developing world; indeed several are on the rise in the United States and other parts of the developed world. An example is West Nile Virus, which was first identified in New York in 1999. It is now documented in all 48 contiguous states (Petersen et al., 2013). With the increasing reality of climate change and its associated global warming that is predicted to occur over the coming century and beyond, it is highly likely that the catastrophic effects of insect-borne diseases are going to get worse across both the developed and developing world.

Disease transmission by mosquitoes is based on the reproductive requirements of females that take blood meals from humans and other animals in order to complete their gonadotropic cycles. In order to carry out this critical (from a public health perspective) component as well as nearly all the other aspects of both male and female life stages mosquitoes must utilize a diverse and highly sophisticated set of sensory systems. These systems receive and pass along essential information across a range of sensory modalities that is processed to drive the navigation and preference decisions that in many ways underlie the vectorial capacity of mosquitoes. Here we provide an overview of the current status of our mechanistic understanding of the senses in mosquito vectors, with a particular emphasis on the peripheral sensory neurons and receptors.

Mosquito life cycles are conducted in a variety of environments and conditions; accordingly, they have evolved an array of sensory systems with which to sense and respond to a complex set of environmental stimuli and biological cues. These signals are received by a range of sensory cells, most notably neurons of the peripheral nervous system that transduce external signals into neuronal activity or inhibition through a variety of mechanisms. This information is subsequently collected, integrated and otherwise processed by downstream regions of the central nervous system (CNS) in order for mosquitoes to make the salient behavioural decisions that are required to successfully complete a set of discrete lifecycle tasks. Here we describe the sensory processes that impact the major elements of the mosquito lifecycle.