NEURAL BASIS OF HOST PREFERENCE EVOLUTION IN MOSQUITOES

Abstract

An animal’s fitness depends heavily on how it behaves in response to environmental stimuli. Behavior is therefore subject to strong selection and often evolves rapidly. Ever since Darwin, behavioral evolution has been studied extensively at the organismal level. However, we know very little about its proximate neural mechanisms. When behaviors need to change, how do the underlying neural circuits evolve accordingly? This is the central question for my dissertation work. My research takes advantage of a simple but powerful study system—the recent evolution of strong host preference in Aedes aegypti mosquitoes. Ae. aegypti was originated in Africa, but in less than 10,000 years, a form has evolved to specialize in biting humans, from the ancestral generalist form that bites diverse animal species, making it one of the most dangerous disease vectors. Mosquitoes rely primarily on olfaction to locate and discriminate hosts. Correspondingly, the specialist form has evolved a strong preference for human odor over the odor of nonhuman animals. How is host odor discrimination achieved at the neural level, and what have changed in the underlying circuits during specialization on human hosts? I first surveyed the literature broadly to list all possibilities (Chapter 1). I then developed several novel transgenic reagents with CRISPR/Cas9 to access the olfactory circuits in mosquitoes, in order to study behavior at the mechanistic level (Chapter 2). To understand how mosquitoes can discriminate human odor from animal odor, I first focused on the antennal lobe of the specialist mosquito (Chapter 3). By recording activity in the antennal lobe, I found a simple but robust neural code in the mosquito brain that distinguishes human odor from animal odor by stronger activation of a human-sensitive glomerulus. Lastly, I turned to the evolutionary question and compared the neuroanatomy of antennal lobe between the specialist and generalist mosquitoes (Chapter 4). I found broad reshaping of mosquito olfactory circuits during specialization on human hosts. Taken together, my dissertation research provides key insights to the neural mechanisms underlying host discrimination in mosquitoes and its evolution.