Using Ae. aegypti as a model to understand the genomic basis of rapid and repeated evolution

University Of California, San Diego, La Jolla CA

Investigators

Abstract

PROJECT SUMMARY How fast can populations adapt to inhabit a different ecological niche or to keep track with a changing environment? Recent studies in systems as diverse as Galapagos finches, Drosophila melanogaster, and sticklebacks suggest that adaptation can be very fast if adaptive genetic variation is available and the genomic architectures of adaptative traits facilitate a coordinated response to selection – especially if adaptive alleles are grouped together in compact architectures or kept in linkage disequilibrium within chromosomal inversions. But it has been very difficult to link fitness in natural systems, spatial and temporal patterns of allele frequency change, and an understanding of the genomic basis of specific adaptive traits. Aedes aegypti provides a remarkably tractable system in which to answer these questions. In this species, a human-specialist form evolved from a generalist ancestor within the last 5000 years, likely in West Africa. This transition was accompanied by several well-characterized changes in important traits across their lifecycle, from behavior, to life history, to physiology. This species is easy to collect and study in the field, easy to work with in the lab, and has a high quality genome assembly and tractable genetic manipulation with CRISPR-Cas9. In the proposed work, we build on recent work showing that this species shows evidence of several shifts in ecology across sharp spatial clines, and across decades and even seasons in its native range in Africa to characterize the genomic basis of these rapid and repeated shifts in ecology. We will use field study of rapid fluctuations in genome-wide allele frequencies across the starkly different dry and wet seasons of the southern edge of the Sahel in Senegal to characterize the genome-wide distribution of adaptive variation and patterns of selection across the genome. We will couple this with high-resolution mapping of genes involved in key putatively adaptive traits in the lab, and functional characterization of these genes using reciprocal hemizygosity tests in hybrids between human-specialist and generalist lab strains. We will take advantage of this species’ short generation time to carry out experimental evolution studies of the role of genomic architecture in rapid evolution – in particular, we will examine the role of a recently characterized large chromosomal inversion in mediating rapid ecological transitions in space and time. The proposed work will synthesize direct observations of allele frequency change in nature and focused laboratory study to come to a new and deeper understanding of the genomic mechanisms that can enable rapid evolution.