Genomic shifts, phenotypic clines and fitness costs associated with cold-tolerance in the Asian tiger mosquito

Climatic variation is a key driver of genetic differentiation and
phenotypic traits evolution, and local adaptation to temperature is
expected in widespread species. We investigated phenotypic and genomic
changes in the native range of the Asian tiger mosquito, Aedes albopictus.
We first refine the phylogeographic structure based on genome-wide regions
(1,901 double-digest restriction-site associated DNA single nucleotide
polymophisms [ddRAD SNPs]) from 41 populations. We then explore the
patterns of cold adaptation using phenotypic traits measured in common
garden (wing size and cold tolerance) and genotype–temperature
associations at targeted candidate regions (51,706 exon-capture SNPs) from
nine populations. We confirm the existence of three evolutionary lineages
including clades A (Malaysia, Thailand, Cambodia, and Laos), B (China and
Okinawa), and C (South Korea and Japan). We identified
temperature-associated differentiation in 15 out of 221 candidate regions
but none in ddRAD regions, supporting the role of directional selection in
detected genes. These include genes involved in lipid metabolism and a
circadian clock gene. Most outlier SNPs are differently fixed between
clades A and C, whereas clade B has an intermediate pattern. Females are
larger at higher latitudes yet produce no more eggs, which might favor the
storage of energetic reserves in colder climates. Nondiapausing eggs from
temperate populations survive better to cold exposure than those from
tropical populations, suggesting they are protected from freezing damages
but this cold tolerance has a fitness cost in terms of egg viability.
Altogether, our results provide strong evidence for the thermal adaptation
of A. albopictus across its wide temperature range.