Temperature perturbation of cellular host-microbe interactions explains continent-wide endosymbiont prevalence

Endosymbioses influence host physiology, reproduction, and fitness, but
these relationships require efficient microbe transmission between host
generations to persist. Maternally
transmitted Wolbachia are the most common known
endosymbionts, but their frequencies vary widely within and among host
populations for unknown reasons. Here we integrate genomic, cellular, and
phenotypic analyses with mathematical models to provide an unexpectedly
simple explanation for
global wMel Wolbachia prevalence
in Drosophila melanogaster. Cooling temperatures
decrease wMel cellular abundance at a key stage of host
oogenesis, producing temperature-dependent variation in maternal
transmission that plausibly explains latitudinal clines of wMel
frequencies on multiple continents. wMel sampled from a
temperate climate targets the germline more efficiently in the
cold than a recently differentiated tropical variant (~2,200 years ago),
indicative of rapid wMel adaptation to climate. Genomic analyses
identify a very narrow list of wMel alleles—most notably,
a derived stop codon in
the major Wolbachia surface protein WspB—that
underlie thermal sensitivity of cellularWolbachia abundance and
covary with temperature globally. Decoupling temperate wMel and
host genomes further reduces transmission in the cold, a pattern that is
characteristic of host-microbe co-adaptation to a temperate
climate. Complex interactions among Wolbachia, hosts,
and the environment (GxGxE) mediate wMel cellular abundance and
maternal transmission, implicating temperature as a key determinant
of Wolbachia spread and equilibrium frequencies, in
conjunction with Wolbachia effects on host fitness and
reproduction. Our results motivate strategic use of locally
selected wMel variants for Wolbachia-based biocontrol
efforts, which currently protect millions of individuals from arboviruses
that cause human disease.