Introgression of thermal tolerance alleles drives adaptation despite risk of mitonuclear conflict

Hybridization may offer a form of genetic rescue from warming temperatures through the introgression of heat-adapted alleles from a high-tolerance population into a low-tolerance population. However, the success of adaptive introgression can be impeded by incompatibility at other loci, especially those that participate in coadapted gene complexes that could lead to unfavorable combinations in hybrids. We tested the success of introgression of heat-adapted alleles in the face of potential fitness tradeoffs associated with hybridized mitonuclear gene complexes in the crustacean Tigriopus californicus. We created reciprocal hybrid crosses of the San Diego (SD) and Strawberry Hill (SH) populations, which show divergence in both thermal tolerance and mitochondrial genomes, then subjected hybrid populations to ten generations of either selection for thermal tolerance or to control conditions. Lines under selection in both crosses evolved higher thermal tolerance. Moreover, both crosses showed substantial increases in nuclear SD allele frequencies, with the SH♀xSD♂ cross having as much SD introgression as the reciprocal cross despite having higher risk of mitonuclear incompatibilities with its SH mtDNA. This suggests that introgression of warm-adapted alleles was largely successful despite the risk of introducing mitonuclear incompatibilities that could result from genome-wide shifts toward the paternal allele. This outcome was likely made possible by strong mitonuclear matching being maintained in a few genomic regions on different chromosomes, exclusive of those responding to thermal selection, pointing to components of cytochrome c oxidase, in particular COX6A1, as potentially having a disproportionate impact in mitonuclear coadaptation.