Cellular energy production requires coordinated interactions between genetic components from the nuclear and mitochondrial genomes. This coordination results in coadaptation of interacting elements within populations. Interbreeding between divergent gene pools can disrupt coadapted loci and result in hybrid fitness breakdown. While specific incompatible loci have been detected in mutiple eukaryotic taxa, the extent of the nuclear genome that is influenced by mitonuclear coadaptation is not clear in any species. Here, we used F₂ hybrids between two divergent populations of the copepod Tigriopus californicus to examine mitonuclear coadaptation across the nuclear genome. Using developmental rate as a measure of fitness, we fount that fast-developing copepods had higher ATP synthesis capacity than slow developers, suggesting variation in developmental rates is at least partly associated with mitochondrial dysfunction. Using Pool-seq, we detected strong biases for maternal alleles across 7 (of 12) chomosomes in both reciprocal crosses in high-fitness hybrids, while low-fitness hybrids showed shifts towards the paternal population. Comparison with previous results on a different hybrid cross revealed largely different patterns of strong mitonuclear coadaptation associated with developmental rate. Our findings suggest that functional coadaptation between interacting nuclear and mitochondrial components is reflected in strong polygenic effects on this life-history phenotype, and reveal that molecular coadaptation follows independent evolutionary trajectories among isolated populations.

SDxSH_FAST_read_counts.txt: Mapped read counts for fast-developing F2 hybrids from the cross SD-female x SH-male. Counts for each allele are the average across mappings to each reciprocal genome reference. SD: San Diego, California; SH: Strawberry Hill, Oregon.

SDxSH_SLOW_final_counts.txt: Mapped read counts for slow-developing F2 hybrids from the cross SD-female x SH-male. Counts for each allele are the average across mappings to each reciprocal genome reference. SD: San Diego, California; SH: Strawberry Hill, Oregon.

SHxSD_FAST_read_counts.txt: Mapped read counts for fast-developing F2 hybrids from the cross SH-female x SD-male. Counts for each allele are the average across mappings to each reciprocal genome reference. SD: San Diego, California; SH: Strawberry Hill, Oregon.

SHxSD_SLOW_final_counts.txt: Mapped read counts for slow-developing F2 hybrids from the cross SH-female x SD-male. Counts for each allele are the average across mappings to each reciprocal genome reference. SD: San Diego, California; SH: Strawberry Hill, Oregon.

SDxSH_FAST_AF.txt: Allele frequencies for fast-developing F2 hybrids from the cross SD-female x SH-male. Only SNP loci that were successfully genotyped in the four sampled pools are shown in the table. SD: San Diego, California; SH: Strawberry Hill, Oregon.

SDxSH_SLOW_AF.txt: Allele frequencies for slow-developing F2 hybrids from the cross SD-female x SH-male. Only SNP loci that were successfully genotyped in the four sampled pools are shown in the table. SD: San Diego, California; SH: Strawberry Hill, Oregon.

SHxSD_FAST_AF.txt: Allele frequencies for fast-developing F2 hybrids from the cross SH-female x SD-male. Only SNP loci that were successfully genotyped in the four sampled pools are shown in the table. SD: San Diego, California; SH: Strawberry Hill, Oregon.

SHxSD_SLOW_AF.txt: Allele frequencies for slow-developing F2 hybrids from the cross SH-female x SD-male. Only SNP loci that were successfully genotyped in the four sampled pools are shown in the table. SD: San Diego, California; SH: Strawberry Hill, Oregon.

SDxSH_FAST_200kb_win.txt: Window-average allele frequencies of the respective "AF" files.

SDxSH_SLOW_200kb_win.txt: Window-average allele frequencies of the respective "AF" files.

SHxSD_FAST_200kb_win.txt: Window-average allele frequencies of the respective "AF" files.

SHxSD_SLOW_200kb_win.txt: Window-average allele frequencies of the respective "AF" files.