Pervasive Mitonuclear Coadaptation Underlies Fast Development in Interpopulation Hybrids of a Marine Crustacean

Abstract

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 multiple 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 found 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) chromosomes in both reciprocal crosses in high-fitness hybrids, whereas low-fitness hybrids showed shifts toward 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.

Keywords: ATP synthesis; copepods; hybridization; pool-seq; postzygotic isolation.

Fig. 1.

Frequency distributions of developmental time to metamorphosis in Tigriopus californicus. Individuals were scored as the number of days from hatching to reaching copepodid I stage. (A) Outbred parental populations, San Diego (SD, n = 1,368) and Strawberry Hill (SH, n = 1,416); (B) SD♀×SH♂ (n = 2,097); (C) SH♀×SD♂ (n = 3,093). Shaded areas in B and C represent the subset of individuals (n = 300) pooled from each phenotypic range.

Fig. 2

Rate of ATP synthesis in fast- and slow-developing F2 hybrid copepods. Developmental rates were quantified as the number of days from hatching until metamorphosis into copepodid I stage (fast: 6 days; slow: 15+ days). Measurements are of complex I-fueled ATP production in isolated mitochondria. Rates between fast and slow groups within each hybrid cross were significantly different (t-tests, P < 0.05).

Fig. 3

Pool-seq analysis of allele frequencies in fast-developing F2 hybrid copepods. (A) Allele frequencies for each reciprocal cross along the 12 autosomes. Each point represents a mean of frequencies across SNPs in 200-kb windows. Legend on right side of panel aids in interpretation of mitonuclear matching/mismatching; (B) Results of Z-statistics (Huang et al. 2012) comparing allele frequencies between crosses at individual SNP loci (n = 106,929). Red dashed line marks the false-discovery rate (FDR) threshold of 0.01.

Fig. 4

Pool-seq analysis of allele frequencies in slow-developing F2 hybrid copepods. (A) Allele frequencies for each reciprocal cross along the 12 autosomes. Each point represents a mean of frequencies across SNPs in 200-kb windows. Legend on right side of panel aids in interpretation of mitonuclear matching/mismatching; (B) Results of Z-statistics (Huang et al. 2012) comparing allele frequencies between crosses at individual SNP loci (n = 106,929). Red dashed line marks the false-discovery rate (FDR) threshold of 0.01.

Fig. 5

Comparison of allele frequencies deviations between crosses across chromosomes. Plotted are boxplot distributions of Z-statistics quantifying the difference in frequencies between fast-developers from reciprocal crosses in SD×SH (this study), and in SD×SC (SC = Santa Cruz, Healy and Burton 2020). Each boxplot comprises Z-statistics of 1,000 randomly sampled SNP loci. P-values are from Wilcoxon tests comparing Z-statistics between crosses, and underlined chromosomes are those showing significant differences.

Fig. 6

DNA sequence differentiation between SD and two populations across nuclear protein-coding genes. SD versus SC has 13,704 gene alignments, and SD versus SH has 14,485.