Postzygotic isolation involves strong mitochondrial and sex-specific effects in Tigriopus californicus, a species lacking heteromorphic sex chromosomes

Abstract

Detailed studies of the genetics of speciation have focused on a few model systems, particularly Drosophila. The copepod Tigriopus californicus offers an alternative that differs from standard animal models in that it lacks heteromorphic chromosomes (instead, sex determination is polygenic) and has reduced opportunities for sexual conflict, because females mate only once. Quantitative trait loci (QTL) mapping was conducted on reciprocal F2 hybrids between two strongly differentiated populations, using a saturated linkage map spanning all 12 autosomes and the mitochondrion. By comparing sexes, a possible sex ratio distorter was found but no sex chromosomes. Although studies of standard models often find an excess of hybrid male sterility factors, we found no QTL for sterility and multiple QTL for hybrid viability (indicated by non-Mendelian adult ratios) and other characters. Viability problems were found to be stronger in males, but the usual explanations for weaker hybrid males (sex chromosomes, sensitivity of spermatogenesis, sexual selection) cannot fully account for these male viability problems. Instead, higher metabolic rates may amplify deleterious effects in males. Although many studies of standard speciation models find the strongest genetic incompatibilities to be nuclear-nuclear (specifically X chromosome-autosome), we found the strongest deleterious interaction in this system was mito-nuclear. Consistent with the snowball theory of incompatibility accumulation, we found that trigenic interactions in this highly divergent cross were substantially more frequent (>6×) than digenic interactions. This alternative system thus allows important comparisons to studies of the genetics of reproductive isolation in more standard model systems.

Figure 1

Linkage map used in QTL analysis of T. californicus. Five candidate genes for nuclear–mitochondrial interactions are underlined: TcCYC (cytochrome C), RPOL (mitochondrial RNA polymerase), TcTFB1 (mitochondrial transcription factor B1), TcRISP (mitochondrial rieske iron-sulfur protein) and TcTFAM (transcription factor A, mitochondrial). Marker distances were taken from Foley et al. (2011).

Figure 2

Bar plots of the relative frequencies of SD homozygous (light gray), SC homozygous (dark gray) and heterozygous (black) individuals at each marker locus across the genome; for the linkage-mapping population of nauplii (from Foley et al., 2011) and by sex and mitochondrial background for the F₂ QTL population. *0.05<P>0.01 after Bonferroni correction; **0.01<P>0.0001 after Bonferroni correction; ***P<0.0001 after Bonferroni correction, asterisks vertical over bars.

Figure 3

QTL for NMR in T. californicus F₂. For each sex and mitochondrial background, the LOD plots are shown, with LOD maxima indicated by open circles, and the two LOD confidence interval shown by the solid black line. Genome-wide significance thresholds are indicated by the solid gray line and chromosome-specific thresholds by the dotted gray line. The additional horizontal gray line in the SCmit M LOD plot indicates a break in the axis. Transparent gray boxes indicate intervals containing a candidate gene (see Figure 1). Effect plots are shown below the LOD plot, with the log relative survival of the SC homozygote relative to the SD homozygote in black, the heterozygote in gray and the additive expectation of the heterozygote as dotted gray. Significant deviations from the additive expectation are indicated by asterisks.

Figure 4

LOD plots and effect plots for sex in an F₂ mapping population of T. californicus by mitochondrial background. In the LOD plot, the horizontal black line represents the significance threshold. In the effect plot, the black line is the additive effect of the SD allele and the gray line is the dominance effect; female is scored as 0 and male as 1. An asterisk indicates a significant dominance effect.