Genomic scans reveal multiple mito‐nuclear incompatibilities in population crosses of the copepod Tigriopus californicus

Abstract

The evolution of intrinsic postzygotic isolation can be explained by the accumulation of Dobzhansky‐Muller incompatibilities (DMI). Asymmetries in the levels of hybrid inviability and hybrid sterility are commonly observed between reciprocal crosses, a pattern that can result from the involvement of uniparentally inherited factors. The mitochondrial genome is one such factor that appears to participate in DMI in some crosses but the frequency of its involvement versus biparentally inherited factors is unclear. Here we assess the relative importance of incompatibilities between nuclear factors (nuclear‐nuclear) versus those between mitochondrial and nuclear factors (mito‐nuclear) in a species that lacks sex chromosomes. We used a Pool‐seq approach to survey three crosses among genetically divergent populations of the copepod, Tigriopus californicus, for regions of the genome that are affected by hybrid inviability. Results from reciprocal crosses suggest that mito‐nuclear incompatibilities are more common than nuclear‐nuclear incompatibilities overall. These results suggest that in the presence of very high levels of nucleotide divergence between mtDNA haplotypes, mito‐nuclear incompatibilities can be important for the evolution of intrinsic postzygotic isolation. This is particularly interesting considering this species lacks sex chromosomes, which have been shown to harbor a particularly high number of nuclear‐nuclear DMI in several other species.

Strong selective effects of mitochondrial DNA on the nuclear genome

“…Effects of mitonuclear coevolution were not evenly spread across the nuclear genome, but involved at least 5 of the 12 chromosomes with clear deviations favoring coevolved alleles on chromosomes 1 to 5. Relative to previous studies in T. californicus hybrids (31)(32)(33), this clear pattern toward partial recovery of coevolved mitonuclear genotypes is most likely a consequence of selecting individuals based on variation in a fitness-related trait that has been correlated with mitochondrial performance in this species (30).…”

“…Additionally, we observed little evidence for allele frequency variation consistent with nuclear-only effects. If these potential effects are examined as in Lima et al (32), only frequency variations on chromosome 8 in fast developers and on chromosome 11 in slow developers may be indicative of modest effects of nuclear genetic variation alone. Yet, deviations favoring coevolved alleles in fast developers were rarely symmetrical between the reciprocal crosses.…”

“…6000 (Illumina, San Diego, CA). Sequencing reads were trimmed and filtered as in Lima et al (32) and mapped to the SD T. californicus reference genome v2.1 and an updated reference genome for the SC population (22) with BWA MEM v0.7.12 (48). Allele frequencies at fixed SNPs between the parental populations were determined with PoPoolation2 (49) as described elsewhere (32,41).…”

Speciation and the developmental alarm clock

“…Genes that act cell non-autonomously, as for secreted proteins or diffusible signaling molecules, may tend to evolve slower if they also tend to exhibit greater expression breadth and lower modularity, unless they are predisposed to co-evolutionary dynamics. Reproductive isolation between species need not only involve classic regulators of development, however, as attested by incompatibilities that commonly seem to involve chromosome segregation and cyto-nuclear interactions (Blackman 2016, Lima et al 2019.…”

“…and mito-nuclear incompatibilities can provide important reproductive barriers between species(Hill 2015, Lima et al 2019. To the extent that some developmental stages may be more sensitive to the disruption of chromosome segregation or mitochondrial function, such as phases of heightened cell division or metabolism, such developmentally-tangential genetic pathways might nevertheless contribute to ontogenetic patterns of hybrid dysfunction.Gene duplication and gene origination:Gene duplication is a powerful factor in the evolution of phenotypic novelty(Kaessmann 2010).…”