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 F 2 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 (46 Â ) than digenic interactions. This alternative system thus allows important comparisons to studies of the genetics of reproductive isolation in more standard model systems.

Systematic analysis of complex genetic interactions

“…For example, the number, magnitude, and properties of digenic and trigenic interactions clarifies aspects of speciation theory in evolutionary biology (36, 37). Hybrids between species exhibit reduced fitness, which is usually attributed to negative (‘epistatic’) interactions among genes that diverged in isolated populations.…”

Incompatibility between Nuclear and Mitochondrial Genomes Contributes to an Interspecies Reproductive Barrier

“…Although DM incompatibilities were originally linked to interactions between nuclear genes, miscommunication between nuclear and mitochondrial genomes has been implicated in yeast (Lee et al, 2008), drosophila and other insects (Dickman and Moehring, 2013; Foley et al, 2013), fish (Bolnick et al, 2008; Niehuis et al, 2008) and in primate xenomitochondrial cybrid cell lines (Bayona-Bafaluy et al, 2005). Previous studies in drosophila found male-specific infertility associated with mitochondrial polymorphism (Clancy et al, 2011; Innocenti et al, 2011).…”

Metapopulation patterns of additive and nonadditive genetic variance in the sea bass (Dicentrarchus labrax)

“…(2005). Situations in which polygenic sex determination mediated by mtDNA effects could generate striking changes in sex ratio among distinct hybrid crosses have just begun to be explored in T. californicus (Alexander et al., 2015; Foley, Rose, Rundle, Leong, & Edmands, 2013) and in freshwater fish species ( Cottus sp . ; Cheng, Czypionka, & Nolte, 2013).…”