Evaluating evidence of mitonuclear incompatibilities with the sex chromosomes in an avian hybrid zone

Abstract

The exploration of hybrid zones and the intergenomic conflicts exposed through hybridization provide windows into the processes of divergence and speciation. Sex chromosomes and mitonuclear incompatibilities have strong associations with the genetics of hybrid dysfunction. In ZW sex‐determining systems, maternal co‐inheritance of the mitochondrial and W chromosomes immediately exposes incompatibilities between these maternal contributions of one species and the Z chromosome of another. We analyze mitochondrial and Z chromosome admixture in the long‐tailed finch (Poephila acuticauda) of Australia, where hybridizing subspecies differ prominently in Z chromosome genotype and in bill color, yet the respective centers of geographic admixture for these two traits are offset by 350 km. We report two well‐defined mitochondrial clades that diverged ∼0.5 million years ago. Mitochondrial contact is geographically co‐located within a hybrid zone of Z chromosome admixture and is displaced from bill color admixture by nearly 400 km. Consistent with Haldane's rule expectations, hybrid zone females are significantly less likely than males to carry an admixed Z chromosome or have mismatched Z‐mitochondrial genotypes. Furthermore, there are significantly fewer than expected mitonuclear mismatches in hybrid zone females and paternal backcross males. Results suggest a potential for mitonuclear/sex chromosome incompatibilities in the emergence of reproductive isolation in this system.

Gene expression in male and female stickleback from populations with convergent and divergent throat coloration

“…In a hybrid zone of a bird, the long‐tailed finch Poephila acuticauda , TTC39B cosegregates with carotenoid‐based bill color. This led Hooper et al ( 2019 ; also see Lopez et al, 2021 ) to hypothesize that, since carotenoids are hydrophobic and require a lipoprotein partnership to be transported to their tissue of deposition, TTC39B may play such a role. At a much broader taxonomic scale, a different Tetratricopeptide Repeat gene, RCP2 , regulates carotenoid accumulation and coloration in monkeyflowers (Stanley et al, 2020 ).…”

Experimentally testing mate preference in an avian system with unidirectional bill color introgression

“…The long‐tailed finch Poephila acuticauda is an Australian estrildid finch characterized by a yellow‐billed subspecies in the West ( P. a. acuticauda ) and a red‐billed subspecies in the East ( P. a. hecki ) that come into secondary contact on the eastern edge of the Kimberley Plateau (Figure 1a , Hooper et al, 2019 ). In addition to their difference in bill color, subspecies are also distinct in their nuclear and mitochondrial genomes (Hooper et al, 2019 ; Lopez et al, 2021 ), and to some degree in their songs (Zann, 1976 ) and sperm size (Rowe et al, 2015 ). The respective geographic centers of genetic and bill color admixture are significantly displaced from each other: the hybrid zone for bill color (as well as three candidate genes underlying variation in this trait) is located 350 km east of the hybrid zone for the vast majority of the genome (Hooper et al, 2019 ; Lopez et al, 2021 ).…”

“…In addition to their difference in bill color, subspecies are also distinct in their nuclear and mitochondrial genomes (Hooper et al, 2019 ; Lopez et al, 2021 ), and to some degree in their songs (Zann, 1976 ) and sperm size (Rowe et al, 2015 ). The respective geographic centers of genetic and bill color admixture are significantly displaced from each other: the hybrid zone for bill color (as well as three candidate genes underlying variation in this trait) is located 350 km east of the hybrid zone for the vast majority of the genome (Hooper et al, 2019 ; Lopez et al, 2021 ). Genetic analyses suggest that variation for yellower bills has introgressed from subspecies acuticauda into subspecies hecki (Hooper et al, 2019 ; Lopez et al, 2021 ).…”

“…The respective geographic centers of genetic and bill color admixture are significantly displaced from each other: the hybrid zone for bill color (as well as three candidate genes underlying variation in this trait) is located 350 km east of the hybrid zone for the vast majority of the genome (Hooper et al, 2019 ; Lopez et al, 2021 ). Genetic analyses suggest that variation for yellower bills has introgressed from subspecies acuticauda into subspecies hecki (Hooper et al, 2019 ; Lopez et al, 2021 ). Given that bill color in the long‐tailed finch is an oligogenic trait—that is, heritable variation is seemingly governed by only a small number of genes—(Hooper et al, 2019 ) and has a steep phenotypic cline, it is unlikely that stochasticity alone is responsible for this apparent unidirectional introgression of bill color.…”

Developmental rate displays effects of inheritance but not of sex in inter-population hybrids ofTigriopus californicus

“…The heritability of this trait variation among hybrid individuals is potentially another important factor determining if mitonuclear incompatibilities can create strong barriers for gene flow between populations, and to our knowledge, the transmission of incompatibilities across generations has not been directly assessed. Additionally, it is possible for the effects of mitonuclear incompatibilities to vary between females and males (Jelić et al, 2015, Mossman et al, 2016b; Đorđević et al, 2017; Hoekstra et al, 2018, Carnegie et al, 2021; Erić et al, 2022), which may be the result of genetic interactions involving sex determining loci (e.g., heterologous sex chromosomes; Lopez et al, 2021), or of the predominantly maternal inheritance of mitochondrial DNA in metazoans (e.g., Giles et al, 1980). For example, the ‘mother’s curse’ hypothesis posits that mutations in mitochondrial DNA causing beneficial interactions in females will accumulate, even if they cause negative interactions in males, due to the lack of paternal transmission of mitochondrial DNA (Frank & Hurst, 1996; Gemmell et al, 2004).…”