Mitochondrial Evolution and the Mitonuclear Compatibility Species Concept
Interest in animal ornamentation leads inexorably to interest in speciation. Taxonomists use ornamental traits to sort avian populations into species, and sexual selection is proposed to play a central role in the process of speciation in complex animals. The growing focus of my lab group on the coadaptation of mitochondrial genes and nuclear genes to achieve mitochondrial function and core respiration has presented new thinking about the nature of metazoan species and why a mitochondrial gene (COX1) works so well as an animal DNA barcode. We focus on the genomic architecture of the eukaryotes wherein mitochondrial and nuclear genes must function in tight coordination to produce the complexes of the electron transport chain and enable cellular respiration. Coadaptation of these interacting gene products is essential for organism function
and coadaption can only be maintained through perpetual coevolution of mitochondrial and nuclear genes. Mitonuclear coevolution in isolated populations leads to speciation because population-specific mitonuclear coadaptations create between-population mitonuclear incompatibilities and hence barriers to gene flow between populations. Mitonuclear compensatory coevolution may play a key role in this process. In addition, selection for adaptive divergence of products of mitochondrial genes, particularly in response to climate or altitude, can lead to rapid fixation of novel mitochondrial genotypes between populations and consequently to disruption in gene flow between populations as the initiating step in animal speciation. This line of research has led to a new species concept:
THE MITONUCLEAR COMPATIBILITY SPECIES CONCEPT
A species is a population that is genetically isolated from other populations by incompatibilities in uniquely coadapted mt and nuclear genes.
We are working to test these ideas by looking at mitochondrial function and ornamentation in birds and copepods. Speciation in relation to mitonuclear genotype, mitochondrial function, and ornamentation will be a focus of lab research in upcoming years.
Key recent citations related to speciation from the Hill Lab:
Hill, G. E. and Powers, M. J. 2021. Ecomorphs are not species: the case of the Cassia Crossbill. J. Avian Biology 2021: e02896
Hill, G. E. 2020. Genetic hitchhiking, mitonuclear coadaptation, and the evolution of mitochondrial genomes. Ecology and Evolution 10: 9048-9059.
Hill, G. E. 2020. Mitonuclear Compensatory Coevolution. Trends in Genetics 36: 403-414.
Justyn, N., Callaghan, C. T., and Hill, G. E. 2020. Birds rarely hybridize: a citizen science approach to estimating rates of hybridization in the wild. Evolution
Hill, G. E. 2019. Reconciling the mitonuclear compatibility species concept with rampant mitochondrial introgression. Integrative and Comparative Biology59: 912–924.
Hill, G. E. and Zink, R. M. 2018. Hybrid speciation in birds, with special reference to Darwin's finches. Journal of Avian Biology
Hill, G. E. 2017. The mitonuclear compatibility species concept. Auk: Ornithological Advances 134: 393–409.
Hill, G. E. 2016. Mitonuclear coevolution as the genesis of speciation and the mitochondrial DNA barcode gap. Ecology and Evolution, 6(16), 5831-5842. doi:10.1002/ece3.2338
Hill, G. E. 2015. Selection for reinforcement versus selection for signals of quality
and attractiveness. Ideas in Ecology and Evolution 8:67-69.
Hill, G. E. 2015. Mitonuclear Ecology. Molecular Biology and Evolution
32 (8): 1917-1927. doi: 10.1093/molbev/msv104.