About the author
Ben Wiens is a Ph.D. candidate in the Mammal Division of the Biodiversity Institute at the University of Kansas, working in Dr. Jocelyn Colella’s lab. He is broadly interested in using natural history collections and genomic data to study the process of speciation, especially when barriers to gene flow remain incomplete. His current work is focused on elucidating the evolutionary processes that have resulted in differential introgression across the nuclear and mitochondrial genomes in North American red-backed voles (Clethrionomys). You can learn more about his research at his website.
Why is mitochondrial introgression so frequently observed in nature?
Mitochondrial genomes encode for 13 genes that play essential roles in energy metabolism, heat production, and numerous other organismal processes (Calvo et al., 2016). Yet those 13 genes are not enough to fully carry out mitochondrial processes and must interact with an additional ~1200 nuclear genes (N-mt genes) for proper functioning (Hill, 2015). As such, mitochondrial genes and N-mt genes are expected to be heavily co-evolved; indeed, laboratory crosses have demonstrated many examples of highly disadvantageous and/or lethal mitonuclear incompatibilities in hybrid offspring (e.g. Moran et al., 2024; Pereira et al., 2021). Given these findings, we might expect mitonuclear discordance to be rare in nature, but on the contrary, there are numerous examples of mitochondrial introgression across the tree of life (Toews & Brelsford, 2012). This leads to such questions as:
- What accounts for the discrepancy between expectations based on lab crosses and observations in nature?
- Are there mechanisms through which populations can quickly adapt to mitochondrial introgression?
- Are there cases where the benefits of mitochondrial introgression outweigh the costs?
Unidirectional mitochondrial introgression: the case of red-backed voles
In the high-latitudes of North America, two species of red-backed voles meet to form a broad contact zone spanning east-to-west across much of the continent. The northern red-backed vole (Clethrionomys rutilus) occurs across the subtundra of Eurasia and North America, whereas the southern red-backed vole (C. gapperi) inhabits coniferous and mixed forest habitats of North America. They meet in the northern boreal forests of Southeast Alaska (SEAK), British Columbia (BC), and Northwest Territories (NWT), and the parapatric nature of these species’ distributions has long led to speculation about possible hybridization. Small crossing experiments performed in the 1970s and genetic studies in the 2000s using one or two loci confirmed hybridization was possible, but the extent of nuclear admixture remained unknown (McPhee, 1977; Runck et al., 2009).
To increase our understanding of hybridization in this system, I generated RADseq data for 266 individuals from three contact zones (SEAK, BC, and NWT). I was able to recover nuclear and mitochondrial RAD loci, and discovered that despite rampant mitonuclear discordance in SEAK and BC, admixture in the nuclear genome was minimal. Additionally, mitochondrial introgression only occurred in one direction: out of 266 individuals, 69 had C. rutilus mitogenomes paired with C. gapperi nuclear genomes, but none had the reverse combination. Despite widespread mitochondrial introgression of the C. rutilus mitochondrial genome, <5% of the C. rutilus nuclear genome appeared to have introgressed. This signal of nuclear introgression was strongest at the center of the contact zone in BC, and barely detectable at all in SEAK. Interestingly, the introgressed mitochondrial genome in SEAK formed a distinct clade, distinct from all other C. rutilus mitochondria. By linking intra-specific population structure within each species with patterns of deglaciation since the Last Glacial Maximum (~22 kya), my data suggest that introgression was initiated in SEAK before BC, and that while contact has since ceased in SEAK, it remains ongoing in BC.
Using whole genomes to test for adaptation to discordance
With support from an EECG award, I am addressing questions about mitochondrial introgression in this system in more detail by generating whole genome resequencing data for ~90 individuals. I will start by searching for signals of mitonuclear co-introgression, specifically at N-mt genes. My RADseq data showed small proportions of nuclear introgression in BC, but is it the same loci in the nuclear genome introgressing in every individual? And if so, are those loci associated with mitochondrial functioning? This would suggest that when mitochondrial introgression is recent, the easiest way to adapt is through co-introgression of critical N-mt genes. In contrast, the apparent lack of nuclear introgression in SEAK suggests that after enough time, heterospecific mitochondrial and nuclear genes may be able to adapt to each other, such that co-introgression of N-mt genes is no longer required. I will perform genomic scans for selection and tests for adaptive evolution to search for genes that have evolved in response to mitochondrial introgression. Results from this system will build our understanding of how and why mitochondria are able to so frequently move across species barriers.
References
Calvo, S. E., Clauser, K. R., & Mootha, V. K. (2016). MitoCarta2.0: An updated inventory of mammalian mitochondrial proteins. Nucleic Acids Research, 44(D1), D1251–D1257. https://doi.org/10.1093/nar/gkv1003
Hill, G. E. (2015). Mitonuclear Ecology. Molecular Biology and Evolution, 32(8), 1917–1927. https://doi.org/10.1093/molbev/msv104
McPhee, E. (1977). Parapatry in Clethrionomys; Ethological Aspects of Mutual Exclusionin C. gapperi and C. rutilus.
Moran, B. M., Payne, C. Y., Powell, D. L., Iverson, E. N. K., Donny, A. E., Banerjee, S. M., Langdon, Q. K., Gunn, T. R., Rodriguez-Soto, R. A., Madero, A., Baczenas, J. J., Kleczko, K. M., Liu, F., Matney, R., Singhal, K., Leib, R. D., Hernandez-Perez, O., Corbett-Detig, R., Frydman, J., … Schumer, M. (2024). A lethal mitonuclear incompatibility in complex I of natural hybrids. Nature, 626(7997), Article 7997. https://doi.org/10.1038/s41586-023-06895-8
Pereira, R. J., Lima, T. G., Pierce-Ward, N. T., Chao, L., & Burton, R. S. (2021). Recovery from hybrid breakdown reveals a complex genetic architecture of mitonuclear incompatibilities. Molecular Ecology, 30(23), 6403–6416. https://doi.org/10.1111/mec.15985
Runck, A. M., Matocq, M. D., & Cook, J. A. (2009). Historic hybridization and persistence of a novel mito-nuclear combination in red-backed voles (genus Myodes). BMC Evolutionary Biology, 9(1). https://doi.org/10.1186/1471-2148-9-114
Toews, D. P. L., & Brelsford, A. (2012). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21(16), 3907–3930. https://doi.org/10.1111/j.1365-294X.2012.05664.x
About the EECG
The American Genetic Association grants EECG Research Awards to graduate and post-doctoral researchers who are at a critical point in their research, where additional funds would allow them to conclude their research project and prepare it for publication.
These awards are open to any graduate student or postdoctoral fellow who is a member of the American Genetic Association at the time of application.
Awards are for up to $6,000.