Publishers of the Journal of Heredity
Join the AGA

EECG Embarkation: Mito-nuclear coevolution in the Savannah sparrow, a species with deeply-divergent and broadly sympatric mitochondrial lineages

About the Author

Dr. Phred Benham is a post-doctoral researcher at the Museum of Vertebrate Zoology, University of California Berkeley with Dr. Rauri C. K. Bowie. Phred is broadly interested in the evolutionary mechanisms shaping avian adaptation to different environments. You can follow his research on his website and on mastodon.

Eukaryotic organisms like plants, animals, and fungi, rely on a very old partnership between their own cells and tiny bacteria-like structures called mitochondria. These mitochondria have their own genome, and are crucial for a process called cellular respiration. Unlike the eukaryotic nuclear genome (with paired chromosomes capable of recombination), mitochondrial genomes are unpaired and generally lack recombination. This can lead to a problematic build up of deleterious mutations in the mitochondrial genome. To combat this, nuclear genes interacting with the mitochondrial genes may have to compensate. This co-evolution between nuclear and mitochondrial genomes can drive divergence between species and lead to incompatibilities if the mitochondrial genome of one species is introduced into the nuclear genome of another through hybridization (Burton & Barreto 2012). Strangely, evidence for mitochondrial genes jumping from one species to another is commonly observed in nature (Toews & Brelsford 2012). If changes in genes between the main cell and the mitochondria can lead to problems, why do we see this genome-swapping happening so often (Sloan et al. 2016)?

Figure 1: Savannah sparrow (Passerculus sandwichensis). Photo by Phred M. Benham.

To understand this, my research focuses on a bird called the Savannah sparrow (Passerculus sandwichensis). I started studying these sparrows during my PhD because they are distributed widely across North America (Figure 1), offering a great opportunity to study how they adapt to different environments. I began by looking at the DNA of these birds to understand their history and genetic makeup. Previous research showed that these sparrows have two divergent mitochondrial gene groups (clades) occurring within populations across North America, with a third clade in one region of Mexico (Zink et al. 2005). However, when I looked at the nuclear genome using a method called RADseq, there was no difference among populations in the nuclear genes except in that same region of Mexico (Figure 2; Benham & Cheviron 2019). The presence of divergent mitochondrial genes interacting with the same nuclear genes in Savannah sparrows provides a natural experiment to figure out whether these mitochondrial changes are a problem or not.

Figure 2: Contrasting patterns of mitochondrial and nuclear DNA variation across the distribution of Savannah sparrows. (a) Mitochondrial phylogeny. (b) Mapped distribution of the three ND2 clades recovered by phylogenetic analyses. (c) Population structure in the nuclear genome estimated using RADseq data. Main division is between Nominate savannah sparrows (mtDNA clades A & B) and Mexico (mtDNA clade C) with a contact zone at Morro Bay on the central California coast. Data from Benham & Cheviron 2019.

There are a few reasons why mitochondrial genes might diverge without the rest of the nuclear genome. IGenes from another lineage of birds may have mixed in or the sparrows in that region have simply had different mitochondrial genes for a long time. Determining the source of this divergence is challenging, but demographic analyses point to the latter scenario for Savannah sparrows. Regardless, the maintenance of these divergent mitochondrial genomes allows for investigation into distinct hypotheses. First, this divergence could be functionally neutral due to strong purifying selection eliminating nuclear incompatibilities (functional neutrality). Alternatively, mutations may have accumulated and resulted in compensatory changes in the nuclear genome to maintain function (nuclear compensation).

With support from the AGA’s EECG award, I plan to evaluate these two hypotheses using genomic data from Savannah sparrows. I will sample many sparrows from one region in Wyoming and other places across the species distribution. I aim to:

  1. Look for signals of increased purifying selection in Savannah sparrows compared to other bird species.
  2. See if changes in certain amino acids in the genes could affect how proteins work.
  3. Test if there’s a strong connection between the mitochondrial genes and nuclear genes that work together.

Finding strong evidence of purifying selection, few amino acid substitutions, and a lack of significant associations between nuclear and mitochondrial genomes will support the first hypothesis (functional neutrality). If I find reduced purifying selection, evidence for alterations to protein function by amino acid substitutions, and significant associations between the mitochondrial genome and regions of the nuclear genome enriched for mitochondrial-interacting genes, it will point to the second hypothesis (nuclear compensation). These findings will provide an exciting opportunity to help us understand how mitochondrial and nuclear genes work together in different environments and situations.



Benham, PM, Cheviron, ZA (2019). Divergent mitochondrial lineages arose within a large, panmictic population of the Savannah sparrow (Passerculus sandwichensis). Molecular Ecology. 28: 1765-1783.

Burton, RS, Barreto, FS (2012). A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities? Molecular Ecology. 21: 4942-4957. 

Sloan, DB, Havird, JC,  Sharbrough, J (2016). The on-again-off-again relationship between mitochondrial genomes and species boundaries. Molecular Ecology. 26: 2212-2236.

Toews, DPL, Brelsford, A (2012). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology. 21: 3907-3930. 

Zink, RM, Rising, JD, Mockford, S, Horn, AG, Wright, JM, Leonard, M, Westberg, MC (2005). Mitochondrial DNA Variation, Species Limits, and Rapid Evolution of Plumage Coloration and Size in the Savannah Sparrow. The Condor. 107: 21-28.

Subscribe to Our Blog