Holy mitonuclear co-evolution Robin! Supergene explains local adaptation to divergent climates

Genomic research on the Eastern Yellow Robin reveals a mechanism for local climate adaptation in the absence of a geographical barrier.

Gene jargon makes my head spin, but when I read that there was a species-level difference in mitochondrial DNA between Eastern Yellow Robins living on either side of the Blue Mountains, I was keen for more. Not because I have a particular affinity for mitochondria, even though they are the energy generators of cells, controlled by a separate genome from that of the nucleus*, or because the Eastern Yellow Robin is one of my favourite birds.

No, I was intrigued because birds fly, and Eastern Yellow Robins have an uninterrupted distribution across the Great Dividing Range – for them it is only a hill. So how could there be a trans-Divide split in their mitochondrial genome, a pattern consistent along the whole east coast of Australia, while variation in their nuclear genome is minimal from the coast to the inland? I therefore jumped at the opportunity to assist the Monash University group, especially Ph.D. student Hernan Morales, in the continuation of their research.

Hernan and I set out with mist-nets and song playback to capture Eastern Yellow Robins along a transect from Sydney to Parkes. I supplied a vehicle, catching gear, camping gear and provisions, while Hernan’s bottomless backpack produced needles, vials, preservatives, a laptop, light source – even a spectrometer! All of the birds we captured were released alive, albeit as involuntary micro-blood donors, and after a week in the field Hernan hopped back on the plane with the precious DNA samples. He and Nevil Amos subsequently sampled a replicate trans-Divide transect in Victoria.

Both transects confirmed the mitochondrial split across a remarkably narrow zone just west of the mountains. On our northern transect, some birds with each mitochondrial type were found together at a site near Portland (NSW), but just 30 km either side of this point of overlap, mitogenomes were distinct. So distinct in fact, that had we just analysed the mitochondrial genome alone, we might have considered them separate species.

At first it seemed that the nuclear genome varied little across the transect, but when Hernan looked closely at a smaller subset of genes – those under selection – he had a Eureka moment. There were large differences in this subset of genes between coastal and inland birds, and by mapping them to the best bird genome available (the Zebra Finch), he discovered that these genes were clustered as a sort of “supergene” on one chromosome. This chromosomal region is rich in genes that control the mitochondria (- and yes, mitochondria are controlled by both mitochondrial and nuclear genes).

So Hernan had discovered that the mitochondrial genes and the nuclear genes controlling the mitochondria have co-evolved – time to get excited! Here at last is an explanation of how species-level differences in mitochondrial DNA can be maintained in the face of gene flow, in an animal for which a small mountain range does not present a physical barrier.

While the Great Dividing Range is not a barrier to movement, it appears to be a barrier to physiology. The wetter, eastern side of the range presents a different metabolic landscape to the drier western side. And the metabolism of Eastern Yellow Robins appears to be fine-tuned through “mitonuclear co-evolution”. Birds with mismatched mitochondrial and nuclear genomes are expected to be physiologically inferior, providing a strong selection pressure to maintain the mitochondrial partitioning.

A few ‘naughty’ birds with mismatched mitonuclear genomes were identified in the contact zone, but we suspect that their survival or ability to reproduce is inferior. My co-authors Paul Sunnucks and Sasha Pavlova will be taking this further, given the likely importance of this mechanism in the early stages of speciation. Personally, having had my question answered - I’ll be heading back into my ”whole-animal” comfort zone. And even Hernan has moved on to work on speciation in marine snails in Sweden, though I’m sure this mechanism will be forefront in his mind.

Richard Major (Principal Research Scientist, AMRI, Australian Museum)

More information

• Morales, H. E., A. Pavlova, N. Amos, R. Major, A. Kilian, C. Greening, and P. Sunnucks. 2018. Concordant divergence of mitogenomes and a mitonuclear gene cluster in bird lineages inhabiting different climates. Nature Ecology & Evolution
• Pavlova, A., J. N. Amos, L. Joseph, K. Loynes, J. J. Austin, J. S. Keogh, G. N. Stone, J. A. Nicholls, and P. Sunnucks. 2013. Perched at the mito-nuclear crossroads: divergent mitochondrial lineages correlate with environment in the face of ongoing nuclear gene flow in an Australian bird. Evolution 67: 3412-3428. 

* Most complex organisms have two independent genomes in every cell, both of which code for the production of proteins. One is the mitochondrial genome, which regulates the chemical pathways that generate essential energy for the cell, and the second is the nuclear genome comprising the chromosomes wound up tightly within the cell nucleus. The nuclear genome (~ 1200 megabase pairs in birds) is much larger than the mitochondrial genome (~0.017 megabase pairs). While eggs are whole cells and therefore contain mitochondria, sperm are effectively only cell nuclei. This means that the mitochondrial genome is inherited only from the mother, while the nuclear genome is inherited from both parents.