A Mitochondrial Mystery: Why are there two deeply divergent lineages in the Savannah Sparrow?

Genetic study searches for the most likely scenario to explain this peculiar pattern.

Does the name John Avise ring a bell? The work of this American biologist laid the foundation for phylogeography, the study of historical processes responsible for the present-day geographic distributions of populations. In the early days, phylogeographic research relied heavily on mitochondrial DNA (mtDNA), the circular genome of mitochondria (the powerhouses of the cell). The study of this molecular marker revealed many peculiar patterns, such as deeply divergent lineages within a single species. A recent study in the journal Molecular Ecology tries to explain such a pattern in the Savannah Sparrow (Passerculus sandwichensis).

A Savannah Sparrow in Ontario, Canada © Mdf | Wikimedia Commons

 

Five Possible Scenarios

Previous work on the Savannah Sparrow uncovered two divergent mtDNA lineages (A and B) within a largely panmictic population. Lineage B clusters with a third clade (C) which contains several subspecies (beldingi, rostratus and sanctorum) from northwestern Mexico. However, the focus of this study is on lineages A and B which occur in the nominate subspecies sandwichensis. What could explain this pattern? Here are five possible explanations:

1. Selection for both mtDNA haplotypes
2. Sex-biased dispersal (mtDNA is only transmitted through the female line)
3. Introgression of mtDNA is much quicker than nuclear introgression
4. Independent sorting of mtDNA haplotypes in a large population
5. Complete admixture of two previously isolated populations

The first two explanations can already be discarded. There was no evidence for selection based on statistical tests (specifically the McDonald-Kreitman test) in previous work. And it is unlikely that Savannah Sparrows have sex-specific differences in dispersal. That leaves three possibilities. Enter Phred Benham and Zachary Cheviron, who used genomic data to resolve this mitochondrial mystery.

The deeply divergent mtDNA lineages (A and B) in the Savannah Sparrow. The distribution on the map already shows a lack of geographical structure. What is going on here? (from: Benham & Cheviron 2019 Molecular Ecology).

 

No Population Structure

First, the researchers looked at population structure. If the divergent mtDNA lineages are the outcome of past population division, this should be clear in the nuclear genome. This was, however, not the case. The Savannah Sparrow showed a lack of population structure despite the fact that their breeding distribution runs from Alaska to California, New Mexico, and Virginia. This finding indicates that scenario 3 (differential introgression of mtDNA and nuclear DNA) can be ruled out. Lower levels of nuclear introgression would have resulted in some population structure.

No population structure in the Savannah Sparrow (the cluster of blue dots). Other colors represent Mexican subspecies. Picture by © Cephas | Wikimedia Commons

 

Large Population Size

To discriminate between the last two scenarios, the researchers performed some demographic modelling (using the software δaδi). They simulated numerous scenarios and compared the resulting patterns with the actual data. These analyses supported the idea that the divergent mtDNA lineages arose in a large, panmictic population.

The researchers couldn’t get enough of simulations and explored the demographic conditions under which divergent lineages can develop. This exercise revealed that really large populations – effective population size (Ne) > 350,000 – are needed. This conclusion fits with other avian examples, such as the Passenger Pigeon (Ectopistes migratorius). This extinct species is known for its enormous flocks (Ne has been estimated at 13 million) and also showed deeply divergent mtDNA lineages.

The large effective population size of the Passenger Pigeon can explain the existence of divergent mtDNA lineages in this extinct species. Left: stuffed specimen at James St. John at the Field Museum of Natural History, Chicago, Illinois, USA © James St. John | Wikimedia Commons. Right: Passenger pigeon flock being hunted in Louisiana. The Illustrated Shooting and Dramatic News. © Smith Bennett | Wikimedia Commons

 

Pleistocene

This study suggests that the Savannah Sparrow maintained a constant population size throughout the Pleistocene ice ages. This situation is different from other bird species that show population subdivision during this period. How the Savannah Sparrow managed to resist population contraction and fragmentation remains to be investigated. But it seems likely that this generalist thrived in the continuous band of grasslands, tundra and steppe that ran across the southern edge of advancing glaciers.

 

References

Benham P.M. & Cheviron Z.A. (2019) Divergent mitochondrial lineages arose within a large, panmictic population of the Savannah sparrow (Passerculus sandwichensis). Molecular Ecology.

 

This paper has been added to the Passerellidae page.