Adaptation or chance?

Claire Armstrong unravels the evolution of bill length and malaria resistance in an island bird.

Check out the full paper here

Islands are great

Islands are excellent places for studying evolution. Darwin’s encounters with finches in the Galápagos Islands helped establish his ideas of evolution by natural selection. Each island has its own history of colonisations and extinctions, creating many unique habitats to which new species can adapt. Together with isolation and low levels of dispersal between islands, this often results in high levels of endemism (where a species is found in only one location) throughout island archipelagos. For scientists, islands can be used as “natural laboratories” to explore the role of natural selection across discrete island populations.

My particular island species is a small brown bird called Berthelot’s pipit (Anthus berthelotii), found across three archipelagos off the coast of Africa. This bird was named after the French naturalist Sabin Berthelot, who spent years studying the natural history of the Canary Islands. Berthelot’s pipits spend much of their time foraging for invertebrates in open habitats, dashing across the ground in a manner that has earned them the local nickname of “Corre camino”, which translates as “Roadrunner”.

Fig 1

A Berthelot’s pipit keeping a look-out. Photo © Philip Lamb

A brief history of pipits

Berthelot’s pipits first evolved in the Canary Islands at some point in the last two million years, after an initial colonisation by their mainland ancestors. They were pretty happy staying put until around 8,000 years ago, when several birds crossed hundreds of miles of ocean northwards to settle in Madeira and Selvagens. Since then, there’s been a lack of movement between the archipelagos, which could pave the way for population divergence and speciation.

Fig 2

Left: Berthelot’s pipit colonisations of Madeira and Selvagens from the Canary Islands. Right: the geographic range of Berthelot’s pipits (white box).

We’re interested in finding out the drivers of divergence: are genetic and physical differences between populations caused by adaptation to different habitats, or are they a result of neutral forces? Genetic drift (random fluctuations in genetic variation between generations) and founder effects (the loss of genetic variation during the establishment of a new population by a small number of founding individuals) can result in large genetic divergence between isolated populations, without the need for natural selection.

Bill length and malaria resistance: ecologically important traits

The Berthelot’s pipits of Madeira are described as a separate subspecies, Anthus berthelotii madeirensis, with longer bills in the Madeiran pipits. Research in many other bird species points to a key role of diet and feeding behaviour in shaping the evolution of bird bill morphology, so we predicted that variation in bill length in Berthelot’s pipits could be driven by adaptation to different food sources between the archipelagos. Alternatively, founder effects, followed by isolation and genetic drift, might have been more important for shaping these differences.

Fig 3

Adapting to new diets creates many different bill shapes. Illustration © Glen McBeth

As well as bill morphology, we’re also interested in the evolutionary relationship between Berthelot’s pipits and their pathogens. Parasites, viruses, and other pathogens can drive the evolution of high levels of genetic diversity in genes that provide immunity for the host, to help defend it from rapidly evolving pathogen communities. Avian malaria, caused by parasites in the Plasmodium genus, is a disease which has been devastating for Hawaiian bird populations where it has been recently introduced. In populations with a longer evolutionary history with Plasmodium, avian malaria can reduce survival, body condition, and the number of offspring raised. Infection rates of avian malaria in Berthelot’s pipits vary from island to island, and we want to find out if this is driving selection for different immune defence traits between populations.

What we did

Over the course of two field seasons in 2006 and 2009, we caught Berthelot’s pipits throughout their range, collected blood samples, and measured various physical traits including bill length. Back in the lab, we extracted DNA from the blood samples, and tested these to find out which birds had contracted avian malaria. We then sequenced the DNA of each bird to detect thousands of genetic variants situated throughout the pipit genome.

The next step was to use our set of genetic variants to look for regions of the genome that showed associations with bill length and malaria infection. This looks for variants that are strongly correlated with the trait, for example if individuals with the genotype “AA” have long bills, “AG” have intermediate bills, and “GG” have short bills, then that variant would be associated with bill length.

We found an association with bill length close to a gene which influences bill shape in Darwin’s finches and chickens, so this gene could potentially be affecting bill length in Berthelot’s pipits as well. We investigated whether this genomic region was evolving via divergent selection between the short- and long-billed subspecies. This revealed that the variation at this region, and therefore variation in bill length, was instead shaped by founder effects and genetic drift arising from the colonisation history of Berthelot’s pipits.

The two genetic variants showing the strongest associations with avian malaria infection were situated next to or within genes that play a role in the human immune response, so could have important effects on the ability of Berthelot’s pipits to respond to infection. This association varied between islands, suggesting that evolution of malaria resistance is constantly changing, as we might expect for host-pathogen coevolution.

Finally, we found signatures of divergent selection between the two subspecies at genetic variants situated within genes that have been associated with immune function and metabolism. Though we didn’t find consistent differences between the subspecies for malaria infection, there may be other pathogens that are causing divergent selection between Berthelot’s pipit subspecies. Additionally, selection for traits related to metabolism could indicate adaptation to different climatic conditions between northern and southern populations. Our next step is to sequence whole genomes of several Berthelot’s pipits, which will let us investigate the roles of adaptation and genetic drift in shaping genetic variation in much finer detail.

claireClaire Armstrong is a UEA PhD student funded by the NERC EnvEast Doctoral Training Partnership. Her research uses Berthelot’s pipits as a wild study system for understanding the genomics of adaptation, and how pathogens influence the genetic variation of their hosts. Claire can be found on Twitter @ClaireArmstro.