How Do Darwin’s Finches Change Their Beak Size So Quickly? | @GrrlScientist

Epigenetics may be how Darwin’s finches rapidly change their beak size and shape in response to sudden environmental changes, such as drought or human disturbance, in the absence of gene mutations

by GrrlScientist for Forbes | @GrrlScientist

This piece was a Forbes editor’s pick.

A small ground finch (Geospiza fuliginosa; left) and a medium ground finch (Geospiza fortis; right) at the rural study site. (Credit: Sabrina McNew | doi:10.1186/s12862–017–1025–9)
“Seeing this gradation and diversity of structure in one small, intimately related group of birds, one might really fancy that from an original paucity of birds in this archipelago, one species had been taken and modified for different ends.”
— Charles Darwin, in Voyage of the Beagle, 2nd ed., (1845), p. 380.

How does a population adapt to sudden changes in the environment? According to the most widely accepted paradigm, random genetic changes (mutations) are the source of heritable changes in a plant or animal’s observable characteristics (phenotype). Phenotype, in turn, is the raw material that is acted upon by natural selection, and the most beneficial adaptations are passed on to successive generations. But there is a problem with this paradigm: adaptive genetic mutations are so infrequent that this scenario cannot adequately explain the speed at which adaptation can occur.

One well-known example of speedy adaptation is seen in “Darwin’s finches”; a group of approximately 15 bird species that live in the Galápagos Islands Archipelago, which are located on the equator in the Pacific Ocean. Ongoing field studies have documented rapid changes in these birds’ beak sizes and shapes in response to sudden environmental variations — drought, or human disturbances, for example — yet very few genetic changes have been found that accompany those physical differences between finch species, nor between populations (ref). What guides these important changes and the speed which they can occur in these iconic birds?

The process of adaptation is more subtle than originally thought

Scientists have recently become aware that adaptation is not solely dependent upon genetic mutations; it can also occur through “extra-genetic” mechanisms. At least some changes in gene function and expression patterns are independent of mutations in a gene’s DNA sequence, yet these changes may still be inherited (ref). These alterations are known as “epigenetic changes” (epi comes from the Greek, and translates as “over, outside of, around”) because these changes are in addition to changes in the DNA sequence itself. Epigenetic changes can activate or intensify, lessen or even completely silence, the activity of a particular gene without changing its DNA sequence.

Epigenetic changes can be triggered by environmental events. The changes that dominate alterations in gene expression and function are biochemical in nature, including: addition of a biochemical tag (methylation) to DNA; addition of a biochemical tag (methylation or acetylation) to the histone proteins around which DNA spools; or regulation of gene expression patterns by small RNA molecules.

Epigenetic mechanisms.
Epigenetic mechanisms are affected by several factors and processes including development in utero and in childhood, environmental chemicals, drugs and pharmaceuticals, aging, and diet. DNA methylation occurs when methyl groups — an epigenetic factor found in some dietary sources — tag DNA, thereby activating or repressing genes. Histones are proteins around which DNA can coil for compaction and gene regulation. Histone modification occurs when the binding of epigenetic factors to histone “tails” alters the extent to which DNA is wrapped around histones thereby altering the availability of genes in the DNA to activation. These alterations in gene expression or function can affect and influence a variety of traits. (Credit:
National Institutes of Health / Public domain.)

Probably the most common epigenetic modification is DNA methylation, and just as genetic mutations can be heritable, DNA methylation patterns can be heritable, too. For example, previous work found that some epigenetic variations in five closely related species of Darwin’s finches accompany genes associated with beak size and shape, as well as a number of other important physical traits (ref). We also know that changes in DNA methylation patterns are more common than DNA mutations. Based on these clues, a team of researchers, led by evolutionary ecologist Sabrina McNew, a graduate student at the University of Utah, proposed that epigenetic mutations — NOT genetic mutations — may explain how Darwin’s finches rapidly adapt to new or highly variable environments, such as those created by urbanization.

“Darwin’s finches are known for being phenotypically very variable, yet [they are] genetically pretty similar,” Ms. McNew explained in email.

“We were interested in investigating epigenetic variation between urban and rural populations [of Darwin’s finches] because other exciting recent work suggests that epigenetic mechanisms, such as DNA methylation can be a source of heritable phenotypic variation.”

Are epigenetics the secret to Darwin’s finches’ speedy adaptation?

To test this hypothesis, Ms. McNew assembled a research team and they measured physical traits (morphology) of wild birds in the field, and examined both the genetics and the epigenetics of separate populations of two Darwin’s finch species living at El Garrapatero, a relatively rural, undisturbed locality. They compared these findings to those from urban finch populations living near Puerto Ayora (Academy Bay), the largest town in the Galápagos Islands (Figure 1):

Fig. 1 Study sites and species.
a The Galápagos Archipelago. b Santa Cruz Island; Roads are indicated by narrow grey lines and study sites by red Xs. cGeospiza fortis; photo by J.A.H.K. d Geospiza fuliginosa; photo by S.A.K. Maps in (a) and (b) are modified from © 2016 Google. (Credit: Sabrina M. McNew et al., BMC Evolutionary Biology 2017 | doi:10.1186/s12862–017–1025–9)

The rural and urban study sites are separated by about 10km. Earlier long-term studies (2002–2012) established that the birds in these two finch populations stay put: only one bird (a female medium ground finch) out of 300 marked and recaptured individuals relocated between the two study sites in one decade.

“[T]he finches tend to be fairly sedentary and so we think that most of the birds we caught probably grew up at whichever site they were caught at and probably their parents lived there too,” Ms. McNew said in email.

Both sites are located on the southern and southeastern coast of Santa Cruz Island (Figure 1), and feature the same scrubby arid habitat. Despite the habitat similarities between the rural and urban sites, there is one big difference: urban-dwelling finches dine on a banquet of human foods that are new to them whereas their rural-living cousins do not (ref). And it is well-known that, historically, food is the main driver of beak size and shape in Darwin’s finches.

El Garrapatero in the Galápagos Islands. This was the rural site in this study.
(Credit: Sabrina M. McNew | doi:
10.1186/s12862–017–1025–9)

Ms. McNew and her team captured more than 1,000 individuals of two Darwin’s finch species, the medium ground finch, Geospiza fortis, and the small ground finch, G. fuliginosa (Figure 1). Age and sex were identified for each bird based on size and plumage characters, and the team measured a variety of physical characteristics, including: beak depth, width, and length; leg (tarsus) length; wing length (wing chord); and body mass. A small blood sample was collected from each finch, and a sperm sample was collected from each male. Prior to release, each bird was marked with an uniquely numbered leg-band so individuals could be tracked.

The morphological measurements revealed that medium ground finches from urban areas were larger than their rural-dwelling relatives.

“We were very surprised to see that there was morphological differences between sites for one species. These sites are fairly close to one another and urbanization, like I mentioned, only happened recently. So at least for G. fortis[medium ground finches], it seems like some environmental differences between our urban and rural sites (which are only 10km apart!) are leading to larger finches,” Ms. McNew said.

In contrast, there were no consistent differences between rural and urban populations of small ground finches. This is not surprising since previous work found that medium ground finches’ phenotypes are more variable than small ground finches’ on Santa Cruz Island, and thus, this discovery is consistent with previous findings that medium ground finches adapt more rapidly to local conditions than do small ground finches.

When genetic analyses were conducted later in the lab, the research team found few genetic mutations in the genes encoding these measured traits in rural and urban representatives of both species, and none of those mutations were consistent. Since recent work showed that changes in the copy number of genes is linked to rapid evolution in pepper moths (ref) and in primates (ref), Ms. McNew and her team looked to see whether differences in gene copy number may explain the measured differences between urban and rural populations of these two finch species. Once again, they uncovered no fixed differences in gene copy numbers between the urban and rural populations for either species.

“There’s been some evidence that certain genetic markers underlie variation in beak size and shape, but overall Geospiza finches are very difficult to distinguish genetically,” Ms. McNew said. “Could there be another source of phenotypic variation?”

When the team looked at epigenetics, they found a significant number of differences between urban and rural finches of both species.

“In the finches that we studied, epigenetic alterations between the populations were dramatic, but minimal genetic changes where observed,” said the study’s senior author, biologist Michael Skinner, a professor at Washington State University. Professor Skinner’s lab conducted the genetic and epigenetic analyses for this study.

The team also found these epigenetic differences were species-specific: few were shared between medium and small ground finches, in spite of their close family ties. This suggests that medium and small ground finches are each responding rapidly and in their own unique ways to environmental changes at the urban site.

Boats moored in Puerto Ayora (Academy Bay), the largest town in the Galápagos Islands. Puerto Ayora was the urban site in this study.
(Credit: Sabrina M. McNew | doi:
10.1186/s12862–017–1025–9)

“We were very excited to see epigenetic variation between both species of finches and for both cell types we studied (sperm and blood),” Ms. McNew said. (Epigenetic changes in sperm are probably heritable, whereas those in blood are probably not.)

Many of these observed epigenetic changes were associated with genes involved in metabolism and in intercellular communications. Other epigenetic mutations were associated with genes related to beak size and shape. These changes make intuitive sense in view of the fact that the diet of urban finches is diverging away from that consumed by rural populations (ref).

“These species of finch have distinct diets which could explain the differences in methylation patterns as diet is known to influence epigenetics,” Professor Skinner said.

Did the researchers know what to expect from this study?

“Our group published a paper a couple years ago investigating epigenetic variation among species of Darwin’s finches [ref]. In that case we did find that methylation variation existed among species and increased the more distantly related they were,” Ms. McNew said. “But for populations, especially very close ones, we really didn’t know what to expect.”

Although the team discovered many epigenetic differences between urban and rural representatives for both species, they still don’t know for sure if these alterations somehow influence the observed differences between the urban and rural populations of medium ground finches.

“We’re trying to be cautious in our interpretation of what these methylation changes mean,” Ms. McNew said in email.

Adult male medium ground finch (Geospiza fortis), Santa Cruz, Galapagos. (Credit: putneymark / CC BY-SA 2.0)

“In this study we found morphological changes in one species (G. fortis) but not the other (G. fuliginosa) and we found methylation differences in both species,” Ms. McNew pointed out. “We did some preliminary mapping of differentially methylated regions to see if they were associated with any particular genes, but they were largely scattered all through the genome. So while some [differentially methylated regions] were associated with genes associated with beak growth, more work is needed to really nail down the function of these changes.”

Recent research has shown that a wide variety of stressful environmental events can create epigenetic changes.

“[W]ork by Mike Skinner and others has shown that environmental stressors (pollutants, diet, etc.) can change methylation patterns,” Ms. McNew explained in email. “This means that animals could potentially respond to changes in their environment through these DNA methylation changes and that this response could be more rapid than selection on standing genetic variation.”

“This is a novel mechanism which is not seriously considered in evolutionary biology at this time,” Professor Skinner added.

The field of epigenetics is just getting started, especially research into epigenetic variation in wild populations.

“We think it’s very interesting though that there is epigenetic variation on this small scale (i.e. between two geographically close populations), especially since we could not distinguish the populations genetically,” Ms. McNew said. She noted that this research is “a first step in understanding if epigenetic changes are involved in adaptation to changing environments.”

Unfortunately, Ms. McNew doesn’t have any immediate plans to follow up. But she did share some of her research ideas if the opportunity arises in the future to explore these findings further.

“[I]deally I’d love to do the same study at another couple of sites so we can better understand if the methylation variation is accumulating randomly or linked to urbanization, and [I want to] study parents and offspring so we can learn more about the heritability of these patterns.”

Source:

Sabrina M. McNew, Daniel Beck, Ingrid Sadler-Riggleman, Sarah A. Knutie, Jennifer A. H. Koop, Dale H. Clayton, and Michael K. Skinner (2017). Epigenetic variation between urban and rural populations of Darwin’s finches, BMC Evolutionary Biology, published online on 23 August 2017 ahead of print | doi:10.1186/s12862–017–1025–9

Also mentioned:

Oliver Bossdorf, Christina L. Richards, and Massimo Pigliucci (2008). Epigenetics for ecologists, Ecology Letters 11:106–115 | doi:10.1111/j.1461–0248.2007.01130.x

Michael K. Skinner, Carlos Gurerrero-Bosagna, M. Muksitul Haque, Eric E. Nilsson, Jennifer A.H. Koop, Sarah A. Knutie, and Dale H. Clayton (2014). Epigenetics and the Evolution of Darwin’s Finches, Genome Biology & Evolution 6(8):1972–89 | doi:10.1093/gbe/evu158

Sangeet Lamichhaney, Jonas Berglund, Markus Sällman Almén, Khurram Maqbool, Manfred Grabherr, Alvaro Martinez-Barrio, Marta Promerová, Carl-Johan Rubin, Chao Wang, Neda Zamani, B. Rosemary Grant, Peter R. Grant, Matthew T. Webster, and Leif Andersson (2015). Evolution of Darwin’s finches and their beaks revealed by genome sequencing, Nature 518:371–375 | doi:10.1038/nature14181

Luis Fernando De León, Joost A.M. Raeymaekers, Eldredge Bermingham, Jeffrey Podos, Anthony Herrel, and Andrew P. Hendry (2011). Exploring possible human influences on the evolution of Darwin’s finches, Evolution 65(8):2258–2272 | doi:10.1111/j.1558–5646.2011.01297.x


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Originally published at Forbes on 6 September 2017.

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