Might Epigenetics Hold The Secret To Super-Fast Adaptation?

How do invasive species overcome the genetic bottleneck created by having a tiny founder population?

by GrrlScientist for Forbes | @GrrlScientist

Adult male house sparrow (Passer domesticus).
(Credit: Simon Griffith.)

Invasive species are everywhere these days. After people move them to a new location (whether intentionally or not), these organisms are able to invade an already occupied habitat, out-compete native species and species communities, and carve out a niche that specifically suits their needs.

It is their ability to flourish against all odds that makes the scientific study of invasive species so important: invasives have a lot to teach us about how to adapt to, and prosper in, an alien environment. For example, how does an invasive species overcome the pervasive problem of a tiny founder population? How does an invasive species adapt to a novel environment when they’ve got very little genetic diversity to draw upon? These challenges are similar to those faced by conservation biologists who struggle to preserve endangered animals and plants whose tiny gene pools nearly always result in inbreeding depression. Not only does inbreeding depression decrease the ability of a species to adapt to a novel environment, it increases the prevalence of genetic disorders throughout the population and diminishes the ability of a species to deal with diseases.

Due to the small numbers that are introduced, invasive species experience a genetic bottleneck that results in low levels of genetic diversity. This reduction in genetic diversity is expected to constrain a species’s ability to adapt to an alien environment — yet, somehow, they overcome it. Invasive species’s ability to adapt and expand their population across novel environments presents us with an “invasive paradox” (ref).

Several recent studies have found that, in plants at least, epigenetic mechanisms that alter gene expression without changing DNA sequences may contribute to observed variations in phenotypes (i.e.; ref). Of these epigenetic mechanisms, DNA methylation is the most widely studied. “DNA methylation” refers to the addition of a methyl group to a cytosine nucleotide base, most often when that cytosine is immediately followed by a guanine within the DNA sequence, which are known as “CpG sites”. These CpG sites are common in regulatory DNA sequences, so variation in methylation can alter gene expression, which potentially alters expression of observable characteristics (phenotypes) without actually changing gene sequences.

Epigenetic mechanisms.
Epigenetic mechanisms are affected by several factors and processes including development in utero and in childhood, environmental chemicals, drugs and pharmaceuticals, ageing, 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.)

Previous studies have revealed that DNA methylation patterns undergo rapid changes in response to local environmental changes during an individual’s lifetime (ref). For this reason, it has been proposed that these so-called “epimutations” may be one of several mechanisms whereby organisms increase their ability to adapt to novel environments or to environmental fluctuations, in the absence of genetic variations. Could this epigenetic flexibility be the “secret superpower” that transforms some species into invasives?

Might epigenetics be invasive species’s secret superpower?

Fly into any city in the world, and there they are. You don’t have to be a birder to notice house sparrows, Passer domesticus. These small birds are clad in subdued tans and greys with rich rufous-brown plumage on their wings and backs, and the males also have a black “bib” whose size signals his age and social rank.

As invasives go, house sparrows certainly appear ubiquitous, cheerfully chirping to each other in small family flocks underfoot throughout cities and major metropolitan areas around the world, and their numbers are still increasing in many places. But why? What makes house sparrows so rapidly adaptable? These are a few of the questions that puzzle scientists, too.

Yes, house sparrows can even be found in Moscow, Russia. In winter.
House sparrows (Passer domesticus) perching on a wall in the snow in Moscow, Russia.
(Credit:
Andrey / Creative Commons Attribution 2.0 Generic license.)

A 2013 study of house sparrows that had been introduced into Kenya around fifty years ago suggested that increased phenotypic variation might result from increased epigenetic diversity, and this might compensate for the introduced sparrows’ lack of genetic diversity (ref).

Prior to the Kenyan introduction, several other house sparrow introductions were intentionally made into Australia by the “Australian Acclimatisation society”. This society operates under the maddeningly erroneous notion that native wildlife and plantlife are somehow deficient or impoverished and thus, require human intervention to be “improved” with introductions of non-native European flora and fauna. The Australian house sparrow introductions consisted of birds living in Europe, where it is native, and in India, where it is invasive.

Previous historical and molecular studies identified that at least three separate Australian introductions occurred in the 1860s: Melbourne (VIC); Adelaide (SA); and Brisbane (QLD), along with two isolated translocations from Melbourne to Sydney (NSW) and Hobart (Tasmania). These multiple, distinct introductions provide researchers with a nifty study system for examining different epigenetic patterns in these Australian populations and for comparison to the Kenyan population to test whether the genetic and epigenetic diversity observed in the introduced African population might be similar across the three introduced populations of Australian house sparrows.

Molecular techniques confirm three separate sparrow introductions into Australia

A research collaboration at Macquarie University replicated and expanded upon the original 2013 study of the Kenyan house sparrow introduction (ref) to see whether the Australian sparrows showed the same molecular patterns. To begin, the research team identified 15 sites throughout eastern Australia that can be linked to the three historically independent introduction events for house sparrows (Figure 1):

Figure 1. Map of the Eastern half of Australia labelled with the 15 study sites and their corresponding epigenetic diversity (epi-h) values. Sites derived from the same introduction event are grouped within an oval; 1, the South Australia introduction; 2, the Victoria/New South Wales introduction; 3, the Queensland introduction. The house sparrows’ estimated range edge is also plotted.
(doi:
10.1098/rsos.172185)

To do this, the research team captured 380 wild house sparrows and collected a tiny blood sample from each. They extracted and amplified the DNA, and successfully genotyped 180 individuals. Their microsatellite data identified three population clusters (Figure 2), which are consistent with the three previously identified independent introductions (the Melbourne cluster [VIC and NSW]; the South Australian (SA) cluster from around Adelaide; and the Queensland (QLD) cluster from around Brisbane.) As proof of methodology, their analysis correctly assigned individuals to each population cluster (95.7%, 95.3% and 76.7%, respectively; Figure 2c):

Figure 2. (a) The scatter plot for the CoA of the 16 sample localities with the three clusters that were identified. (b) The scatter plot from the DAPC which used the three population labels with the individual genotypes (n = 623 individuals). © The membership probabilities for the DAPC in (b). The sample labels 1–16 correspond to the sampling localities: Tolga, Townsville, Charleville, Pittsworth, Armidale (removed from epigenetic analyses due to low sample sizes), Dubbo, Cobar, Wentworth, Burrumbuttock, Melbourne, Geelong, Bridport, Mt Gambier, Broken Hill, Adelaide and Coober Pedy, respectively.
(doi:
10.1098/rsos.172185)

The researchers examined epigenetic and genetic differentiation from the three Australian house sparrow populations and compared these to the Kenyan sparrow population. Did their comparisons between the three Australian and the Kenyan populations uncover any correlations between epigenetic and genetic pairwise site variations for any of these study populations? Surprisingly, no, they did not (Figure 3).

Figure 3. Mantel’s test comparing genetic and epigenetic pairwise estimates of ΦST, across all sample sites; there is no relationship (R2 = 0.124, n = 15, p = 0.159).
(doi:
10.1098/rsos.172185)

The research team did discover that the patterns of epigenetic variation are highly variable across populations within each of these clusters, rather than having a shared similarity — as is seen for genetic variation.

These results suggest that at least some of the observed differentiation in DNA methylation arose independently, or at least partly independently, from genetic differentiation. Although a number of studies (mostly in plants) found significant correlations between epigenetic and genetic differentiation, an increasing number of studies report nocorrelations between epigenetic and genetic differentiation. So what does this mean?

The “epigenetics mystery” deepens

“[T]he house sparrow really provides excellent opportunities to study fundamental questions like this, because there are so many introductions across the world,” said senior author, evolutionary ecologist Simon Griffith, a professor at Macquarie University, in email. “They are fairly well-documented and occurred at approximately the same time. As a result, these introductions provide excellent pseudo-experiments and provide a really fantastic way of addressing questions about micro-evolutionary processes, and adaptation to things like climate change.”

As reviled as house sparrows are in many countries, they are admirably adaptable birds.

“In undertaking the study we conducted a few road trips across the huge expanse of inland Australia,” Professor Griffith said in email. “It’s really remarkable how well sparrows have done since being introduced in 1863. They are really adaptable and can be found across the really broad range of climates in Eastern Australia from the tropics down to the temperate climate of Tasmania.”

Adult male house sparrow (Passer domesticus). (Credit: Adamo / CC BY 2.0 de.)

But the molecular mechanisms that underlie the sparrows’ extraordinary adaptability remain elusive.

“The idea that epigenetic variation might be a good way to overcome deficiency in genetic variation sounds like a great idea and some of the first studies found support for that,” Professor Griffith explained in email.

Even some recent studies in other birds appear to suggest that epigenetics may be a molecular mechanism whereby a given population compensates for its lack of genetic diversity (for example; read this). But even those studies indicate that epigenetic differences are correlative only: epigenetic variations have not been demonstrated to be the source, or direct cause, of these observed phenotypic changes.

“However, it is worth re-examining such studies, and addressing the same question in other systems, as possibly the earlier studies might be a little unreliable,” Professor Griffith speculated in email. “Either that, or we are left to conclude that different things may be happening in different populations (which is, of course, highly plausible as well). Epigenetic variation certainly is worthy of further study.”

Although there is no evidence that epigenetic variations may be compensating for the lack of genetic diversity in Australia’s house sparrows, it is possible that such changes may be more numerous or more easily identified shortly after introduction, when the birds are in the earliest stages of adaptation, when genetic diversity lowest and the pressure to adapt quickly to a novel environment is highest.

“I think a lot more people should be studying the house sparrow,” Professor Griffith said in email. “Of course we weren’t the first to realise the potential of this system. David Lack identified the opportunity in the middle of the 20th Century [read more] and there have been lots of classic studies on evolution of traits such as body size that were inspired by his insight.”

But why publish “negative results” refuting your hypothesis that epigenetic changes might somehow be linked to adaptability in invasive species?

“It was somewhat disappointing to examine an interesting question (as first shown by Liebl et al 2013), and not find any support for it, because it was a good idea,” Professor Griffith said in email.

“However, that’s science and it was important to publish these negative results because of the well-known bias in publication (caused by the failure to publish null results).”

As Thomas Huxley, Darwin’s colleague and staunch defender, once succinctly observed: “The great tragedy of science — the slaying of a beautiful hypothesis by an ugly fact.”

Nevertheless, this study is one of just a very few that examine the patterns of epigenetic variation across a number of populations and thus, it contributes to our growing insight into the potential role of epigenetic variation in ecology and evolution.

“We did find a lot of … epigenetic variation across populations and we have no idea what is driving that, or what the consequences of it are.”

Source:

E. L. Sheldon, A. Schrey, S. C. Andrew, A. Ragsdale and S. C. Griffith (2018). Epigenetic and genetic variation among three separate introductions of the house sparrow (Passer domesticus) into Australia, Royal Society Open Science, 5(4):172185 | doi:10.1098/rsos.172185

Also cited:

Fred W. Allendorf and Laura L. Lundquist (2003). Introduction: Population Biology, Evolution, and Control of Invasive Species, Conservation Biology, 17(1):24–30 | doi:10.1046/j.1523–1739.2003.02365.x

Oliver Bossdor, Davide Arcuri, Christina L. Richards, and Massimo Pigliucci (2010). Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana, Evolutionary Ecology, 24(3):541–553 | doi:10.1007/s10682–010–9372–7

Bernard Angers, Emilie Castonguay, and Rachel Massicotte (2010). Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after, , 19(7):1283–1295 | doi:10.1111/j.1365–294X.2010.04580.x

Andrea L. Liebl, Aaron W. Schrey, Christina L. Richards, and Lynn B. Martin (2013). Patterns of DNA Methylation Throughout a Range Expansion of an Introduced Songbird, Integrative and Comparative Biology, 53(2):351–358 | doi:10.1093/icb/ict007

Samuel C. Andrew and Simon C. Griffith (2016). Inaccuracies in the history of a well-known introduction: a case study of the Australian House Sparrow (Passer domesticus), Avian Research, 7:9 | doi10.1186/s40657–016–0044–3

Samuel C. Andrew, Monica Awasthy, Peri E. Bolton, Lee A. Rollins, Shinichi Nakagawa, and Simon C. Griffith (2016). The genetic structure of the introduced house sparrow populations in Australia and New Zealand is consistent with historical descriptions of multiple introductions to each country, Biological Invasions, | doi:10.1007/s10530–017–1643–6


Originally published at Forbes on 30 April 2018.