Evolution after Gene Duplication: a review

I’ve just finished reading Evolution after Gene Duplication, which was edited by Katharina Dittmar and David Liberles and released in 2010.  Before I bought the book I struggled in vain to find a review, so thought I would attempt to provide one here.  However, before opining on the book itself, it’s worth a brief look at the value of writing and reading such a book.

In 1970, Susumu Ohno famously dubbed gene duplication “the major force of evolution”.  By his own admission, this statement was made “on the basis of the scant evidence available”; but the technological advances of the subsequent 43 years have provided the means to test some of his revolutionary hypotheses, and extend our knowledge of evolution by gene duplication.  In their book, Dittmar and Liberles catalogue work from a wide range of fields, and at each stage highlight the improvements these studies have made to our understanding of the evolution of gene duplicates.

Evolution after Gene Duplication (Dittmar & Liberles, 2010) is a valuable exploration of the evolution of gene duplicates (Image reproduced with permission from Wiley)

Evolution after Gene Duplication (Dittmar & Liberles, 2010) is a valuable exploration of the evolution of gene duplicates
(Image reproduced with permission from Wiley-Blackwell)

The book starts with chapters that describe in a broad sense the evolution and divergence of gene duplicates, and the factors governing their retention.  It then moves on to the specifics of the mechanistic basis of duplication, before a series of chapters explore how duplication can be studied using mathematical models, phylogenetics and systems biology.  The final three chapters each consider a different case study: birds, plants, and vertebrates.

This may sound like a lot of topics to cover in one book, but far from skimming over their surface, each is treated in enough depth to warrant inclusion.  Indeed, I found one of the best aspects of the book to be that duplication is considered in its full context.  This served to broaden my outlook on gene duplication, and also provided an accessible introduction to the methods used in these studies.

Another valuable addition are the chapters which explore aspects of gene duplication that are often little-considered or taken for granted, such as redundancy (is it ever selectively advantageous?) and the cost of duplication (what is the size and nature of this cost?).  Both of these sections (by Ran Kafri & Tzachi Pilpel and Andreas Wagner, respectively) do an excellent job in laying out the evidence for the competing hypotheses, as well as extending the ideas with their own thoughts.

An outstanding chapter was “Myths and Realities of Gene Duplication”, by Austin Hughes and Robert Friedman.  Here the authors pull no punches:

“The proliferation of numerous ill-founded statistical methods has given rise to a kind of “computer-assisted storytelling” that purports to test hypotheses but in fact does not adequately consider alternatives.”

They challenge some ideas that were first proposed by Ohno forty years ago, and have become almost canonical since, such as “The Polyploidization Obsession” (their term).   Their dissection of the logical basis and evidence for these ideas makes for refreshing and stimulating reading.

If I had one small gripe, it would be each chapter’s retreading of basic concepts, such as the established evolutionary paths for duplicates (retention, subfunctionalization, neofunctionalization & pseudogenization); however, this is unavoidable in any book that assimilates contributions from so many authors in so many fields.  The repeated treatment of these concepts does at least serve as a barometer for each author’s opinion on such integral ideas.

I would highly recommend Evolution after Gene Duplication.  Its breadth of topic and depth of detailed thought make it a valuable book.



Dittmar, K. & Liberles, D. (2010) Evolution after Gene Duplication.  Wiley-Blackwell.

Ohno, S. (1970) Evolution by Gene Duplication.  Springer-Verlag.


Sea food was good for the mind

by Andrew Farrer

In the 1960s the importance of coastal sites for man living in the Middle Stone Age (250 – 35 thousand years ago) was realised. It seems, from the volume of the remains in human archaeological sites, that shellfish and other marine resources made these locales so appealing. It has been suggested that, more than being just a new food source, shellfish played a role in the evolution of the modern human.

Sea food contains much higher levels of the Omega-3 fatty acids than terrestrial food sources. Omega-3 is famous for being an excellent resource for developing brains; providing some of the building blocks required for maximising brain potential. As a result, living on the coast placed our ancestors in an environment ideal to evolve the complex, organic computer we are now so proud of.

Initially the quantity of Omega-3 consumed would have fulfilled the requirements of our ancestors’ smaller brains but over the generations, as the brain became more expensive, the need for shellfish would have increased. This presents a simple hypothesis: exploitation of marine resources should increase over time. The problem is that Middle Stone Age sites are not described in enough detail to really explore the connection. Worse still, the definition of key criteria varies between sites, making inter-site interpretation virtually impossible.

Hoedjiespunt 1(33° 01’ 42” S 17° 57’ 34” E) is on a peninsula in Saldanha Bay, South Africa. Approximately 68 miles North-West of Cape Town. Images from Google Earth

Figure 1: Hoedjiespunt 1(33° 01’ 42” S 17° 57’ 34” E) is on a peninsula in Saldanha Bay, South Africa. Approximately 68 miles North-West of Cape Town. (Images: Google Earth)

Researchers from the universities of Tuebingen and Cape Town reopened excavations at Hoedjiespunt 1 (see Figure 1 for information) in an effort to set the standard for study and reporting of archaeological data. Will et al. represents the first paper published as a result of this work and focuses on the interpretation of lithics (stone tools) and behaviour. Removing the soil in no more than 3 cm deep layers at a time the researchers found over 3,000 lithic artefacts distributed between three Archaeological Horizons (Archaeological Horizons are layers within the soil, much like strata in rock but formed by human activity). Three unique layers containing archaeologically relevant remains demonstrate that the site was habituated at least three distinct times (See Figure 2). The lithics, dating of shells and consideration of sea levels suggests Hoedjiespunt 1 was utilised 130 – 119 thousand years ago.

The lithics were of four main raw materials: quartz, quartz porphyry, calcrete and silcrete. Only silcrete is considered a good quality stone for knapping (tool preparation) and it is the only material not to be found on site (closest deposits are 6 – 18 miles away). Whilst evidence of all stages of production is found for the other materials, silcrete tools were made off-site. Interestingly the knappers have used different techniques for the differing materials, presumably to get the best results from each stone.

Will et al. suggest that the presence of silcrete shows our ancestors carried tools at all times. They would then have instruments directly available in unexpected situations encountered whilst travelling. Hoedjiespunt 1 seems to have required tool use in quantities that would be impractical to have carried from elsewhere. Poorer quality materials still made adequate tools (quartz forms sharp edges and can be retouched as it goes blunt); so, to me, this seems an economic decision, it was simply more cost effective to use poorer on-site materials than transport good quality ones.

Ocher (a natural pigment) was also found in a modified form. Often used for ritualistic or symbolic drawing it’s commonly seen as a sign of behavioural modernity. It can, however, also be used for hide tanning, insect repellent and as an adhesive. Ocher found at Hoedjiespunt 1 was mainly in the form of pencils though no evidence of design was found.

Figure 2: The three Archaeological Horizons (AH I-III) are clear in the excavation. Topped by a modern humus layer and with shelly sand (SHES) below. (Image: Will et al. 2013)

Figure 2: The three Archaeological Horizons (AH I-III) are clear in the excavation. Topped by a modern humus layer and with shelly sand (SHES) below. (Image: Will et al. 2013)

Whilst comparison between Hoedjiespunt 1 and other sites would reveal the most about changing behaviour at different times and places, this is difficult as the details of other sites are frequently not known in as much depth as Hoedjiespunt 1. However, a lot can be drawn from on-site finds. Data shows that the site was used regularly for short periods (perhaps at specific times of year to coincide with marine resource harvesting) by mobile hunter-gathers. Absolute and relative dating strongly suggests that these were H. sapiens; our direct ancestors. These people demonstrated the ability to plan and appreciate quality; as seen by the non-local preparation and transport of silcrete tools. Connecting lithics to marine resource harvesting is difficult but we can note several factors that support such a conclusion: the shellfish deposits are not natural, shellfish are burned, the three horizons are consistent (the site was used for the same purpose repeatedly) and the locale is best explained by marine resource exploitation as it is neither sheltered from the elements nor a suitable base for terrestrial hunting. In conclusion, our ancestors appear to have had a sustained and stable system that integrated marine resources as a main food source into their diets at Hoedjiespunt 1 and probably elsewhere.

The importance of this paper is not that it presents a ground breaking result (it does not) but that it represents a very important part of science that is often glossed over in our media fuelled world; collection of knowledge. All the sensational headlines seen in newspapers and blogs are born from lots of hard work and the building of a huge base of knowledge. Then a hypothesis and (possibly) a theory can be developed. This paper aims to continue the trend for much more in depth archaeological site review. Will et al. have not proved or disproved the Omega-3 hypothesis but they have certainly provided necessary steps to do so.



Will, M. et al., 2013. Coastal adaptations and the Middle Stone Age lithic assemblages from Hoedjiespunt 1 in the Western Cape, South Africa. Journal of Human Evolution, (64), pp.518–537. Available at: http://www.sciencedirect.com/science/article/pii/S0047248413000924 [Accessed May 31, 2013].

The landscape of evolution

Picture an old record shop.  How do you tell a classic from a dud?  With no way of telling the value of each record, you could just as easily end up with B*Witched as with the Beatles.

Now imagine all of the records in that shop laid out in front of you in the form of a landscape.  Each record forms part of the floor, with different releases of the same album clustered tightly around each other, different albums from the same artist a little further away, artists of the same genre further away still… etc.  Starting from A Hard Day’s Night, you move through Rubber Soul, Help! and Revolver, before finally ending up at Magical Mystery Tour.  But the landscape formed by these records is not flat; some records are higher than others, making an undulating series of peaks, troughs and plains. And the higher you go, the higher the value of whatever record you are standing on.  Looking back behind you, you see a signed copy of Sgt. Pepper’s Lonely Hearts Club Band at the peak of the Beatles’ hill.

Now imagine we could do the same for genetic sequences.  Starting with a simple case, we will consider the four variants (A, C, G and T) at one position in a sequence.  Given that the rest of the sequence is identical, and the sequences are therefore very similar, this is equivalent to considering just one artist with four different albums.  On the x axis we plot the variant, and on the y we show fitness (how well the variant performs):

Much like an artist's albums, some genetic variants are better than others

Much like an artist’s albums, some genetic variants are better than others

Imagine that we are placed on the left end of the line – this is the part of space occupied by A.  One step to the right and we tread on C, another step and we’re on G, and a final step brings us to T on the right.  And as we move from one base to another, we go up and down as the fitness of each sequence increases and decreases.  In this example, G has the highest fitness (it’s the Sgt. Pepper of bases), C and T have intermediate fitness, and A has the lowest fitness.

However, this example only encompasses the fitness of the variants at one base.  If we consider two bases, the landscape changes from a simple 2D line to a more complex 3D surface.  And if we consider more bases (or all the records in the shop), we step into a world with dozens or hundreds of dimensions: the landscape pictured (taken from Hayashi et al, 2006) summarises this high dimensionality into three large peaks, with smaller peaks and troughs at the top of each one.

Fitness landscapes show the paths along which a sequence can evolve (Credit: Hayashi et al, 2006)

Fitness landscapes show the potential evolutionary paths taken by a sequence
(Credit: Hayashi et al, 2006)

Starting at one position we can journey across the landscape, treading the paths along which the sequence can evolve, with every step representing one change in the sequence.  On this journey, we have to remember only one rule: we can never go downhill.  If we go up, it means the sequence is increasing in fitness, and so will survive; however, if we go down it means the sequence is becoming less fit, and will be selected against and removed from the population.

However, this rule soon brings up a problem.  Imagine we walk up a small hill: from here, every direction leads downhill.  If we can never go down, where do we go?  Are we stuck forever on this small hill, at a relatively low fitness, unable to continue evolving?

Luckily, there is a solution: neutral variants.  These variants have different sequences but are as fit as each other, and therefore form ridges in the fitness landscape.  It is along these ridges that we can escape from low hills, into regions of the landscape that have higher peaks.  As the sequence gets longer, the chances of encountering a ridge increase, because each base adds another dimension in which fitness can vary.  As Manfred Eigen puts it in his book Steps Towards Life:

‘raising the number of dimensions increases the number of possible routes’

Using the fitness landscape, we can visualise paths from one sequence to another, and judge whether these paths will be evolutionarily viable.  By distilling the complexity of genotype and phenotype into one space, the fitness landscape gives an intuitive illustration of the process of molecular evolution.




Hayashi Y., Aita T., Toyota H., Husimi Y., Urabe I., et al (2006) Experimental Rugged Fitness Landscape in Protein Sequence Space. PLoS ONE 1(1): e96

Eigen, M. (1996) Steps Towards Life.  Oxford University Press

Eggs can’t run

by Andrew Farrer

Avoiding predation is important. From an evolutionary view being eaten is a poor strategy and I think we can all appreciate the more proximal aversion to being lunch for something else. The world is full of a myriad of strategies to avoid becoming a meal; herding (or flocking), poisonous or foul tasting chemicals, mimicry, camouflage, etc. However, the method that first comes to mind is simple: run. Nothing can beat distance for its defensive capabilities.

The tegu (of the genus Tupinambis) is another lizard who responds to mechanical stimulation, or in this case, tickling.  Credit: Varnyard/YouTube

Eggs, though, are not good at running. If there is no parental care then all they may have at their disposal are camouflage and safety in numbers. For a predator, a clutch of eggs is a nutritious and easy meal. As such, the best strategy for an embryo is to hatch at the earliest possible developmental stage, leave the confines of the egg and become mobile. On the flipside, however, the world can be a harsh place and remaining in the egg as long as possible can protect the embryo. Also, once hatching competence has been reached development does not flat-line. More time developing in the egg could make a hatchling more robust. The solution would seem to be for the embryo to monitor the external environment and adjust its hatching date. Conveniently for them (and this post) that is exactly what they do; it’s called Environmentally Cued Hatching (ECH).

In 2011 J.S. Doody stated that ECH was the “..variation in time, age, or developmental stage at hatching, facilitated by an extrinsic cue..”. It can be divided into three areas: Early Hatching, Delayed Hatching, and Synchronous Hatching (hatching at the same time as other eggs in the clutch). Research is currently scattered and unconnected but in recent years researchers have been drawing together the few papers and the anecdotes that support the ECH hypothesis. The ability to react to environmental cues has been noted in a wide range of organisms. Parasitic flatworm eggs can survive in harsh environments that the larvae cannot, so hatching is delayed until conditions become more favourable. Some molluscs can delay due to food scarcity, and Spitting-spider mothers can trigger early hatching of the eggs clinging to her body so she can better defend herself. There are also examples from nematodes, crustaceans and insects. In the vertebrates, fish may need an extrinsic trigger as well as an intrinsic one to hatch at all and pig-nosed turtle eggs can detect vibrations from hatching siblings, leading to synchronous hatching.

A delicate skink hatches after the egg was touched by a researcher. Vibrations can induce hatching up to 7 days early in this species Taken from (J S Doody, 2011). Credit: N. Pezaro.

A delicate skink hatches after the egg was touched by a researcher.
Vibrations can induce hatching up to 7 days early in this species
Taken from J S Doody (2011). Credit: N. Pezaro.

A recent study by J.S. Doody and P. Paull studied how mechanical stimulation affected the eggs of the Delicate skink (Lampropholis delicate – a lizard native to Eastern Australia). Laboratory experiments showed that mechanical stimulation (in this case, being placed on an orbital shaker for one minute a day) of wild and lab lain eggs resulted in these eggs hatching 3.4 days earlier than a non-stimulated control group. The skink certainly reacted to mechanical stimulations but what about direct threat? Moving to the field the experiments and the results got a bit more interesting.

Delicate skink lay their eggs in narrow, rocky crevices. Doody and Paull located a nest with eggs at the minimum hatching age. To simulate a predator they poked the eggs with the blunt end of a bamboo cooking skewer. Within 10 seconds of being poked 16 of the 19 eggs hatched, the young lizard immediately launching itself from the crevice, falling 1.4 metres to the safety of the leaf litter below (a long way when you’re less than 40 mm long). The remaining 3 eggs also hatched but, being less dare-devilish than their siblings, opted for hiding deeper in the crevice. Simulating an egg being knocked from the nest Doody and Paull pushed 42 eggs out of nest crevices; 36 hatched as result with 12 of those emerging from the egg as it landed. The lizards’ piece de resistance, however, was hatching on open ground; they erupted from the egg and immediately sprinted away. These youngsters could sprint, on average, 41.6 cm (S.D. ±22.76 cm, Range; 5 – 89 cm, n=30) to cover. Not bad for a creature that has never seen the world before, or used its legs.

It’s the explosiveness that indicates an anti-predator response. However, wild skink that hatch early are significantly smaller than those who hatch spontaneously, and their eggs display yolk traces that spontaneous hatchers do not. The loss of energy (and thus body size at hatching) is a smaller cost than death and so worth paying. However the premature hatch could put youngsters at a disadvantage alongside spontaneous hatchers; presumably more so the earlier the hatch was triggered. Still, if you’re going to flee from danger, exploding from your egg beforehand is the way to do it.



Doody, J S. (2011). Environmentally cued hatching in reptiles. Integrative and Comparative Biology, 51(1), 49–61. doi:10.1093/icb/icr043

Doody, J. Sean, & Paull, P. (2013). Hitting the Ground Running: Environmentally Cued Hatching in a Lizard. Copeia, 2013(1), 160–165. doi:10.1643/CE-12-111

Warkentin, K. M. (2011). Environmentally cued hatching across taxa: embryos respond to risk and opportunity. Integrative and Comparative Biology, 51(1), 14–25. doi:10.1093/icb/icr017

Starch gave canine evolution something to chew on

A dog’s dinner can be scraps from the table, a juicy bone or an incredibly unlucky piece of homework.  This omnivory has been present since their domestication around 15,000 years ago, just before humans developed agriculture.  Indeed, it appears that evolving the ability to break down starch (a large, complex molecule) into glucose (much simpler and easier to digest) was a key step in the speciation of dogs from wolves.  So what is the genetic basis of this varied appetite?  And was the evolution of broader gastronomic horizons the cause of domestication, or a consequence of it?

Dogs diverged from wolves roughly 15,000 years ago
(Creative Commons – Author: Dennis Matheson)

These are the questions that Axelsson and colleagues set out to answer.  They sequenced the genomes of 60 dogs from 14 different breeds, as well as 12 wolves to use as a measure of the ancestral state of dogs before their domestication.  Once the sequencing was complete, they pooled all of the dog genomes to make one genome representative of canine diversity (this was done to counter the effects that selective breeding may have had on particular dog breeds).  They then looked for regions in the dog genome that had low diversity (indicative of the action of selection at these sites), and high divergence from wolves (suggestive of a role in dog speciation).

They found 36 regions that had both low diversity and high divergence.  In these 36 regions were a total of 122 genes, 10 of which were involved in digestion.  This gave the authors 10 candidate genes, some or all of which could have driven the adaptation to starch digestion in early dogs.  They found evidence for selection on three: AMY2B, MGAM and SGLT1.

AMY2B is an amylase that breaks down starch into maltose.  Intriguingly, the number of sequencing reads mapping to this gene in dogs was far higher than in wolves, suggestive of a duplication of this gene in dogs (two copies would be expected to double the number of reads, four copies would quadruple it, and so on).  Investigating this further using qPCR (which quantifies the level of expression of a gene in RNA, or the number of copies of a gene in genomic DNA), the authors found between 2 and 15 copies of AMY2B in different dog breeds.  And when they measured AMY2B expression and the ratio of starch to maltose in the blood (a proxy for AMY2B activity), both were 5-20 times higher in dogs than wolves.  AMY2B duplicates have clearly been retained by selection, and this increase in AMY2B copy number is correlated with increased starch digestion.  However, what is not clear is how many of these different copies are contributing to starch digestion in each breed.  There could be slightly elevated expression of each copy, or one or two copies could have massively increased expression; both situations would lead to the increase in overall amylase levels seen by the authors.

Starch was an abundant food source, making the ability to digest it selectively advantageous in early dogs (Creative Commons – Author: Antony Stanley)

Intriguingly, duplication has also been documented in human amylase.  At some point after humans diverged from mice, amylase (which is usually expressed only in the pancreas) duplicated to produce two copies.  One of these copies remained pancreas-specific, while the other specialized to be expressed only in the saliva (Meisler & Ting, 1993).  It would be fascinating to know whether a similar situation of duplication and specialization has occurred in these dog amylases.

The next gene showing evidence of selection was maltase-glucoamylase (MGAM), which breaks down maltose into glucose.  The authors sequenced MGAM in an additional 71 dogs from 38 breeds, and found that 68 of these dogs carried the same allele (gene form).  They also found that expression of MGAM was 12 times higher in dogs than wolves.  That this allele has been preserved in such a large proportion of dog breeds is powerful evidence for its importance in starch digestion.

The final gene implicated in the evolution of starch digestion was SGLT1, which helps transport glucose across the gut wall into the blood.  Again, the authors looked at the sequence of SGLT1 in 71 dogs, and found a high level of divergence from wolves.  However, the evidence for selection on this gene is weaker than the other two for a couple of reasons: firstly, their sequencing covered only one end of the gene, not its entire length; and secondly, they found no difference in expression of SGLT1 in dogs and wolves.

There is one caveat to the expression studies carried out for all three genes, about which the authors are admirably candid:

‘we cannot rule out that diet-induced plasticity contributed to this difference”

In other words, it may have been that they happened to compare some particularly well-fed dogs with some very hungry wolves, and that this caused much of the difference in their levels of gene expression and their maltose:glucose ratio.  But in my opinion, given the strong evidence for selection at AMY2B and MGAM, and the difficulty in standardizing diets across all individuals measured (would you want to tell a wolf what to eat?), this weakness is not fatal to their argument.

Changes in AMY2B and MGAM were selected for during dog domestication (Creative Commons - Author: Steve Guttman)

Changes in AMY2B and MGAM were selected for during dog domestication (Creative Commons – Author: Steve Guttman)

So it appears that selection has acted on multiple stages in the starch digestion pathway.  Fascinatingly, this selection has taken different forms: at the starch-maltose stage (AMY2B) gene duplicates have been selectively retained; whereas at the maltose-glucose stage (MGAM) there have been changes in the sequence and expression of a single gene.

However, one mystery remains: did this selection on starch digestion happen before dogs were domesticated (wolves scavenging at waste dumps), or after their initial domestication (guard/hunting dogs fed starchy waste)?  Perhaps a better question is: does it matter which came first?  A far more interesting issue is how dogs adapted to this new food source, and Axelsson et al have provided a convincing exploration of the genetic basis of this adaptation.


Axelsson, E. et al (2013) The genomic signature of dog domestication reveals adaptation to a starch-rich diet.  Nature advance online publication

Meisler, M.H. and Ting, C-N (1993) The remarkable evolutionary history of the human amylase genes.  Critical Reviews in Oral Biology & Medicine 4: 503-509

The power of one base: The under-explored Rock pigeon demonstrates the power of micro-evolution

by Andrew Farrer

I was surprised to learn that the domestication of the Rock Pigeon (Columbia livia) has resulted in over 350 breeds. In a stunning example of macro-evolution within a species this domestication has led to some striking phenotype differences. Researchers have now started to explore the genomic diversity, genetic structure and phylogenetic relationships present in these birds. Studying the (relatively) simplistic genetic differences between breeds gives researchers a base to explore the more complex and less distinct differences between other avian species.

A Rock Pigeon takes flight (Creative Commons – Author: A.D. Wilson)

A Rock Pigeon takes flight (Creative Commons – Author: A.D. Wilson)

In a study by Shapiro et al. 38 domestic birds from 36 breeds and 2 feral individuals were sequenced, the results supporting the assumption that these birds would make good models. The Rock Pigeon isn’t on any endangered lists; its effective population size is roughly 521,000 which, apart from a recent bottle neck, has been stable for 1.5 million generations. More importantly, though, with a low expected Linkage Disequilibrium between gene pairs, association mapping techniques are possible (Association mapping exploits the fact that new alleles for new traits will still be close to ancestral genetic sequences. As such you can use SNP chips to explore specific regions of the genome in many individuals and link these differences with differences in phenotype).

Breed relationships were drawn up based on this initial examination and simulations showed that all the breeds had originated from a single ancestral population (rooted using sister species; Columbia rupestris). From this base, further analyses were conducted to associate specific genes and alleles with some of the phenotypic differences. (In case you were wondering, the two feral individuals included in this study appear to be descended from homing pigeons. Whether their ancestors escaped or got lost isn’t clear).

A Red Jacobin Pigeon. The white head is just visible (Creative Commons – Author: J. Gifford)

A Red Jacobin Pigeon. The white head is just visible (Creative Commons – Author: J. Gifford)

Change in plumage colouration is the primary result of bird domestication. This is followed by plumage and structural (skeletal and soft tissue) change and finally changes in behaviour. The head crest is an example of plumage alteration. This feature results from a reversed angle of feather projection on the neck. Growing upwards the feathers form a ring around the head, giving the bird a crown, or crest, of feathers. The degree varies between breeds. Some have no crest at all (the apparent ancestral state) whilst some have quite extreme crests (the Jacobin (pictured) hopefully doesn’t require a wide field of vision!). Importantly the presence of the crest follows a Mendelian recessive pattern, suggesting a single gene is responsible.

Re-sequencing confirmed that a single locus controlled the presence/absence of the crest. It was the pigeon homolog of the Ephrin receptor B2 gene, part of the tissue patterning and morphogenesis pathway in chickens and presumed to be similar in pigeons.  Comparison between 8 crested birds showed that the same mutation caused the presence of the crest in differing breeds. The non-synonymous substitution of a Thymine (T) for a Cytosine (C) generates the recessive allele, the substitution of one base in the entire genome, causes the presence of the crest. As noted the trait is recessive so an individual requires both copies of the gene to be the T allele to have a crest. The presence of the C allele in one or both genes results in no crest.

The same mutation in all crest bearing breeds suggests a single occurrence in a common ancestor or repeated selection from a standing occurrence in the original, wild Rock Pigeon population. With crested breeds not necessarily being more closely related to each other than to non-crested breeds the standing occurrence hypothesis seems viable. Although, it seems to me that in such an artificially selected group it would be easy, whilst the allele was not fixed in the population to breed it in or out of sister lineages or to breed in other alleles in different genes that cause two closer related breeds to appear differentiated. For instance if you took a stock of birds and split them into three populations, you could breed the crest into two whilst not the third. However, if you also select strongly for other traits in the second of the crested populations you would cause the two crested populations to differ at more loci than the first crested population and the non-crested population.

English trumpeter(Creative Commons - Author: J.Gifford)

English trumpeter (Creative Commons – Author: J.Gifford)

Contrast the Red Jacobin and the English Trumpeter (pictured); Ephrin receptor B2 gene causes the presence of both birds’ crest but the differences are caused by the effects of other genes along the pathway. For one single base change, though, to be the trigger for such an apparent trait really does show how tiny genetic changes can lead to phenotypic differences; differences which could easily impact upon fitness. Such an example shows how micro-evolution could easily generate macro-evolutionary changes; changes that could lead to speciation events. It may even be possible for a single base to make all the difference – it does here.



Shapiro, M.D. et al (2013) Genomic diversity and evolution of the head crest in the rock pigeon. Science 339: 1063-1067

Evolutionary ingenuity often seems a bit weird

by Andrew Farrer

Simultaneous hermaphrodites are fascinating organisms. Unlike the more famous sequential hermaphrodites, such as the clown fish and sea horse (who change sex during their life cycle), simultaneous hermaphrodites are male and female simultaneously. During a single copulation event both partners donate and receive sperm.

C reticulata

Almost all nudibranchs (commonly referred to as sea slugs, despite this term also applying to taxonomic groups not related to nudibranchs) are simultaneous hermaphrodites.  With such an unusual sexual arrangement, our first question would be; why? There are several hypotheses, the most favoured of which is that for organisms living in low population densities and with low mobility it is beneficial to be able to play both roles. Turning that question on its head, we could ask: why not a simultaneous hermaphrodite?

Sex (the “mixing” of DNA between generations) does increase fitness (Lee et al. 2010) but exactly why is contentious. Reversing Muller’s Ratchet (thus preventing mutational meltdown) is commonly cited. However, despite the benefits, there are costs. The “two-fold cost” is incurred because a sexual organism, unlike an asexual organism, must locate a partner (a conspecific) with which to exchange DNA (Otto & Lenormand 2002).

Unfortunately, further problems are caused by mitochondria (and other non-nuclear DNA carrying organelles). Mitochondria with differing genomes do not like being in a cell together and the ensuing war can be catastrophic for the host cell. To avoid this deadly encounter, cells evolved to allow the mitochondria from only one parent into the next generation. The cell who’s mitochondria are passed on are female, the other cell, who’s mitochondria don’t pass on, are male (Lane 2005). Unfortunately, in avoiding the mitochondrial war, organisms have doubled the two-fold cost. Whilst the two-fold cost concentrated on the issue of needing a conspecific partner at all; now only half the conspecifics available are suitable. Two-fold became four-fold.

This leads us neatly back to simultaneous hermaphrodites. Why do it? Well, now all the conspecifics around are potential partners again and they still avoid the mitochondrial death trap. So nudibranchs, as weird as they seem, have solved an evolutionary conundrum quite neatly.

However, a Japanese team (Sekizawa et al. 2013) have observed a behaviour which places one nudibranch, Chromodoris reticulata, back in the realms of weird. This nudibranch is a simultaneous hermaphrodite which, after copulation, disposes of its penis and replaces it with a new one.

Around 20 minutes (20.57 ±7.04 min.) after copulation ends the penis is severed from the body. Within 24 hours (approximately) a new penis is formed from a spiral structure of undifferentiated tissue in the body. Indeed, the individual generally absconds from sex for this period, although on occasion it will play the female role.

C reticulata

The discarded penis is barbed and is sometimes found with sperm clinging to it. The authors hypothesised that this is either a sperm replacement technique, removing sperm from a previous mating, or excess sperm from the mating. They point out that a DNA test is needed to resolve this. I would suspect it is sperm replacement; it is wasteful of an individual to create such excess sperm that it is so clear post-copulation. Also, unless the barbs evolved to remove the individual’s own excess sperm (which seems unlikely), this hypothesis doesn’t explain their presence. The difficulty in removing the penis from the vagina of the partner is also noted as a reason for the discarding. Perhaps damage to the non-muscular penis results in a decreased effectiveness in later copulations. It also seems a risk to insert a penis covered in another individual’s sperm into a partner: the barbs are less effective against any sperm to be removed and there is the possibility of insemination by the trapped sperm.

There is little doubt that the severing of the penis is beneficial to Chromodoris reticulata; that it outweighs the costs of producing a replacement and the loss of mating potential during that period. That’s the beauty of evolution; in context it always makes sense. That doesn’t stop the idea sounding quite “unusual”. I think it keeps the nudibranchs in the bizarre category for now.

Lane, N., 2005. Power, Sex, Suicide. Mitochondria and the Meaning of Life, Oxford University Press.

Lee, S.C. et al., 2010. The evolution of sex: a perspective from the fungal kingdom. Microbiology and molecular biology reviews : MMBR, 74(2), pp.298–340. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2884414&tool=pmcentrez&rendertype=abstract [Accessed August 4, 2011].

Otto, S.P. & Lenormand, T., 2002. Resolving the paradox of sex and recombination. Nature reviews. Genetics, 3(4), pp.252–61. Available at: http://www.ncbi.nlm.nih.gov/pubmed/11967550 [Accessed June 13, 2011].

Sekizawa, A. et al., 2013. Disposable penis and its replenishment in a simultaneous hermaphrodite. Biology Letters, 9(February).