Monday, April 27, 2015

Arms races as analogies

What is progress in evolutionary terms? An absolute increase in complexity, perhaps? Many biologists (myself included) would say that natural selection has no foresight; that organisms don’t evolve adaptations in anticipation of what is to come. This is different from denying that evolution can often take predictable directions, such as increasing the size of weapons, or the complexity of communication. As Dawkins and Krebs proposed in a brilliant paper [1], arms races are situations in which one can predict a kind of evolutionary progress through escalating conflict. Measured purely in terms of evolutionary fitness, the fastest antelope isn’t an improvement on its ancestors, because all its contemporaries are also faster, and so are their predators. Just like the Red Queen in Alice in Wonderland, everyone is effectively running as hard as they can to stay in the same place relative to everyone else in the evolutionary race to survive and reproduce. However in absolute terms, arms races can cause progress in the sense that today’s antelope and cheetah are faster than their ancestors.

For historians (including evolutionary biologists), the notion of an arms race is a compelling framework for explaining and predicting the consequences of conflict. In AnimalWeapons: The Evolution of Battle, Doug Emlen makes a very convincing case that evolutionary arms races are often strongly analogous to those in human warfare. Although much of his book addresses the more obvious parallels in weapon evolution – increases in antler or battleship size as conflicts escalate – there is also a fascinating discussion of asymmetric arms races, in which one side is attacking, and the other defending. I particularly enjoyed the parallels between army ants and Assyrians attacking the highly evolved and elaborate fortresses of termites and the city of Lachish respectively.

Just as human history involves arms races of attack and defence, the rest of biological history is rife with asymmetric arms races – most dear to my heart, those between parasites and hosts. Viruses constantly evolve new ways to invade our immune systems, while we both evolve and invent ways to defend ourselves from infection.

Cuckoo:Cheating by Nature, just published by Nick Davies, is all about this kind of arms race, but in this case, both parasites and hosts are birds. As Davies discusses beautifully, brood parasitic birds, which manage to “trick” other birds into bearing the entire burden of childcare, are some of nature’s ultimate cheats. The arms race idea applies because it’s evolutionarily costly to rear someone else’s children at the expense of one’s own, and host birds are under strong selection to detect and deter parasitism, such as recognising and rejecting a foreign egg. This selects for egg forgeries on the side of the parasite, which in turn selects for better discrimination by hosts, and sometimes, to making eggs with more independently varying signatures so that they are harder to forge [2]. The result of this mimicry arms race is eggs with remarkably diverse colour and pattern signatures in two unrelated bird lineages.

Cuckoo is a tale of the finest scientific passion and skilful detection that goes beyond presenting a masterly overview of brood parasite research to painting a personal and highly inspiring account of behavioural ecology at its best.  Nick Davies is one of the giants in this field of biology that tries to explain why animals have evolved to behave the way they do. He is a giant because of the simple elegance of his experiments. Much of science, including evolutionary biology, is tools-driven. Astronomers discover new things with improved telescopes, and biologists are now experiencing a similar revolution with increasingly affordable genomics. Davies has the rare ability to design experiments that require little more than a pair of binoculars, and possibly, a painted balsa wood model, to unearth secrets that would otherwise remain as unanswered questions. I’ll let you read the book to find out how exactly how he does this, because he would make it come alive better than I ever could.

Animal Weapons is just as riveting, but in a very different way. The scope of this book is broader, and Emlen takes more conceptual risks. One of the main ideas Emlen proposes is a novel precondition necessary for weapons arms races to escalate: namely, the importance of duels. If fighters are constrained to a one on one confrontation, the best fighters reliably win, so there is an arms race to evolve bigger, better weapons. In the absence of a duel, say, in a scramble of ardent male horseshoe crabs or in battles with guns instead of swords, this tight correlation between an individual fighter’s abilities and the chances of winning breaks down, so extreme personal weapons are unlikely to evolve. Interestingly, this idea comes from military history, a subject that is skilfully interwoven into the entire book, with illuminating results. Briefly, the reasoning behind this is that large weapons are costly, and thus an honest signal of fighting ability (an idea developed in another fun book, The Handicap Principal) [3]. Once large weapons become honest signals, they act as deterrents to inferior combatants because it is cheaper for both sides to avoid a fight with a known conclusion. This second function would select for extra large weapons because extra large signals would be more daunting than just slightly larger ones, even if the latter would still help you win a fight. So given the existing ingredients for an arms race, with an excess of males duelling for defensible resources, the increasing selection pressure to evolve bigger weapons faster should case the arms race to accelerate. A second novel idea is the prediction that in symmetric arms races that constrain members of the same species and sex to a duel, the race will accelerate towards the end.

While both authors use their passion and personal experience to introduce the broader implications of arms races, the two books are an intriguing contrast in tone and content. Animal Weapons, as the title implies, is largely about escalating conflict between members of the same sex and species. This is consistent with Doug Emlen’s childhood fascination with arrowheads and his brilliant scientific work on how and why male beetles evolve and develop such a diversity of horns (or other ways to gain a mate). Just like the increasingly enormous and elaborate weaponry in the book, American hyperbole may have been subjected to a similar arms race to impress. Emlen’s writing is infectiously engaging in its sincerity, and like the subject matter, it is certainly forceful. In contrast, Cuckoo is full of English understatement, while still managing to bubble with humour and enthusiasm like a pair of twinkling eyes in an otherwise impassive face. The arms races it deals with focus specifically on trickery and detection, sneak invasion and defence, rather than on the broader theme of battle, be it duel or siege, in nature or culture.

Both books are especially worth reading because they bring alive the personalities and passions of their authors in ways that few popular science books succeed in doing. Any aspiring scientist should want a window into how both these top scientists think, and anyone else will simply enjoy biology at its best. By best, I mean a deep love of natural history and an abiding sense of curiosity that fuel the skill and dedication needed generate and test ideas to explain how and why the living world works the way it does. These people love what they do and both books are full of endearingly self-deprecating anecdotes and personal insights. For instance, Davies often writes of identifying with the birds he has watched with fresh joy every year, and observes that like the territorial reed warblers he studies, he prefers to have his own patch when doing fieldwork. This led to an almost sleepless night when a warden told him an old man had been spotted searching for nests in his beloved patch, till he realised with relief the next morning that the “old man” must have been himself. A characteristic Emlen anecdote (some of the funniest are lurking in the footnotes) is all action and adventure, including one about getting covered in hundreds of minuscule ticks while valiantly collecting howler monkey poo miles from camp in a daily struggle to keep some very precious dung beetles fed.

Another very engaging aspect of both books is their constant reference to history and art. Davies writes often of personal sources of inspiration, which include poetry and art that make him see nature in a new light. He pays a special tribute to Eric Ennion, a self-taught and superb bird painter, and his account of how Edgar Chance, a Victorian gentleman, worked out the natural history of cuckoo parasitism is more thrilling than any detective fiction. Emlen writes of unearthing old arrowheads or Mayan with the same deep empathy for how others saw the world, and Animal Weapons is full of interesting military history.

Reading both books made me think about how biologists apply the notion of arms races in evolution, and which arms races they choose to focus on. To borrow the very useful framework from Dawkins and Krebs, evolutionary arms races can come in four broad flavours, each with predictably different outcomes. Cuckoo is largely about asymmetric arms races between species. The asymmetry refers to what Dawkins calls the “life-dinner principal”. A hare that doesn’t run fast enough loses its life, whereas a fox just loses its dinner. Animal Weapons touches on this type of race, but is largely about symmetric arms races within species, such as duelling males fighting for the chance to mate, and escalation results in the evolution of extremes.
Similarly, a cuckoo chick that doesn’t manage to convince hosts to take care of it loses its life, whereas duped host parents lose some children, but live to breed another day. It may not be too surprising to see hosts "lagging" in the arms race against brood parasites.
There are two more categories of arms race that these books don’t focus on. Symmetric arms races within species, essentially what Darwin referred to as his “Principal of Divergence” [4], and causes the phenomenon modern biologists call character displacement. No one really focuses on this category as an arms race, possibly because it encompasses most of ecology, and is too loose and broad to be useful. More interesting, and alluded to in Cuckoo, are asymmetric arms races within a species. Parent-offspring conflict [5], for instance, or conflict between genes inherited from fathers and genes inherited from mothers [6]. A particularly delightful example is a fairly recent paper by David Haig, proposing genomic imprinting for infant sleep as a way for paternally inherited genes to delay inter-birth intervals so that mothers invest more than is optimal for their genes on the current child [7].

I suspect my personal attraction to arms races is due to the irony inherent in a process that produces such beauty, complexity and diversity from conflict. Like anything historical, much of evolution occurs because of chance, such as a meteor colliding with the earth, or a few finches colonising a new island. The really compelling thing about natural selection is that it explains the non-chance side of evolution – the exquisite fit between form and function. And natural selection gets most interesting not when organisms are adapting to the physical environment, but when the environment consists of other organisms, be they siblings, parents, predators or parasites, because they co-evolve. In other words, an arms race ensues. To butcher Darwin’s almost biblical concluding paragraph in the Origin [4], “from the war of nature…endless forms most beautiful and most wonderful have been, and are being, evolved.”

1.         Dawkins, R. & Krebs, J. 1979 Arms Races Between and Within Species. Proc. R. Soc. B-Biol. Sci. 205, 489–511. (doi:10.1098/rspb.1979.0081)
2.         Spottiswoode, C. N. & Stevens, M. 2010 Visual modeling shows that avian host parents use multiple visual cues in rejecting parasitic eggs. Proc. Natl. Acad. Sci. U. S. A. 107, 8672–8676. (doi:10.1073/pnas.0910486107)
3.         Zahavi, A. & Zahavi, A. 1999 The Handicap Principle: A Missing Piece of Darwin’s Puzzle. OUP USA.
4.         Darwin, C. 1859 On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. 1st edn. London, UK: Murray, John.
5.         Trivers, R. L. 1972 Parental investment and sexual selection. In Sexual selection and the descent of man, 1871–1971 (ed B. Campbell), pp. 136–179. Chicago, IL: Aldine.
6.         Haig, D. 2004 Genomic imprinting and kinship: how good is the evidence? Annu. Rev. Genet. 38, 553–585. (doi:10.1146/annurev.genet.37.110801.142741)
7.         Haig, D. 2014 Troubled sleep Night waking, breastfeeding and parent–offspring conflict. Evol. Med. Public Health 2014, 32–39. (doi:10.1093/emph/eou005)

Monday, November 17, 2014

Sperm and chromosomes competing

The mouse Y chromosome has recently been revealed, and its content is strikingly different from the handful of other mammalian sex chromosomes sequenced so far. I have written about how the many recently acquired, repetitive DNA sequences in the mouse Y are signatures of a evolutionary arms race with the X chromosome. In short, both the Y and X chromosomes in the house mouse genus have 50-100 copies of the same three sets of genes, because the copies on the X are "drivers" that exclude Y chromosomes from the next generation, while copies on the Y are "suppressors" that defend the Y chromosome.

This is a classic instance of one of my favourite evolutionary phenomena with the unfortunate, clumsy names, "meiotic drive" and "segregation distortion". The reason drive is so compelling is that it is the archetypal result of selfish genes in action, and the perfect example to trot out when explaining that selection does not act "for the good of the species", or sometimes, for the good of the individual.

From the viewpoint of a driving allele (a particular version of a gene) on the X chromosome, genes on the Y chromosome are a waste of space. A good way to double its fitness, would be to make sure none of the Y chromosomes get into sperm, so all the offspring of a male with this driving allele will be daughters (because he would only make sperm with X chromosomes). This is no good for the Y chromosome, and it seems to have solved the problem by acquiring genes that resemble the driving X copies enough to suppress them. An arms race of more driving X copies and more defending Y ensues.

The other cost of a driving allele, whether it is on the X or some other chromosome, is that the male carrying this allele will be making much less sperm than males without the rogue gene. Essentially, his sperm making efficiency is being compromised by these selfish genes because sperm that don't carry them don't make it to the next generation.

If all males had exclusive access to their mates, this wouldn't be much of a problem, since even half their sperm would be more than enough to fertilise eggs. However, most female mice are likely to mate with more than one male, so sperm competition would select for males without driving alleles because they would have more sperm than males handicapped by internal genomic conflicts.

One prediction that arises from this, is that one should see more signs of an arms race between genes on the X and Y chromosomes in species with less sperm competition. In other words, more repeated copies of the driver and suppressor alleles on both sex chromosomes -- a phenomenon known as co-amplification. The sex chromosomes of three mouse species in the Y chromosome paper do indeed vary in composition and size, but it isn't clear how much sperm competition varies in these species. Furthermore, mating systems are notoriously variable and evolve rapidly, so they might not generate a steady enough selection pressure to detect clear differences in co-amplification between conflicting sex chromosomes.

Soh, Y. Q. S., Alföldi, J., Pyntikova, T., Brown, L. G., Graves, T., Minx, P. J., … Page, D. C. (2014). Sequencing the Mouse Y Chromosome Reveals Convergent Gene Acquisition and Amplification on Both Sex Chromosomes. Cell159(4), 800–813. doi:10.1016/j.cell.2014.09.052

Sunday, October 5, 2014

Learn about evolution and laugh

Most readers of newspapers or magazines are likely to have encountered evolutionary explanations and worse, justifications for almost any human activity, from rape to raw meat diets. There are several things wrong with these melodramatic logical leaps. In Paleofantasy, Marlene Zuk masterfully, and with characteristic bluntness, debunks every fallacy and fantasy, walks you through the basics of evolutionary theory and makes you laugh out loud, all at the same time.

The subject matter for this book is brilliant, because as humans, which one of us isn’t really quite fascinated by our own history, and what it might mean for our present and future behaviour? There are a slew of well-written introductions to evolution on the market, many of which spend a great deal of effort trying to convince readers that evolution does indeed occur. There is nothing wrong with these books, but they tend to attract readers who are already members of the evolutionary choir, rather than people who might otherwise consider themselves largely uninterested in science. Almost anyone would be interested in questions like: Are humans still evolving? What does evolution tell us about what we like to eat, do for fun or why we get old and die when we do? In answering these questions, Zuk brilliantly explains both the key theory and some fairly abstruse methodology with such clarity and humour that without realising it, the reader is given a first class grounding in modern evolutionary biology. That is what makes this book the perfect gift and ideal reading in an introductory course for non-biology majors while still being great fun for any biologist, who must often trot out similar vignettes for friends and family.

One of the most commonly encountered confusions are arguments along the lines of “our ancestors evolved to do X (where X can be running barefoot, or being promiscuous) therefore we are justified in doing X. Paleofantasy steps through aspects of human life, from diet, to exercise, sex, birth, death and disease, and two threads run through the book: firstly, that what is “natural” or “evolved” does not equal what is good, and secondly, that it’s usually jolly tricky to know what is “natural” in our evolutionary past.

Advocates of paleolifestyles seldom agree on what is natural, and for good reason. There simply isn’t much evidence for a single, static and decipherable Flintston-esque evolutionary past for humans, so it’s anyone’s guess what our ancestors did, which allows for personal preferences to run amok. Zuk is particularly good and finding stunningly funny quotes from earnest Paleo-bloggers who rhapsodize over the beneficial effects of subsisting on pork belly or doing spontaneous busts of press-ups and sprints to simulate the heaving of boulders and the need to flee from enraged rhinos in our so-called evolutionary past.

Zuk’s main point, which she dedicates a chapter to, is that evolution can happen a lot faster than you might think, and that it can occur at very different speeds. So even if there were a relatively long period of environmental stability in our past, that doesn’t mean we haven’t changed genetically since the invention of agriculture. Besides, humans pride themselves on their flexibility and ingenuity, so it should come as no surprise that in our evolutionary past, we were probably rather good at moving about, living in a wide range of places and with a wide range of social systems. We are generalists like rats, and we like to think we’re smarter. This chapter on rapid evolution is probably my favourite, because it introduces some of the most classic examples of rapid evolution like finch beaks and viruses, but also displays some of Zuk’s own work on Hawaiian cricket males who have evolved in the space of a few years to stop serenading females because the song also attracts deadly parasites that would otherwise kill the males before they had a chance to mate.

In the very next chapter, Zuk discusses the poster child of human evolution – the ability of cattle-herding populations to digest milk as adults. Not only is this example a jolly good bit of evidence for rapid, culturally imposed (you could say self-inflicted) human evolution, it also gives Zuk the chance to explain some tricky methodology with admirable clarity and simplicity. And it will give readers a good idea of just how biologists work, from collecting the blood and spit of people around the world to the logic underlying computer tests.

Peppered throughout the book are not just pictures of how science is done, but also an affectionate but perceptive portrayal of scientists as people. Starting with her own delightfully distinctive, no-nonsense style, wry humour and sensible brand of feminism, Zuk is superb and showing how every scientist has his or her own (often enchanting) biases and mannerisms. She lets slip that Linnaeus, father of modern biological classification, decided to name the main plant groups according to the numbers of husbands or wives each plant had. Similarly, the Grants, who measured natural selection in action on Darwin’s finches in the Galapagos come alive in her anecdote about their group meeting on returning from the field after a massive El Nino changed the landscape dramatically from brown and barren to a verdant paradise. The Grants and their students could barely contain themselves at the sight of photos, excitedly remarking upon every tree, resplendent in unaccustomed greenery. In contrast, Zuk, then a student from a different lab, found this so tedious she had to slip out. That anecdote and many others, captures both the thrilling and the mundane in science, practised by subjective scientists. For a superb book on the Grants' work, I highly recommend The Beak of the Finch.

Paleofantasy doesn’t simply showcase instances of evolution by natural selection as demonstrated by Darwin’s finches. Zuk deals directly with the fact that evolution is simply defined as change, and so can occur in different ways, of which selection, whether natural or human is merely one. For those who might want reassurance that this is indeed a good introduction of evolutionary theory, Zuk explains concepts like drift, the role of contingency and history in evolution, adaptive landscapes, arms races and the ideas that evolution is a tinkerer. If these phrases are Greek to you, read the book. She also puts to rest the notion that evolution is in anyway directed, or that any living thing today could be “more evolved” or superior to any other living thing, since they have all been evolving for equally long. 

The only aspect of evolution I would have liked to see more of in this marvellous book is conflict. Perhaps this is because Zuk didn’t wish to put off people with a rosier view of human nature, but as we’ve established, nothing in evolution prescribes or justifies our moral choices. She does present the intriguing notion that humans have an unusually extended childhood as a way for parents to have a lot of relatively cheap labour. However her chapter on family remains relatively silent on the converse scenario in parent-offspring conflict, where children can be thought of as little machines for manipulating parents into caring more for them than for their current or potential siblings.

There is a delightful extension of the theory behind parent-offspring conflict, proposed by David Haig, which essentially explains much of behaviour or even foetal growth in terms of conflict between genes inherited from mums and dads within an individual’s body. It’s as if your parents could extend their evolutionary battle to your body, rather than just tussling over who is left holding the baby. For instance, Haig just proposed that genes inherited from fathers are the copies that make babies cry more at night, the better to exhaust mum so she takes longer to produce a competition in the form of a sibling. In contrast, copies of the same genes inherited from mum would make babies less likely to cry. This, and all other instances of Haig’s conflict explanation for “genomic imprinting” – the phenomenon where a gene’s actions differ depending on the sex of the parent they came from, rather than the actual gene sequence – is contingent on males being unable to guarantee that they will always be the exclusive mate of a female. As a result, genes from fathers will benefit if they can cause offspring to behave in relatively selfish ways, such as growing rapidly in utero, while genes inherited from mothers can best counter this by having the opposite effect on offspring, such as silencing signals to grow. It’s not that mothers don’t need healthy offspring, but they would pass on the most genes if they could divide up their lifetime’s resources evenly across an optimal number of children. In contrast, males who might only father one or some of that mother’s children, will have not genetic interests in her other progeny, and their genes would do best if they could cause their offspring to exploit mum as much as possible, to the detriment of mum’s other offspring. My favourite popular books on the general subject of conflict (and cooperation) are still The Selfish Gene and TheExtended Phenotype by Richard Dawkins. Please don’t get put-off by his later polemical pieces like The God Delusion.

Zuk herself is arguably most famous for the “Hamilton-Zuk hypothesis”, which is founded on the continual conflict between sexually producing organisms and their parasites. The notion is that the main way for relatively slowly reproducing things like humans to stay one step ahead of bacteria and viruses is to keep coming up with new combinations of immune defences encoded in our genes. These genes can be reshuffled, where genes from our mum and dad are literally recombined every time one of us makes eggs or sperm, and then they get paired with a new mixture when we have sex. The sexiest mates should be the ones that will help make children with the most varied combinations of genes, the better to confound those rapidly reproducing parasites. If you want a more thorough treatment, you should read Zuk’s book Sexual Selections. But if you just want a good general Christmas present for anyone who likes reading, please consider Paleofantasy.

Thursday, June 5, 2014

A rare bird

Bicknell's thrush (Catharus bicknelli)

This Bicknell's thrush was singing lustily at the misty top of Pico Peak, VT one ethereal May morning. Recently designated a separate species from the grey-cheeked thrush (Catharus minimus), which breeds just south of the tundra and winters in the tropical forests of South America, the Bicknell's thrush is a good deal more impractical. It breeds on mountaintops in New England and southeastern Canada, and only winters on montane forests in the Caribbean. Courtesy its hopelessly selective preference for some of the habitats most vulnerable to anthropogenic degradation, there aren't many of these birds left.