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.”

Postscript: I did some experiments in Zambia and found that little bee-eaters, African hosts of another deadly brood parasitic bird, are also remarkably maladapted when it comes to avoiding parasitism.

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)