Portal de Periódicos da CAPES

Evolution’s weather vane?

2017; Elsevier BV; Volume: 27; Issue: 17 Linguagem: Inglês

10.1016/j.cub.2017.07.037

1879-0445

Simon Conway Morris,

Evolution and Science Education

Nobody, or so we all hope, imagines evolution to be entirely open-ended. A myriad of factors — fluid viscosities, the electromagnetic spectrum, the affinity of phosphorous for oxygen, and for all I know, the cosmological constant — collectively constrain in their various ways the paths of evolution. Conversely, not even the most ardent enthusiast for convergent evolution imagines the process to be entirely deterministic. The balance lies somewhere in between, although to echo Jorge Luis Borges’s famous conceit, I suspect that the discussion will be more reminiscent of two bald men fighting over a comb. Admittedly, Borges was talking about the Falklands War, but is the conflict amongst evolutionary biologists between those in favour of Fate as against those who look to Chance that much different? Both sides have important points to make, but given we only have one history of life, and know nothing of extraterrestrial alternatives, maybe the debate will ultimately prove futile? Or maybe not. To what extent evolution is broadly predictable matters very much indeed, and for two reasons. Firstly, if evolution does turn out to be highly channelled, then we will have a reliable guide to the biology of extraterrestrials (if there are any). Secondly, this debate re-opens the question of what are the driving forces of evolution. Natural selection is obviously one, which tallies with the adaptive constraints that convergence repeatedly reveals. However, are there deeper forces at work, as hinted at by the great D’Arcy Thompson — forces that delineate a sort of universal, if not Platonic, biology? When evolution is spoken of in terms of ‘attractors’, as indeed it increasingly is, then convergence may be telling us something much more important about the evolutionary landscape. Improbable Destinies represents a finger-post in these ongoing debates, but is it pointing in the right direction? There are few better people to address these questions than Jonathan Losos, not least because of his classic analysis of the ecomorphs of anolid lizards. Not only is this example an object lesson in convergence, revealing uncannily similar evolutionary solutions to living in the various habitats of islands such as Cuba and Jamaica, but also his work depended on dedicated and challenging field work. It is in this broad area that his book really shines, narrating as it does the trials, tribulations and occasional joys of life in the field and in the laboratory. These various campaigns include truly epic projects, not least Rowan Barrett’s work in the Nebraska sandhills building mega-pens for his deer mice and Rick Lenski’s industrial-scale study of the evolutionary trajectories of Escherichia coli. These studies and a series of parallel investigations are exemplars of not only the ingenuity of the experimental method, but also importantly reveal the scientists’ scope of imagination, be it tackling an entrenched bureaucracy at Rothamsted (the famous Park Grass Experiment) or building a twenty-pond stickleback hotel. That the latter, based at the University of British Columbia, has been nicknamed the Speciation Accelerator is not entirely fanciful. In their various ways, these projects echo the scale and enterprise of high-energy physics and giant telescopes. As importantly, to the first approximation, these and other research programmes point to a recurrence of evolutionary outcome, although the devil is often in the details. Either way, Losos’ descriptions of the ins and outs of life at the scientific coal-face are thrilling, exemplifying the very best traditions of popular science writing. The wider canvas to all of this is to take up Stephen Jay Gould’s baton and once again ask what evolutionary outcomes we might expect if ‘the tape of life’ were to be re-run. Gould’s position, and possibly mine, need little rehearsal. Are the twists and turns of history sufficient to redirect evolution in effectively unpredictable trajectories? Alternatively, does the ubiquity of convergence suggest that certain outcomes, including intelligence, are inevitable? Drawing on John Beatty’s work, Losos offers us a more nuanced approach regarding these evolutionary contingencies. Beatty suggests there is an important distinction. Are we looking to unpredictability per se — an asteroid on the head, a chance mutation, that sort of thing — or alternatively, does it depend on causal dependencies, such that State D is very unlikely to arise without prior States A, B and C? As it happens, these distinctions soon run into trouble. Mutations, for example, may be more constrained than is sometimes thought, not least in terms of the hotspots that Virginie Orgogozo and others have pinpointed. So too, on ‘day zero’ mass extinctions are exceedingly tiresome, but at heart these episodes are paradoxically creative, accelerating what is going to happen anyway. Trilobites were always doomed, molluscs were already taking over the oceans in the Palaeozoic, mammals were busy diversifying in the Cretaceous. Mass extinctions change the time-scales, but not the rules. In addition, co-option and redeployment readily sabotage many causal chains — think for example of the crystallins. And when all else fails, nature is adept at re-invention, as with the olfactory proteins of insects which blithely draw on proteins entirely unrelated to the opsins to arrive at the classic 7TM configuration. These notions will be unpacked elsewhere and perhaps are less germane to the immediate issue at hand. This is because at the heart of Losos’ book lies the conviction that, while convergent evolution is important, perhaps even under-appreciated, it is wildly ambitious to then proceed to the claim that evolution is predictable. It is here, however, that his analysis begins to unravel, and in a number of interesting ways. Things get off to a slightly shaky start with a brief discussion of what are claimed to be evolutionary ‘one-offs’, such as the archer fish or elephant’s trunk. It all depends on what you mean by ‘one-off’. An anabantid fish (Colisa) also enjoys spitting, while for probiscidean trunks, the fossil record suggests the fully fledged appendage evolved at least five times. Better still, the extinct dinotheriums had a nasal protrusion more reminiscent of that of the proboscis of the perissodactylean tapirs. Finally, by reminding oneself of the wider functional constraints of muscular hydrostats, we then discover that the elephant trunk has perhaps under-appreciated convergences with the mammalian tongue, and even the tentacles of the Pearly nautilus. In this way, we begin to view evolution in the context of the wider patterns of recurrence that transcend specific taxonomic groups. Not that Losos fails to supply us with many interesting instances of convergence — dinoflagellates pretending to be tapeworms and that sort of thing. Both George McGhee and I have attempted more complete rosters of examples, and yet another catalogue is scarcely necessary. Nevertheless, among his chosen examples, Losos perhaps sells us a bit short. It is a pity, for example, that among the woodpecker avatars he didn’t include the Madagascan vangid Falculea or Neotropical furnariids (e.g. Xenops), nor amongst extinct mammalian woodpeckeroids call upon the notoungulates (Hegetotherium), marsupial Yalkaparidon, let alone the more familiar apatemyids. So too, with the mantid forelimb attention is rightly drawn to the mantispids, but what about the six other insect groups that arrived at the same solution, not least the staphylinid beetles? When it comes to convergence, the occasional coincidence may be unremarkable, but recurrence should make us suspicious. Remember the warning to 007 by Goldfinger: “Once is happenstance. Twice is coincidence. The third time, it’s enemy action”. These remarks are perhaps only quibbles. More serious are three aspects of how we view convergence. The first is that in this book, for the most part, the fossil record receives too short a shrift. Given its lamentable incompleteness, perhaps this is justified. Even so, and to give only one example, the much wider geographical distribution of extinct marsupials leads one to suspect that far beyond such classic examples as the thylacosmilids, many more convergences with the placentals are yet to be recognized. Could, for example, the Eocene Ghamidtherium be a marsupial bat (www.42evolution.org/can-kangaroos-fly-2/)? The second question revolves around how one construes one’s convergences. For example, Losos patiently unpacks the correspondences between such filter feeders as the whale shark and baleen whales, but goes on to point out that, on closer inspection, the similarities are pretty wobbly. The latter, for example, are very unlikely to re-evolve gill slits. Quite right to bring this up, and did anybody think otherwise? However, much more exact and informative convergences exist — with the whale shark, go to such fish as the Mesozoic pachycormiforms like Ohmdenia and Rhinconichthys (or even the Palaeozoic titanichthyids). And for the baleen whale? The first convergent port-of-call is the brown pelican. In documenting this apparently ludicrous convergence, Daniel Field and co-workers not only provide an elegant documentation as to why we might want to compare a bird and cetacean, but stress that this convergence is substantially deeper than it might at first appear. And this too is a point neglected by Losos. Repeatedly among convergences, we find an entire complex of correspondences that demonstrate how the same problems may be solved in apparently diverse ways, but lead to integrated systems whose functions are effectively identical. The third point concerns the combinatorial vastness of evolutionary ‘hyperspace’ — the territory of immense numbers that far exceeds the small change used by cosmologists — versus what appears to be the infinitesimally small number of viable solutions. Losos wheels out an old canard, the duck-billed platypus, holding it forth as an evolutionary singleton. Most likely he is correct but is that the point? Returning to the example of the elephant trunk as a muscular hydrostat, it is the wider argument that matters. In the grand scheme of things, how likely is it that structures such as the electro- and mechanoreceptors, the type of toxin or its method of delivery, will evolve? From the narrow perspective the duck-billed platypus is indeed, as Losos says, “a mishmash”, but in the wider world these (and many other) examples demonstrate that there are basic and inescapable features of biological organization. In terms of sensory systems, not only those arrangements employed by the duck-billed platypus, but all other types (including even infra-red detection) are variants on a handful of themes. And the same applies to toxins. Various, certainly. Unlimited? Apparently not, and as any protein chemist will tell you, with very good reason. And so it continues. When Losos writes “a single, optimal solution exists, leading natural selection to produce the same evolutionary outcomes over and over” (p. 5) he misses the point. Not a unique solution, but a handful of them are used, repeatedly. Are there any truly unique solutions? Quite possibly there are, but still one should be careful. The bolas spider might qualify as one (although the sex pheromones it employs are convergent), and so too might the mutation that allows E. coli to access citrate (even though this bacterium has evolved different mechanisms to the same end). To imagine, however, that these re-affirm the open-endedness of evolution is grasping at straws. So, who deserves possession of Borges’s comb? Losos is probably with the majority in his opinion, but the jury is still out. Not that a lack of resolution should be a disappointment, especially because there are at least two other elephants in the room. One that Losos briefly addresses is the quandary of human uniqueness. Predictably, he follows the received wisdom that the nascent cognitive capacities in a number of species, consistent of course with the undoubted evolutionary continuity between humans and other species, provide a bridge that is reinforced by the archaeological record. But just how secure is this bridge? What Thomas Suddendorf has labelled as ‘The Gap’ may yet open some unexpected doors, not least in terms of language, mathematics and music. These questions, of course, go far beyond what Losos has set out to do, but we should all appreciate the irony that only one species knows that it has evolved, and at least some of its representatives find this fascinating. So too, only we would wish to know if animal vocalizations are a sort of proto-language (seemingly not), that mathematics emerged from numerosity (most unlikely) or that a direct line of continuity runs between whale song and the closing section of Götterdämmerung (if you believe that you’ll believe anything). The acid test to all these points, and indeed the entire thesis presented in Losos’ challenging book, will be the documentation of extraterrestrial biospheres. Losos presents us with an intriguing list of some of the alternative possibilities. When, however, I recall that a dog and a cockroach walk in very much the same way, that leaky membranes will generate warmth, plants will evolve seeds and reptiles a placenta, then I am moderately confident that, however bizarre in appearance these organisms might be, on closer inspection, our extraterrestrial counterparts will be remote only in terms of the parsecs that currently separate us. So, after this robust defence of convergence, surely I will continue to man the barricades, dodging the bullets and smiling sweetly at the swirling crowds? Hardly necessary. In Current Biology alone since the beginning of this year I count at least six mainstream papers on convergence. Quite frankly, the whole business is becoming far too popular. Time to move on.