Flaws of Nature The Limits and Liabilities of Natural Selection

Back in 2019, I reviewed Daniel S. Milo's book Good Enough which was a critique of adaptationist storytelling. For organisms to survive, evolution by natural selection does not, and need not always result in perfect adaptations. Andy Dobson's Flaws of Nature revisits this thought-provoking idea will reel you right in: "It's evolution, but not the Greatest Hits" (p. 16).

Most popular accounts of evolution focus on the amazing adaptations of organisms to their environment. But, Dobson counters, "whilst there seems no end to evolution's artistry, it is all too easy to be blinded by the pyrotechnics on display" (p. 14). To better understand natural selection it is equally instructive to consider what it can not do. Though on paper it is a relentless mechanism to weed out the evolutionary unfit, in practice the process often results in suboptimal adaptations, cumbersome traits, evolutionary dead ends, and runaway selection that in the end is costly to all parties involved.

A large chunk of this book looks at the different kinds of conflict that prevent perfect adaptations. In many situations, the interests of the different parties in life's interactions do not necessarily align. Several chapters consider conflicts between species, such as arms races between predators and prey, birds that continue to be the victim of cuckoldry, and an unending battle with parasites that hosts seem unable to win. The really quite interesting reason these conflicts persist is that the stakes are lopsided or, in more technical terms, that selection pressures are uneven. In the context of predator-prey interactions, Richard Dawkins and John Krebs coined the "life-dinner principle" in a 1979 paper. Simply put, predators stand to lose a meal, while prey stand to lose their lives. Thus, there is a far stronger selection pressure on prey species. Indeed, most predation attempts in nature fail. As Dobson details, similar dynamics with uneven selection pressures also underlie cuckoldry and parasitism.

Then there is conflict between the sexes. Dobson discusses the various theories proposed to explain how mate choice can lead to runaway selection for ornamental traits in one of the two sexes. You think peacock? Let Dobson delight you with tales of fish with unwieldy sword-shaped tails or flies with obscenely long eyestalks. Some sexually selected traits are risky, potentially lethal, yet "there is no way off the merry-go-round; males are doomed to exist in a precarious balance, sitting on the knife-edge between being unattractive but alive, and attractive but dead" (p. 99). This is not a men-only club, though, and Dobson discusses species where females sport ornaments and males are the choosier sex.

Other chapters examine conflict within families by looking at the evolution of altruism. Especially in eusocial insects, this can lead to extreme adaptations that seem little rewarding for the individuals involved, such as the Brazilian ant species Forelius pusillus where some workers sacrifice themselves at the end of the day to seal off the nest entrance from the outside and do not survive the night. This is closely tied to the last form of conflict considered here, that between individuals and their genes. What ultimately survives across the generations are genes; the individual is but a vessel to get them there (there is not a little nod to The Selfish Gene here). This offers interesting insights into why organisms age and circles back to the book's recurrent theme of uneven selection pressures: these also change during a lifetime. There is strong selection pressure to reproduce early to ensure you stay in the game of life. What happens to the body and the individual after that is less relevant as far as evolution is concerned. Add an idea such as antagonistic pleiotropy, i.e. genes that have positive effects at a young age but harmful effects later in life, and you start to see how senescence could have evolved.

Next to conflicts resulting from uneven selection pressures, two further chapters consider the influence of the environment. At its most extreme, natural selection leads to evolutionary traps and dead ends that leave organisms lethally vulnerable to environmental change (e.g. island species that are defenceless against invasive species). More often it leads to a parade of compromises and botch-jobs. Is it not crazy that marine mammals cannot breathe underwater? Why did they just not evolve gills? The answer is path dependency: the imprint of the past borne by all lifeforms inevitably restricts the available options. Evolution does the best it can with the material at hand but cannot go back to the drawing board.

Of all the lessons this book imparts, the most important one is an explanation for why natural selection does not necessarily result in perfect adaptations: evolution lacks foresight. There is no supervisor here that could pull all players in line and defuse an ongoing arms race, nor a grand plan that steers organisms towards a set end goal.

Flaws of Nature is admirably accessible to readers with minimal background in evolution and takes regular digressions to explain basic concepts with inventive metaphors, whether it is the evolution of sex or the concept of indirect fitness. It would be a good starting point before delving into Milo's headier Good Enough. For readers steeped in evolutionary biology, it is a welcome reminder of the sorts of questions and potential misunderstandings that those outside the field sometimes have. That said, the book simultaneously offers plenty of stimulating insights for readers who do have a background in evolutionary biology. Whether it is the finer points of the oft-misunderstood concept of kin selection or Dobson's contention that species become progressively worse off as a consequence of escalating arms races.

A subtle undercurrent in the book is how the sobering reality of evolution not invariably leading to improvements, let alone perfection, clashes with our interpretation of nature. His short final chapter makes this explicit and takes aim at the appeal to nature fallacy peddled by lifestyle gurus and alternative medicine practitioners who falsely equate natural with good: "there is no correlation between the naturalness of a product or behaviour and its inherent virtues" (p. 244). Even more treacherous is turning to nature for moral guidance, for "the natural world is full of events and behaviours that no one could reasonably view as morally instructive" (p. 246).

Flaws of Nature is a witty and smart ride into the dark underbelly of evolution. The process of natural selection becomes that much more fascinating when you focus on its flaws and limitations.