Claims that evolutionary biology is flawed or importantly incomplete are as old as the field. The criticisms are characterized by their diversity at any given time (as seen in the laundry lists of ideas and observations that are championed by critics; Ho and Saunders 1984; Pigliucci and Müller 2010; Chorost 2013; Rose 2016a), and by their persistence over time (West-Eberhard 2009); there are very strong similarities between the arguments of, say, mid-twentieth century critics (e.g. Waddington 1957, 1960; Bateson 1958), and critics writing over 50 years earlier (e.g. Mivart 1871; Mozley 1884, pp. 396–7), or 50 years later (e.g. Laland et al. 2011, 2014; Teresi 2011; Rose 2016a, b).

This does not mean that the critics are wrong. Both the diversity and persistence of criticism might be explained by intransigence and lack of ambition in the field, by “the intolerance and narrow-mindedness of some of those who advocate [Darwinism]” (Mivart 1871), particularly in its “orthodox”, “ultra” or “hardline” forms (Teresi 2011; Rose 2016a).Footnote 18 However, this explanation is not very plausible. Critics and “novel” findings of all kinds have never lacked attention in evolutionary biology, and this sprawling field could have no means of enforcing conformity to any of its tenets,Footnote 19 even if it could agree on what they were.

It has been argued here that the discontent is better understood as stemming from a few inescapable properties of living things, which lead to disappointment with evolutionary biology, and a nagging feeling that reform must be overdue. It has been further argued that particular discontent stems from misunderstandings and dislike of one well-known subfield: the study of adaptive function, in the tradition of behavioural ecology (Tinbergen 1963; Cuthill 2009). One of the few things shared by the laundry list items is their minor role in theories of adaptive function. Therefore, all can be championed as alternatives to such research (things we that we might, or should, study instead), or as observations that promise to invalidate these theories (because they affect outcomes in the world, but are not centre stage in the theories). This subfield is a particular target because it is atypical (most researchers do not share its goals), because it requires a very partial description of evolution (as something like inclusive fitness maximization), and because it uses ideas of apparent purpose and imaginary agency, but in a limited way (to make testable predictions, and not to inspire or dignify).

For all of these reasons, the special criticism directed at the subfield is not surprising, but it is a pity. With its inherent focus on plastic phenotypes (Grafen 1999), and whole organisms (Grafen 2007), its common focus on sociality and cooperation (West et al. 2007), deep roots in ecology (Cuthill 2009), strong ties to developmental biology (Hogan and Bolhuis 2009), agnosticism about the details of inheritance (Grafen 1991; Gardner 2011), and above all, its remarkably productive synthesis of modelling, field observation and experiment, behavioural ecology seems like the sort of science that many critics of evolutionary biology might otherwise embrace.

If the account above can explain some puzzling things, it also has obvious weaknesses. First—and as ever in biology—an attempt to explain a pattern is not to deny the exceptions. This article makes no serious attempt to rebut any single criticism of evolutionary biology, and no attempt at all to restrict what is studied. What has been argued is that there can be smoke without fire—that persistent and voluble criticism of evolutionary biology is to be expected, whether or not anything is seriously wrong.

Second, the above account involves some speculation about extra-scientific motives, and this is always foolhardy and offensive. But it may be unavoidable. We do need to explain why ideas are so often hailed as important before they have done much scientific work, and why claims that seem utterly banal (‘things are more complicated’, ‘natural selection doesn’t explain everything’, ‘individuals with the same genotype can have different phenotypes’), might be treated as momentous, vital or urgent. It is also undeniable that a lot of writing about evolutionary biology has its mind on higher things (the same, shopworn collection of topics, from Marx and Spencer, to markets and trolley problems). Evolutionary biology, like history, but unlike other natural sciences, raises issues of purpose and agency, alongside those of complexity and generality (Anonymous 1953; Mount 2016), and so there will always be those who agree with Carr (1964) that methods and explanatory goals cannot and should not be separated from political or religious agendas (Maynard Smith 1998, Ch. 5; Rose 2016a). Some may even agree with Bateson (1958), that Waddington’s work on genetic assimilation (showing that environmentally-induced traits can become less sensitive to environmental conditions following allele frequency change) really does have implications for “the battle between non-moral materialism and the more mystical view of the universe”.Footnote 20 It is remarkable, for example, that much of the funding for challenging current practice in evolutionary biology comes from The John Templeton Foundation (Pennisi 2016), which is committed to using science to reveal underlying purpose, and rejecting what Nagel (2012) calls “the Materialist Neo-Darwinian Conception of Nature”. But perhaps this is just history repeating itself as farce: if poetry couldn’t save us, nothing on the laundry lists will either.

If criticism of evolutionary biology is inevitable, why grouse about it? It is easy to habituate to misleading alarm calls (Cheney and Seyfarth 1988), and churlish to complain about peripheral ideas, which, by definition, have little influence on what most scientists do. However, claims that evolutionary biology is misguided or importantly incomplete are not harmless, but actively hinder progress in the field. Indeed, they do so in several ways. First, the claims misrepresent the field to the wider public. It is unfair to use guilt by association—many fine studies are cited on creationist websites—but a field that urgently needs reform is a field “in crisis” (Mazur 2010), and when it fails to reform, this lends credibility to claims that scientists are, at best, hidebound and foolish, and at worst, guilty of ideologically-motivated deception (Mazur 2010; Teresi 2011). Such claims find an eager audience among those who reject the scientific consensus on other grounds. For example, Fodor and Piattelli-Palmarini (2010) present a priori objections to (their version of) natural selection, but also include a fairly typical laundry list to add some empirical heft. Chorost (2013) criticized Nagel (2012) for not including a laundry list. Second, and within the field, the claims encourage neophilia. This makes us unwilling to build on previous work, to integrate new findings and ideas with existing explanatory frameworks, to replicate published results (Nakagawa and Parker 2015), or to solve the field’s many outstanding problems (Maynard Smith 1977; John 1981). It also distracts attention from the ways in which all biologists can do something genuinely new, such as expanding the range of study organisms. The comparative method (Maynard Smith and Halliday 1979), Krogh’s principle (Krebs 1975), and our ignorance of biodiversity (Nee 2004), all suggest that this is one way that we might usefully extend the field.