Open Access

Evidence and Evolution: The logic behind the science: Elliott Sober Cambridge University Press, Cambridge, UK; 2008;

412 pp; ISBN 978-0-521-87188-4 (Hardback) $82.35; 978-0-521-69274-8 (Paperback) £16.99
  • Christian P. Robert1
Human Genomics20115:130

https://doi.org/10.1186/1479-7364-5-2-130

Published: 1 January 2011

Introduction

Evidence and Evolution was written by Elliott Sober, a philosopher of science who has worked on the notion of evidence, in the statistical meaning [1] of the word. All chapters relate to papers that he has authored or co-authored over the past few years. Evidence and Evolution does not aim to demonstrate the validity of one evolution theory against another, but rather at validating statistical ways of testing such hypotheses. While Sober establishes that creationism cannot be analysed within this framework because it fails to make predictions, subsequent chapters consider ways to evaluate evidence about natural selection (against the drift alternative) and about common ancestry, without drawing conclusions. Sober also relates very much to the original works of Charles Darwin -- sometimes placing too much emphasis on his over-generalisations -- but this historical touch nonetheless adds to the already considerable appeal of the book.

First, an acknowledgement of my limitations is in order. As a statistician, I cannot evaluate the philosophical relevance of the book, even though the arguments are fairly accessible to a layman like me; however, I appreciate the critical assessment of Popper's testability criterion when applied to creationism, as well as the extensive coverage of statistical principles for testing. A philosophical perspective on Evidence and Evolution is given by Pfeifer [2]. Furthermore, being equally a layman in population genetics and evolutionary biology, I have difficulties in assessing the impact on biologists of the debate about the construction of tests, as the examples given seem to be too formalised and simplistic to be realistic. My review is therefore necessarily biased towards a statistician's perspective and hence maybe unnecessarily critical in terms of what I perceive as a lack of proper modelling. Indeed, I bemoan the absence throughout the book of a genuine statistical framework that would allow for a complete statistical analysis of even one real dataset, including the estimation aspects that are bypassed, as this would illustrate much more clearly the concepts at work.

In addition, while I understand the historical and philosophical appeal of discussing creationism, since Darwin was subjected to many attacks on this very issue, I am sceptical about the impact that the book could have on the current debate. Unsurprisingly (and I will explain why below), the book discusses creationism in very general, and hence vague, terms. There are so many possible accounts of the intervention of a god or another supernatural being in the management of the world, that to pick one in particular would be like grabbing at water -- all remaining versions emerging unscathed from a detailed criticism of the chosen one. But to maintain that creationism is testable (in Popper's sense), as Sober does, is to open a similar 'Pandora's box' about which version he is considering. I thus personally deplore the inclusion of Chapter 2 in the book, even though this position is not taken on statistical grounds.

This review proceeds linearly through the four chapters of the book: 'Evidence', 'Intelligent design', 'Natural selection' and 'Common ancestry'. To reiterate, it focuses primarily on the statistical aspects of the debate initiated by Sober, without discussing the biological or philosophical consequences. Although a hard read at times, proceeding through Evidence and Evolution was a worthy and rewarding experience for me that led me to re-think the terms and objects of statistical testing when applied to a scientific theory. The book is accessible to the layman (in any of the three fields -- philosophy, biology, statistics) and I thus encourage readers to persevere with it.

Statistical evidence

Although frequency data and a well-supported empirical theory can provide a basis for assigning prior probabilities, the principle of indifference cannot. (p. 27)

The first chapter is fairly well written and presents a reasonable picture on the different perspectives (Bayesian, likelihood, frequentist) used for hypothesis testing and model choice, although it misses references to the relevant literature (for instance, there is no reference to Berger and Wolpert [3] when the likelihood principle is discussed). Akaike's information criterion is promoted as the method of choice, but this is a well-established model choice tool that can be accepted at a general level. Paradoxically, I find the introduction to Bayesian principles to be overly long (as is often the case in cognitive sciences) since, as the author acknowledges from the start, 'Bayes' Theorem is a result in mathematics [that] is derivable from the axioms of probability theory' (p. 8). This is especially blatant when considering that Sober takes a very long while to introduce prior densities on parameter spaces, a reluctance that is consistent with the parameter-free preferences of the book. The (standard) criticisms he addresses to the choice of those priors (which should be 'empirically well-grounded' [pp. 26 and 27], as also pointed out in the previous quote) periodically resurface throughout the book, but are far from convincing, as they mistake the role of the prior distributions as reference measures [4] for expressions of truth. The extended criticism of the foundations of Neyman - Pearson testing procedures is thorough and could benefit genuine statistician readers, as well as philosophers and biologists.

The Akaike framework makes plausible a mixed philosophy: instrumentalism for models, realism for fítted models. (p. 98)

At a general level, I have two statistical difficulties with this chapter. First, while Sober introduces the Akaike information criterion as a natural penalty for comparing models of different levels of difficulty, I fear that the notions of statistical parsimony and dimension penalty are mentioned much too late in the chapter. Using a likelihood ratio for embedded models is, for instance, meaningless unless a correction for the difference in dimensions is introduced. Second, the models used in this chapter and throughout the book are singularly missing variable parameters, which makes all tests appear as a comparison of point null hypotheses. The presence of nuisance or interest parameters should be better acknowledged.

Bayesianism is a substantive epistemology, not a truism. (p. 107)

At a specific level, it is not possible to address all the minor points with which I disagree, but I think Sober is misrepresenting the Bayesian approach to model choice and that he is missing the central role played by the Bayes factor in this approach. The fact that the Bayes factor is an automated Ockham's razor with the proper penalty for differences in dimension [5] is altogether missed. In particular, Sober reproduces Templeton's error [6]. Indeed, he states that 'the simpler model cannot have the higher prior probability, a point that Popper (1959) emphasised' (p. 83). And Sober further insists that there is no reason for thinking that
p θ = 0 > p θ > 0

is true (p. 84). (This commonsense constraint obviously does not make sense for continuous state spaces, since comparing models requires working with foreign dominating measures.) Even though the likelihood ratio is a central quantity in the chapters that follow, I am also reluctant to agree with introducing a specific category for likelihoodists (sic!), since, besides a Bayesian incorporation, a calibrated likelihood leads either to a frequentist Neyman - Pearson test or to a predictive tool, such as Akaike's (which is also frequentist, in that it is an unbiased estimator). In addition, the defence of the Akaike criterion is overdone, in particular the discussion about the unbiasedness of Akaike's information criterion (AIC), which confuses the fact that the averaged log-likelihood is an unbiased estimator of the Kullback - Leibler divergence with the issue that the AIC involves a plug-in estimator of the parameters, as shown on pages 85 and 101. The arguments for AIC versus Bayesian information criterion (BIC) are weak, from BIC being biased (correct but irrelevant) and Bayesian (incorrect), to the fact that it contradicts the above fallacious ordering of simple versus complex models. A discussion of the encompassing framework of George and Foster [7] would have been welcomed at this stage.

While the above points are due criticisms (from a statistician), the fact remains that this chapter is an exceptionally good and lucid discussion of the philosophy of testing and that it could well serve as the basis of a graduate reading seminar. I thus recommend it to all statistician readers and teachers.

'Intelligent' design

When dealing with natural things we will, then, never derive any explanations from the purpose which God or nature may have had in view when creating them and we shall entirely banish from our philosophy the search for final causes. For we should not be so arrogant as to suppose that we can share in God's plans. René Descartes, Les Principes de la Philosophie, Livre I, 28.

The second chapter of Evidence and Evolution tries to address the case of 'intelligent' design from an epistemological perspective -- namely, as to whether or not evidence-based reasoning can be applied to this line of thought. As pointed out above, I was loathe to get into this chapter, for fear of being dragged into a barren and useless debate, but it stands the test from an academic perspective, in that it is written from a purely philosophical perspective. I was originally expecting more statistical arguments, given the tenor of the first chapter, but I realise that this would have been a fruitless exercise, given the infinite polymorphism of 'intelligent' design theories.

Tout étant fait pour une fin, tout est nécessairement pour la meilleure fin. Remarquez bien que les nez ont été faits pour porter des lunettes, aussi avons-nous des lunettes. Voltaire, Candide, Chapitre 1.

I find the introduction of the chapter interesting, in that it relates the creationist thesis to a long philosophical tradition (witness the above quote from Descartes) rather than to the current unscientific debate about 'teaching' creationism in US and UK schools. The disputation of former theses, such as that of Paley's watch, however, takes up most of the chapter, which is disappointing in my opinion. (The remark that 'Paley was well-aware of the relevant facts about monkeys and typewriters' (p. 120) sounds like an anachronism, since the typewriter still had to emerge in the early 1800s. A reference to Voltaire's Candide ridiculing design would have been more appropriate.) Somehow, predictably (in the sense that this would have been my first argument) Sober mostly states the obvious when arguing that when gods or other supernatural beings enter the picture, they can explain any observed fact with the highest likelihood, while being unable to predict any fact not yet observed. I would have preferred to see hard scientific facts and the use of statistical evidence, even of the AIC sort, although -- as noted previously -- I can see the ultimate lack of purpose in picking a specific version of creationism that could lend itself to a full statistical analysis. While I consider Sober's analysis of Popper's testability to be of independent interest, as it rightly remarks that all probabilistic theories are unfalsifiable in Popper's sense (p. 130), it does not bring further arguments because Sober coherently argues that even the theory of 'intelligent' design is falsifiable.

Bayesian philosophers of science see each hypothesis as competing with its own negation. (p. 354)

In Section 2.19 (about model selection), the comparison between a single parameter model and a 1,000,000 parameter model hints at Ockham's razor [5, 810] but, once again, Sober misses the point about a major aspect of Bayesian analysis. Indeed, through the use of hyperpriors and hyperparameters, observations about one group of parameters also provide information about other groups of parameters when these are related via a hyperprior (as in small area estimation). Given that the author hardly ever discusses the use of priors over the model parameters and seems to rely instead on plug-in estimates, he does not take advantage of the marginal posterior dependence between the different groups of parameters.

Testing for selection

To test a theory, you need to test it against alternatives. (p. 190)

The 'Natural selection' chapter is difficult to read for a layman like me, in that it seems overly repetitive, using somehow obvious arguments while missing clear-cut conclusions and directions. This slant must be due to the philosophical priorities of the author but, despite him opposing a modelling using the Brownian motion to a modelling using an Ornstein - Uhlenbeck process at the beginning of the chapter -- which would have made for a neat parametric model comparison -- there is no quantitative argument or illustration found in this third chapter relating to statistics. This is unfortunate, as the questions of interest (testing for natural selection versus pure drift or versus phylogenetic inertia or even for tree structure in phylogenetics) could clearly also be conducted at a numerical level, through the AIC factor or through a Bayesian alternative. The aspects I found most interesting in this chapter may therefore be deemed as marginal by most readers, namely: (a) the discussion whether or not the outcome of a test should depend at all on the modelling assumptions (the author seems to doubt this, hence relegating Bayesian techniques to their dust-gathering shelves); and (b) the point that parsimony is not a criterion per se.

What we need is a probability distribution of the different values A might have, conditional on each hypothesis. (p. 210)

About the first point, the philosophical stance of the author is not completely foolproof, in that he concedes -- witness the above quote -- that testing hypotheses without accounting for the alternative is not acceptable. This would almost irremediably call for a truly Bayesian resolution, but my impression is that Sober looks at the problem from a purely dichotomous perspective, either the hypothesis or the alternative being true. This is a bit of a caricatural representation, as he incorporates the issue of calibrating parameters under the different hypotheses, and there is a sort of logical discrepancy lurking in the background of the argument. Again, working out a fully Bayesian analysis of a philogenetic tree -- mentioned on page 190 as one of the model's assumptions -- would have clarified the issue immensely. And rejecting Bayesianism on the grounds that 'there is no objective basis for producing an answer' (p. 239) is limited on the epistemological side. This is particularly frustrating when considering the above quote, where Sober acknowledges the need for a posterior distribution over the ancestral trait A and where he advocates using 'equilibrium probabilities as priors for the state of the ancestor A' (p. 211).

Even though I understand that the book is not trying to debate the support for a specific evolutionary hypothesis, but rather the methods used to test such hypotheses and the logic behind them, a completely worked-out example would have made it much easier for me (and perhaps other readers) to appreciate Sober's points. To mention one such issue, the construct of an efficiency or fitness function (discussed throughout the chapter; eg p. 196) that could drive the natural selection is not discussed from a realistic biological perspective but strikes me instead as a purely formal entity (the exception being the aphid-eating time of Figure 3.8). Note that Section 3.9 is more model orientated, using molecular data, although neither the significantly different (p. 238) results nor the Akaike score are given. (There is also a conceptual mistake there, in that the neutral hypothesis is stated as d13 - d23 = 0 instead of E[d13 - d23] = 0; see Figure 3.25 for a similar confusion.) Thus, I fail to see who would benefit from reading this chapter as a whole -- even though particular points are worthwhile contributions to the philosophy of testing. For instance, a biologist would most likely process the arguments and illustrations provided by Sober but could leave the chapter with a feeling of frustration at the apparent lack of conclusion. (As a statistician, I fail to understand how the likelihoods repeatedly mentioned by Sober can be computed because they never involve any parameters.)

Parsimony does not provide a justification for ignoring the data. (p. 250)

Since I believe that the Ockham's razor argument has had a global negative impact on the understanding of the parsimony requirement in testing,[5, 11] I find the warning signals about parsimony (given in the last third of the chapter) more palatable. Parsimony being an illdefined concept, especially from a statistical perspective (where even the dimension of the parameter space is debatable [12]), no model selection is acceptable if only based on this argument. Note further that parsimony is understood in two different ways in the book, one being connected to the Ockham's razor and the other leading to the specific phylogenetic parsimonious reconstruction (defined on p. 207 as the 'minimizing the total amount of evolution that must have occurred in the genetic tree', although I fail to understand the numerical illustration provided on the same page). In addition, Sober [10] makes a similar point in somehow more accessible (if non-statistical) terms.

Instead of evaluating hypotheses in terms of how probable they say the data are, we evaluate them by estimating how accurately they'll predict new data when fitted to old. (p. 229)

The chapter also addresses the distinction between hypothesis testing and model selection as paramount -- a point I subscribed to for a long while, before getting convinced of the opposite -- but I cannot get to the core of this argument. It seems that Sober sees model selection through the predictive performances of the models under comparison, if the above quote is representative of his thesis. (Overall, I find the style of the chapter slightly uneven, perhaps this is due to the fact that some sections, like Section 3.7, are simply adapted from earlier papers rather than having been completely rewritten for this publication.)

Statistically speaking, there is also a difficulty with the continuity assumption in this chapter. To be more precise, I note there is a long discussion about reaching the optimum configuration (for polar bear fur length) under the selection-plus-drift (SPD) hypothesis, but I think evolution happens in discontinuous moves. (Think, for instance, of changes in the number of chromosomes.) The case about the existence of a local minimum (Section 3.4) and the difficulty in moving from a local mode to a global mode is characteristic of this difficulty with the continuity assumption. For instance, a 'valley' on a 'fitness curve' that in essence takes three possible values over the three different types of eye design does not really constitute a bottleneck in the optimisation process. Similarly, the temporal structure of the statistical models in Sections 3.3 and 3.5 is never mentioned, even though it needs to be defined for the tests to take place. (For instance, in several places, time is mentioned without a clear definition. I have trouble in understanding how a finite time or even the original time, t = 0, can be assessed in such settings.) The past versus current convergence to stationarity or equilibrium -- and hence to optimality under the SPD hypothesis -- is an issue, as is the definition of time in the very simple 2 × 2 Markov chain example. And, given a 2 × 2 contingency table, such as

Table 1

 

fixed

polymorphic

synonymous

17

42

nonsynonymous

7

2

testing for independence between both factors is a standard among the standards: I thus fail to understand the lengthy and inconclusive discussion on pages 240 - 243. (The presentation of the 2 × 2 contingency tables in Figure 4.11 is fairly unusual, in that the position of the counts and the factor values are inverted.) Another statistical difficulty relates to the implicit use of plug-in estimates and to Sober's reluctance to adopt Bayesian arguments based on marginals. In the discussion on pages 255 - 256 about drawing inference on phylogenetic trees, the Markovian independence between branches of the trees, given the first-level ancestors, is confused with the impossibility of doing inference 'on ancestors that are "deeper"'. The independence between non--contiguous nodes of the tree only holds conditional on the intermediate nodes; it vanishes when integrating over the intermediate nodes.

Common or separate ancestry

Darwinians would not be satisfied if all life on Earth derived from the same large slab of rock. (p. 269)

The final chapter of the book (apart from the concluding summary) is about common ancestry and may be the most statistically orientated of the three last chapters. This is not to say that the chapter is without faults, including, in particular, a tendency to repeat the same arguments, but this is somehow the chapter that I appreciated the most. It starts with a detailed analysis of how the hypothesis of common ancestry should be set, the main distinction being between one organism and several, while pointing out the confusing effect of lateral gene transfer. Inference about phylogenetic trees and the use of genetic sequences rather than simplistic traits gets us closer to the true issues at stake. Another interesting feature of this chapter is the reference to Darwin's reflections on the common origin of life on Earth, through many quotes.

If those prior probabilities are obscure, the same will be true of the posterior probabilities. (p. 277)

Thus, the statistical issue is one of testing for a common ancestor versus separate ancestors for a set of organisms. The nature of the information contained in the data is never described precisely enough to understand whether this fits the principle of total evidence stressed throughout the book. The chapter also shows a more lenient disposition towards Bayesian solutions (relying on priors on p. 301) but Section 4.3 ends up with a damning statement, due to the impossibility of defining an objective prior because Sober wants prior probabilities that have some authority. This is a self-defeating constraint, leading to empirically well-grounded priors (p. 276).

Those propositions suffice for similarity to be evidence for common ancestry, and they have broad applicability. (p. 283)

The part about Reichenbach's [13] sufficient condition for a common trait to induce a likelihood ratio larger than one in favour of the common ancestor hypothesis needs to be discussed, as this is the point that I find the most puzzling in the chapter. Indeed, most of Reichenbach's nine assumptions connect both models under comparison, (ie common ancestry versus separate ancestry) by
Pr X = i | Z = j = Pr X = i | Z 1 = j , Pr Y = i | Z = j = Pr Y = i | Z 2 = j ,
and
Pr Z = j = Pr Z 1 = j = Pr Z 2 = j ,

where X and Y are the observed character traits for two species, and Z is the common ancestor trait, while Z1 and Z2 are the separate ancestor traits. These types of assumption are statistically and philosophically meaningless, in the sense that the models under comparison should not share any parameters. If the point is about determining which model is 'true', the 'wrong' model does not exist, there is no Z or (Z1, Z2), and hence the corresponding parameters do not have any substance either. For instance, when building a Bayesian model to compare single ancestor and separate ancestors models, there is a separate prior distribution on each group of parameters. The common parameter assumption is thus not compatible with selecting one of the two models. This unrealistic framework may be the result of a reluctance to handle true (ie unknown) parameters as happens in a regular statistical analysis (see, for example, the lament that 'until values for adjustable parameters are specified, we cannot talk about the probability of the data under different hypotheses'; p. 338). What is striking is the reliance of the whole chapter on this unnatural set of hypotheses, since it keeps resurfacing throughout the chapter. Sober writes that Propositions l - 9 are not consequences of the axioms of probability, nor are they necessary conditions for common ancestry to have a higher likelihood than separate ancestry (p. 283). Nonetheless, this is creating an unnecessary bias in the perception of the problem which may induce critics of evolution to reject the whole approach.

If there was no such common ancestor, what would alignment ever mean. (p. 29l)

The theme of the missing model that I have alluded to earlier in this review is also recurrent in this chapter. There are a lot of paragraphs about the choice of the representation of the differences between two species, from trait to gene sequence, and the author acknowledges that the difficulty in this choice has to do with a requirement for a more advanced theoretical representation (model) adapted to more complex data. This sounds rather obvious when stated that way, but the book wanders around this point for several pages. (An example is the above quote, which misses the point about sequence alignment; this is a perfectly welldefined measure of distance, common ancestor or not. An interesting discussion appears on page 29l about the bias induced by alignment, the conclusion being that 'aligning sequences is not loading the dice'. I think that alignment is akin to maximum likelihood plug--in and hence favours the null hypothesis. It should therefore be accounted for in the statistical procedure.) The overall conclusion is a vague call for the principle of total evidence (which is a rephrasing of the likelihood principle), after rightly dismissing the majority rule (p. 295). As illustrated by the section on multiple characters, the discussion is confusing without a proper model. It is only on page 300 that a completely defined model for the evolution of a dichotomous trait (ie the simplest possible case) appears. (A minor point of contention here is the use of bias for the Markovian model of chromosome transformation, where reversibility would have been more appropriate.) This model is a rather crude tool, as it depends on arbitrary calibration factors such as P(Z = 0) = 0.99 (instead of the absorbing 1) and, more importantly, on an unspecified time t (as in 'what time is it on the evolutionary clock?'). The corresponding likelihood ratio is then (under one of the selection schemes)
0 . 01 b t 2 + 0 . 99 0 . 01 b t + 0 . 99 2

where the dependence on those calibration factors is obvious. This illustrates the impossibility of reaching a satisfactory conclusion without first going through a statistical analysis of the problem.

Although this is not the purpose of the book, I think the debate about causality is rather superficial. For instance, while, in Section 3.6, causality and correlation are differentiated (see footnote 22 on p. 224 and p. 233), Section 3.8 embarks upon testing for a causal connection, discussing Reichenbach [13] without mentioning the Humean thesis of the logical and statistical impossibility of such a test. Most of Chapter 4 is about testing 'whether there was a common cause' (p. 247). A notion of information is mentioned on page 305 without being defined, and I do not understand whether or not this relates to Fisher's information [14] or to the Kullback divergence, as, apparently, no parameter is involved.

It is possible for data to discriminate among a set of hypotheses without saying anything about a proposition that is common to all the alternatives considered. (p. 3l5)

The debate about the phylogenetic tree reconstruction versus the test for common ancestry (Sections 4.7 and 4.8) lacks appeals for the very reason explained above. The tree structure may be incorporated within the model(s) and integrated out in a Bayesian fashion to provide the marginal likelihood of the model(s). Although this seems to be an important issue, as illustrated by the controversy with Templeton,[15, 16] the opposition between likelihood inference and 'cladistic' parsimony is not properly conducted, in that, as a naïve reader, I cannot understand Sober's presentation of the latter. This section is much more open to Bayesian processing by abstaining from the usual criticism about the lack of objectivity of the prior selection, but it entirely misses the ability of the Bayesian approach to integrate out the nuisance parameters, whether they are the tree topology (standard marginalisation) or the model index (model averaging). The debate about the limited meaning of statistical consistency makes the valid point that consistency only puts light on the case when the hypothesised model is true, but extended consistency could have been considered as well, namely that the procedure will bring the hypothesised model as close as possible to the 'true' model within the hypothesised family of models. What I gather from this final section is that cladistic parsimony tries to do without models (if not without assumptions), which seems to relate to Templeton's views about Bayesian inference.

This is the most enjoyable chapter of the book from my point of view, even though the lack of real illustrations makes it less potent than it could be. It also shows the limitation of a philosophical debate on simplistic idealisations of the real model. The book rarely acknowledges (see pp. 236 and 334) that genealogical hypotheses are composite. An incorporation of the parameter estimation in the inferential process would have improved the depth of the debate.

Conclusion

A quantitative assessment of goodness of fit is indispensable when evolutionary models are compared. (p. 362)

Evidence and Evolution is very well written, with few typographical errors. The style is sometimes too light, with an abundance of analogies that I regard as sidetracking, but this generally makes for easier reading. As I have described in this review, I have points of contention with the philosophical views about testing in the book, as well as with the methods described therein, but this does not detract from the appeal of reading the book. The lack of completely worked out statistical hypotheses in realistic settings remains my major criticism. While the author's criticisms of the Bayesian paradigm are often shallow (such as the one on p. 97, ridiculing Bayesians drawing inference based on a single observation), there is nothing fundamentally wrong with the statistical foundations of the book. I therefore repeat my recommendation of Evidence and Evolution, particularly Chapters 1 and (paradoxically) 5. Obviously, readers familiar with Sober's earlier papers and books will most likely find a huge overlap with, these, but others will appreciate Sober's viewpoints on the notion of testing hypotheses in a (mostly) unified perspective.

Authors’ Affiliations

(1)
Université Paris-Dauphine, CEREMADE, IUF and CREST

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Copyright

© Henry Stewart Publications 2011