Adaptiveness and adaptation

This essay is structured as follows. First, I describe the adaptationist program, or teleonomy, in biology. Second, I review the methodologies of this program. Third, I discuss the role that the environment of evolutionary adaptedness plays in the adaptationist program. Fourth, I argue that studies of the “adaptiveness” of human behavior have not been conceptually anchored in the adaptationist program. Fifth, I analyze two studies of adaptiveness and show why they neither test nor inspire novel hypotheses about the design of the human brain/mind. Finally, I conclude that the “adaptivist” approach to human behavior does not begin with well formed hypotheses about the design of human brain/mind mechanisms and that it consists of procedures that could not test such hypotheses if they were proposed.     

Psychological essentialism from first principles

Cognitive scientists have documented the existence of “essentialist” intuitions in humans: from a very early age, we assume that things have deep unobserved properties that make them what they are. I provide a sketch of an adaptationist explanation of psychological essentialism, arguing that these intuitions are the unsurprising output of adaptations for inductive inference. Variations on this insight have previously been used mostly as after-the-fact speculations, yet theories of adaptive function should ideally have a primary role in informing psychological research. Here I propose that viewing essentialist intuitions through an adaptationist lens has implications for some widespread assumptions about the phenomenon. Notably, researchers' focus on “higher-level” processes like categorization has led them to assume that essentialism is restricted to a few cognitive processes, but the ubiquity of inductive inference problems in cognition suggests otherwise. Additionally, because essentialist intuitions are the output of mechanisms solving related but distinct inference problems, it is unlikely that a single mechanistic theory can account for them all.     

The ‘Disadapted’ Animal: Niko Tinbergen on Human Nature and the Human Predicament

This paper explores ethologist Niko Tinbergen’s path from animal to human studies in the 1960s and 1970s and his views about human nature. It argues, first, that the confluence of several factors explains why Tinbergen decided to cross the animal/human divide in the mid 1960s: his concern about what he called “the human predicament,” his relations with British child psychiatrist John Bowlby, the success of ethological explanations of human behavior, and his professional and personal situation. It also argues that Tinbergen transferred his general adaptationist view of animal behavior to the realm of human biology; here, his concern about disadaptation led him to a view of human behavior that was strongly determined by the species’ evolutionary past, a position that I call evolutionary determinism. These ideas can be seen in the work he carried out with his wife, Elisabeth Tinbergen, on autism. The paper concludes that Tinbergen’s vision of human nature constitutes another version of what anthropologist Clifford Geertz called in 1966 the “stratigraphic” conception of the human: a view of human nature as a composite of levels in which a universal ancestral biological core is superimposed by psychological and cultural layers that represent accidental variation at best and pathological deviation at worst.     

The Creativity of Natural Selection? Part I: Darwin,Darwinism, and the Mutationists

This is the first of a two-part essay on the history of debates concerning the creativity of natural selection, from Darwin through the evolutionary synthesis and up to the present. Here I focus on the mid-late nineteenth century to the early twentieth, with special emphasis on early Darwinism and its critics, the self-styled “mutationists.” The second part focuses on the evolutionary synthesis and some of its critics, especially the “neutralists” and “neo-mutationists.” Like Stephen Gould, I consider the creativity of natural selection to be a key component of what has traditionally counted as “Darwinism.” I argue that the creativity of natural selection is best understood in terms of (1) selection initiating evolutionary change, and (2) selection being responsible for the presence of the variation it acts upon, for example by directing the course of variation. I consider the respects in which both of these claims sound non-Darwinian, even though they have long been understood by supporters and critics alike to be virtually constitutive of Darwinism.     

Evolutionary Psychology: The Burdens of Proof

I discuss two types of evidential problems with the most widely touted experiments in evolutionary psychology, those performed by Leda Cosmides and interpreted by Cosmides and John Tooby. First, and despite Cosmides and Tooby's claims to the contrary, these experiments don't fulfil the standards of evidence of evolutionary biology. Second Cosmides and Tooby claim to have performed a crucial experiment, and to have eliminated rival approaches. Though they claim that their results are consistent with their theory but contradictory to the leading non-evolutionary alternative, Pragmatic Reasoning Schemas theory, I argue that this claim is unsupported. In addition, some of Cosmides and Tooby's interpretations arise from misguided and simplistic understandings of evolutionary biology. While I endorse the incorporation of evolutionary approaches into psychology, I reject the claims of Cosmides and Tooby that a modular approach is the only one supported by evolutionary biology. Lewontin's critical examinations of the applications of adaptationist thinking provide a background of evidentiary standards against which to view the currently fashionable claims of evolutionary psychology.     

The Fate of the Method of ‘Paradigms’ in Paleobiology

An earlier article described the mid-twentieth century origins of the method of “paradigms” in paleobiology, as a way of making testable hypotheses about the functional morphology of extinct organisms. The present article describes the use of “paradigms” through the 1970s and, briefly, to the end of the century. After I had proposed the paradigm method to help interpret the ecological history of brachiopods, my students developed it in relation to that and other invertebrate phyla, notably in Euan Clarkson’s analysis of vision in trilobites. David Raup’s computer-aided “theoretical morphology” was then combined with my functional or adaptive emphasis, in Adolf Seilacher’s tripartite “constructional morphology.” Stephen Jay Gould, who had strongly endorsed the method, later switched to criticizing the “adaptationist program” he claimed it embodied. Although the explicit use of paradigms in paleobiology had declined by the end of the century, the method was tacitly subsumed into functional morphology as “biomechanics.”     

Rebuilding ships while at sea—Character individuality,homology, and evolutionary innovation

How novel traits originate in evolution is still one of the most perplexing questions in Evolutionary Biology. Building on a previous account of evolutionary innovation, I here propose that evolutionary novelties are those individualized characters that are not homologous to any characters in the ancestor. To clarify this definition, I here provide a detailed analysis of the concepts of “character individuality” and “homology” first, before addressing their role for our understanding of evolutionary innovation. I will argue (1) that functional as well as structural considerations are important for character individualization; and (2) that compositional (structural) and positional homology need to be clearly distinguished to properly describe the evolutionary transformations of hierarchically structured characters. My account will therefore integrate functional and structural perspectives and put forward a new multi-level view of character identity and transformation.     

The levels of analysis revisited

The term levels of analysis has been used in several ways: to distinguish between ultimate and proximate levels, to categorize different kinds of research questions and to differentiate levels of reductionism. Because questions regarding ultimate function and proximate mechanisms are logically distinct, I suggest that distinguishing between these two levels is the best use of the term. Integrating across levels in research has potential risks, but many benefits. Consideration at one level can help generate novel hypotheses at the other, define categories of behaviour and set criteria that must be addressed. Taking an adaptationist stance thus strengthens research on proximate mechanisms. Similarly, it is critical for researchers studying adaptation and function to have detailed knowledge of proximate mechanisms that may constrain or modulate evolutionary processes. Despite the benefits of integrating across ultimate and proximate levels, failure to clearly identify levels of analysis, and whether or not hypotheses are exclusive alternatives, can create false debates. Such non-alternative hypotheses may occur between or within levels, and are not limited to integrative approaches. In this review, I survey different uses of the term levels of analysis and the benefits of integration, and highlight examples of false debate within and between levels. The best integrative biology reciprocally uses ultimate and proximate hypotheses to generate a more complete understanding of behaviour.     

Engineering and evolvability

Comparing engineering to evolution typically involves adaptationist thinking, where well-designed artifacts are likened to well-adapted organisms, and the process of evolution is likened to the process of design. A quite different comparison is made when biologists focus on evolvability instead of adaptationism. Here, the idea is that complex integrated systems, whether evolved or engineered, share universal principles that affect the way they change over time. This shift from adaptationism to evolvability is a significant move for, as I argue, we can make sense of these universal principles without making any adaptationism claims. Furthermore, evolvability highlights important aspects of engineering that are ignored in the adaptationist debates. I introduce some novel engineering examples that incorporate these key neglected aspects, and use these examples to challenge some commonly cited contrasts between engineering and evolution, and to highlight some novel resemblances that have gone unnoticed.     

PHYLOGENETIC ANALYSES OF THE CORRELATED EVOLUTION OF CONTINUOUS CHARACTERS: A SIMULATION STUDY

We use computer simulation to compare the statistical properties of several methods that have been proposed for estimating the evolutionary correlation between two continuous traits, and define alternative evolutionary correlations that may be of interest. We focus on Felsenstein's (1985) method and some variations of it and on several “minimum evolution” methods (of which the procedure of Huey and Bennett [1987] is a special case), as compared with a nonphylogenetic correlation. The last, a simple correlation of trait values across the tips of a phylogeny, virtually always yields inflated Type I error rates, relatively low power, and relatively poor estimates of evolutionary correlations. We therefore cannot recommend its use. In contrast, Felsenstein's (1985) method yields acceptable significance tests, high power, and good estimates of what we term the input correlation and the standardized realized evolutionary correlation, given complete phylogenetic information and knowledge of the rate and mode of character change (e.g., gradual and proportional to time [“Brownian motion”] or punctuational, with change only at speciation events). Inaccurate branch length information may affect any method adversely, but only rarely does it cause Felsenstein's (1985) method to perform worse than do the others tested. Other proposed methods generally yield inflated Type I error rates and have lower power. However, certain minimum evolution methods (although not the specific procedure used by Huey and Bennett [1987]) often provide more accurate estimates of what we term the unstandardized realized evolutionary correlation, and their use is recommended when estimation of this correlation is desired. We also demonstrate how correct Type I error rates can be obtained for any method by reference to an empirical null distribution derived from computer simulations, and provide practical suggestions on choosing an analytical method, based both on the evolutionary correlation of interest and on the availability of branch lengths and knowledge of the model of evolutionary change appropriate for the characters being analyzed. Computer programs that implement the various methods and that will simulate (correlated) character evolution along a known phylogeny are available from the authors on request. These programs can be used to test the effectiveness of any new methods that might be proposed, and to check the generality of our conclusions with regard to other phylogenies.     

Explanatory pluralism in evolutionary biology

The ontological dependence of one domain on another is compatible with the explanatory autonomy of the less basic domain. That autonomy results from the fact that the relationship between two domains can be very complex. In this paper I distinguish two different types of complexity, two ways the relationship between domains can fail to be transparent, both of which are relevant to evolutionary biology. Sometimes high level explanations preserve a certain type of causal or counterfactual information which would be lost at the lower level; I argue that this is central to the proper understanding of the adaptationist program. Sometimes high level kinds are multiply realised by lower level kinds: I argue that this is central to the understanding of macroevolution.     

Rethinking the fast-slow continuum of individual differences

The idea that individual differences in behavior and physiology can be partly understood by linking them to a fast-slow continuum of life history strategies has become popular in the evolutionary behavioral sciences. I refer to this approach as the “fast-slow paradigm” of individual differences. The paradigm has generated a substantial amount of research, but has also come increasingly under scrutiny for theoretical, empirical, and methodological reasons. I start by reviewing the basic empirical facts about the fast-slow continuum across species and the main theoretical accounts of its existence. I then discuss the move from the level of species and populations to that of individuals, and the theoretical and empirical complications that follow. I argue that the fast-slow continuum can be a productive heuristic for individual differences; however, the field needs to update its theoretical assumptions, rethink some methodological practices, and explore new approaches and ideas in light of the specific features of the human ecology.     

Evo-devo and the search for homology (“sameness”) in biological systems

Developmental biology and evolutionary studies have merged into evolutionary developmental biology (“evo-devo”). This synthesis already influenced and still continues to change the conceptual framework of structural biology. One of the cornerstones of structural biology is the concept of homology. But the search for homology (“sameness”) of biological structures depends on our favourite perspectives (axioms, paradigms). Five levels of homology (“sameness”) can be identified in the literature, although they overlap to some degree: (i) serial homology (homonomy) within modular organisms, (ii) historical homology (synapomorphy), which is taken as the only acceptable homology by many biologists, (iii) underlying homology (i.e., parallelism) in closely related taxa, (iv) deep evolutionary homology due to the “same” master genes in distantly related phyla, and (v) molecular homology exclusively at gene level. The following essay gives emphasis on the heuristic advantages of seemingly opposing perspectives in structural biology, with examples mainly from comparative plant morphology. The organization of the plant body in the majority of angiosperms led to the recognition of the classical root–shoot model. In some lineages bauplan rules were transcended during evolution and development. This resulted in morphological misfits such as the Podostemaceae, peculiar eudicots adapted to submerged river rocks. Their transformed “roots” and “shoots” fit only to a limited degree into the classical model which is based on either–or thinking. It has to be widened into a continuum model by taking over elements of fuzzy logic and fractal geometry to accommodate for lineages such as the Podostemaceae.     

The proximate/ultimate distinction in the multiple careers of Ernst Mayr

Ernst Mayr's distinction between “ultimate” and “proximate” causes is justly considered a major contribution to philosophy of biology. But how did Mayr come to this “philosophical” distinction, and what role did it play in his earlier “scientific” work? I address these issues by dividing Mayr's work into three careers or phases: 1) Mayr the naturalist/researcher, 2) Mayr the representative of and spokesman for evolutionary biology and systematics, and more recently 3) Mayr the historian and philosopher of biology. If we want to understand the role of the proximate/ultimate distinction in Mayr's more recent career as a philosopher and historian, then it helps to consider hisearlier use of the distinction, in the course of his research, and in his promotion of the professions of evolutionary biology and systematics. I believe that this approach would also shed light on some other important “philosophical” positions that Mayr has defended, including the distinction between “essentialism: and “population thinking.”     

Historical and philosophical perspectives on the study of developmental bias

Throughout the recent history of research at the intersection of evolution and development, notions such as developmental constraint, evolutionary novelty, and evolvability have been prominent, but the term “developmental bias” has scarcely been used. And one may even doubt whether a unique and principled definition of bias is possible. I argue that the concept of developmental bias can still play a vital scientific role by means of setting an explanatory agenda that motivates investigation and guides the formulation of integrative explanatory frameworks. Less crucial is a definition that would classify patterns of phenotypic variation and unify variational patterns involving different traits and taxa as all being “bias.” Instead, what we should want is a concept that generates intellectual identity across various researchers, and that unites the diverse fields and approaches relevant to the study of developmental bias, from paleontology to behavioral biology. I point to some advantages of conducting research specifically under the label of “developmental bias,” compared with employing other, more common terms such as “evolvability.”     

Possible atavisms of genitalia in two species of earwig (Dermaptera), Proreus simulans (Chelisochidae) and Euborellia plebeja (Anisolabididae)

Male and female genitalia generally show a rapid evolutionary rate, which raises the problems related to homologization and the determination of the polarities of evolutionary changes. In earwigs (Dermaptera), multiple or branched female sperm-storage organs (spermathecae) have been reported for members of the Karschiellidae, Pygidicranidae, and Diplatyidae, collectively termed the “basal” Dermaptera. Whether the complicated spermathecae represent a plesiomorphy or an apomorphy has not been resolved. Here I report the occurrence of multiple or branched spermathecae in gamma-irradiated samples of two earwig species, Euborellia plebeja (Dohrn, 1863) (Anisolabididae) and Proreus simulans (Stål, 1860) (Chelisochidae), which belong to the “higher” Dermaptera (Apachyidae, Labiduridae, Anisolabididae, Spongiphoridae, Chelisochidae, and Forficulidae). Females belonging to the higher Dermaptera normally have a single-unbranched spermatheca. I discuss examples of possible atavisms in relation to the evolutionary pathways of spermathecal morphology. Possible atavisms in the number of male organs for sperm transfer (virgae) are also reported.     

Is tibetan polyandry adaptive?

This paper addresses methodological and metatheoretical aspects of the ongoing debate over the adaptive significance of Tibetan polyandry. Methodological contributions include a means of estimating relatedness of fraternal co-husbands given multigenerational polyandry, and use of Hamilton’s rule and a member-joiner model to specify how inclusive fitness gains of co-husbands may vary according to seniority, opportunity costs, and group size. These methods are applied to various data sets, particularly that of Crook and Crook (1988). The metatheoretical discussion pivots on the critique by evolutionary psychologists of adaptationist accounts of polyandry. Contrary to this critique, I argue that valid adaptationist explanations of such practices do not necessitate cognitive mechanisms evolved specifically to produce polyandry, nor that there must have been exact equivalents of Tibetan agricultural estates and social institutions in human evolutionary history. Specific issues raised when one posits either kin selection or cultural evolution to explain the adaptive features of Tibetan polyandry are also discussed.     

THE EVOLUTION OF REPRODUCTIVE EFFORT IN LIZARDS AND SNAKES

Life history theory suggests that the optimal evolved level of reproductive effort (RE) for an organism depends upon the degree to which additional current reproductive investment reduces future reproductive output. Future reproduction can be decreased in two ways, through (i) decreases in the organism's survival rate, and/or (ii) decreases in the organism's growth (and hence subsequent fecundity). The latter tradeoff–that is, the “potential fecundity cost”—should affect the evolution of RE only in species with relatively high survival rate, a relatively high rate of fecundity increase with body size, or a relatively high reproductive frequency per annum. Unless these conditions are met, the probable benefit in future fecundity obtained from decreasing present reproductive output is too low for natural selection to favor any reduction in RE below the maximum physiologically possible. Published data on survival rate, reproductive frequency and relative clutch mass (RCM) suggest that many lizard species fall well below the level at which natural selection can be expected to influence RE through such “potential fecundity” tradeoffs. Hence, the relative allocation of resources between growth and reproduction is unlikely to be directly optimized by natural selection in these animals. Instead, energy allocation should influence the evolution of RE only indirectly, via effects on an organism's probability of survival during reproduction. Survival costs of reproduction may be the most important evolutionary determinants of RE in many reptiles, and information on the nature and extent of such costs is needed before valid measures of reptilian RE can be constructed.     

Constraining the adaptationism debate

This contribution to the adaptationism debate elaborates the nature of constraints and their importance in evolutionary explanation and argues that the adaptationism debate should be limited to the issue of how to privilege causes in evolutionary explanation. I argue that adaptationist explanations are deeply conceptually dependent on developmental constraints, and explanations that appeal to constraints are dependant on the results of natural selection. I suggest these explanations should be integrated into the framework of historical causal explanation. Each strategy explicitly appeals to some aspect of the evolutionary process, while implicitly appealing to others. Thus, adaptationists and anti-adaptationists can offer complementary causal explanations of the same explanandum. This eliminates much of the adaptationism debate and explains why its adversaries regularly agree with each other more than they would like. The adaptationism issue that remains is a species of the general issue of how to privilege causes in explanation. I show how a proposed solution to this general problem might be brought to bear on evolutionary explanations, and investigate some difficulties that might arise due to the nature of the evolutionary process.     

What is a phenotype? History and new developments of the concept

Even though the word “phenotype”, as well as the expression “genotype–phenotype relationship”, are a part of the everyday language of biologists, they remain abstract notions that are sometimes misunderstood or misused. In this article, I begin with a review of  the genesis of the concept of phenotype and of the meaning of the genotype-phenotype “relationship" from a historical perspective. I then illustrate how the development of new approaches for exploring the living world has enabled us to phenotype organisms at multiple levels, with traits that can either be measures or parameters of functions, leading to a virtually unlimited amount of phenotypic data. Thus, pleiotropy becomes a central issue in the study of the genotype–phenotype relationship. Finally, I provide a few examples showing that important genetic and evolutionary features clearly differ with the phenotypic level considered. The way genotypic variation propagates across the phenotypic levels to shape fitness variation is an essential research program in biology.