My best papers: Biology, part II (2000-2009)

by Massimo Pigliucci

This is the second installment (you can find the first one here) of my favorite technical papers, selected among those I published during my first academic career, as an evolutionary biologist. The period covered below goes from 2000 to 2009 (though some papers were published afterwards), when I was a faculty at Stony Brook University. After that, I switched to full time philosophy, but I may need to wait a few years before having a sufficient publication record in that field to be able to pick favorites... If you’d like full e-reprint of any of the papers below (or those from the previous installment), just drop me an email. The full list of my publications is here.

The fall and rise of Dr Pangloss: adaptationism and the Spandrels paper 20 years later (with J. Kaplan, Trends in Ecology and Evolution, 2000).

Twenty years have passed since Gould and Lewontin published their critique of ‘the adaptationist program’ – the tendency of some evolutionary biologists to assume, rather than demonstrate, the operation of natural selection. After the ‘Spandrels paper’, evolutionists were more careful about producing just-so stories based on selection, and paid more attention to a panoply of other processes. Then came reactions against the excesses of the anti-adaptationist movement, which ranged from a complete dismissal of Gould and Lewontin’s contribution to a positive call to overcome the problems. We now have an excellent opportunity for finally affirming a more balanced and pluralistic approach to the study of evolutionary biology.

Are ecology and evolutionary biology “soft” sciences? (Annales Zoologici Finnici, 2002).

Research in ecology and evolutionary biology (evo-eco) often tries to emulate the “hard” sciences such as physics and chemistry, but to many of its practitioners feels more like the “soft” sciences of psychology and sociology. I argue that this schizophrenic attitude is the result of lack of appreciation of the full consequences of the peculiarity of the evo-eco sciences as lying in between a-historical disciplines such as physics and completely historical ones as like paleontology. Furthermore, evo-eco researchers have gotten stuck on mathematically appealing but philosophically simplistic concepts such as null hypotheses and p-values defined according to the frequentist approach in statistics, with the consequence of having been unable to fully embrace the complexity and subtlety of the problems with which ecologists and evolutionary biologists deal with. I review and discuss some literature in ecology, philosophy of science and psychology to show that a more critical methodological attitude can be liberating for the evo-eco scientist and can lead to a more fecund and enjoyable practice of ecology and evolutionary biology. With this aim, I briefly cover concepts such as the method of multiple hypotheses, Bayesian analysis, and strong inference.

Evolution of phenotypic integration in Brassica (Brassicaceae) (with C.J. Murren and N. Pendleton, American Journal of Botany, 2002).

Phenotypic integration is a necessary characteristic of living organisms that results from genetic, developmental, and functional relationships among traits. The nature of these relationships can be influenced by the environment. We examined patterns of phenotypic integration of six species of rapid cycling Brassica and of Raphanus sativus within a phylogenetic context. Specifically, we tested the hypothesis that hybrid species show intermediate levels of integration in morphological and life-history characters compared to their putative parentals. We used matrix correlation tests to examine if cytogenetic relationships or ecological similarities among species partially explained the patterns of phenotypic integration. There was a significant negative relationship between the ecological and cytogenetic matrices, suggesting that more closely related species were ecologically dissimilar. However, neither ecological nor cyto- genetic matrices significantly explained differences among species in the pattern of their phenotypic correlations. Set correlation analysis indicated that important traits within the modules and the strength of the correlations within modules differed across species. We also found that there were a greater number of significant correlations between modules than within modules. Hybrid species were more integrated (had greater number of significant trait correlations) than either of their parents, both within and between modules. However, univariate analyses of character means of the hybrid species were not significantly different from the combined mean of their putative parents for 5, 6, or 7 of the 11 phenotypic characters (for Brassica napus, B. juncea and B. carinata, respectively); for the remaining characters, the hybrids were more similar to one of the parents.

Shade-induced plasticity and its ecological significance in wild populations of Arabidopsis thaliana (with C. Callahan, Ecology, 2002).

In laboratory studies of Arabidopsis thaliana, plants shaded by neighboring vegetation (or subject to treatments mimicking shade) flower at a younger developmental stage, and sometimes earlier in time. We examined whether this shade avoidance response varies among and within natural populations of A. thaliana, and whether it corresponds to variable selection regimes at shaded and unshaded field sites, by conducting a two-year reciprocal transplant study and a parallel greenhouse study that manipulated the presence and timing of shade. In the field, shading had limited or inconsistent impacts on survivorship across several phases of the growing season. The date of bolting was earlier at the shadier site compared to the less shady site, but in the greenhouse there was no significant shade- induced plasticity for this trait. In both studies, we detected directional selection gradients favoring earlier bolting in shade, but gradients favoring earlier bolting were as strong in nonshaded conditions. The number of rosette leaves at bolting (i.e., the developmental stage of flowering) was significantly reduced by shade in both studies. However, there was either no directional selection on this trait, or selection to flower with more rather than fewer leaves. Despite the contrast in habitats, there was limited differentiation between populations for survivorship, reproductive fitness, size-related or flowering time traits, and no differ- entiation for trait plasticities. Some traits were variable among families within populations. A trade-off between age and developmental stage may limit the response to selection for flowering time, possibly explaining limited local adaptation. The adaptive significance of shade-induced flowering time plasticity remains equivocal. Future studies of the plasticity of flowering time in A. thaliana should investigate the effects of shading regimes together with other environmental variables on size- and timing-related traits.

Comparative Studies of Evolutionary Responses to Light Environments in Arabidopsis (with H. Pollard and M.B. Cruzan, American Naturalist, 2003).

In this article, we compare the reaction norms to foliage shade (changes in light quality, spatially fine-grained environmental variation) and photoperiod (day length, spatially coarse-grained environmental variation) in several haplotypes of Arabidopsis thaliana from Scandinavia. We found that both across-environment means and phenotypic plasticities evolved continuously and very rapidly within this group. Both character means and trait plasticities were highly integrated, in part as predicted by the adaptive plasticity hypothesis for response to foliage shade (the so-called shade-avoidance syndrome). We found that a significant but small fraction of the variance in across-treatment trait means and plasticities in response to one environmental factor is explained by variation of the same traits in response to the other factor. Genetic relatedness based on chloroplast DNA sequence variation among haplotypes was not associated with variation in across-treatment character means or their plasticities, suggesting that evolution of these characters has occurred on a local geographic scale via reticulation (outcrossing) among maternal lines rather than by the differential survival of selfing lineages.

Genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? (with C.J. Murren, Evolution, 2003).

The idea of genetic assimilation, that environmentally induced phenotypes may become genetically fixed and no longer require the original environmental stimulus, has had varied success through time in evolutionary biology research. Proposed by Waddington in the 1940s, it became an area of active empirical research mostly thanks to the efforts of its inventor and his collaborators. It was then attacked as of minor importance during the ‘‘hardening’’ of the neo-Darwinian synthesis and was relegated to a secondary role for decades. Recently, several papers have appeared, mostly independently of each other, to explore the likelihood of genetic assimilation as a biological phenomenon and its potential importance to our understanding of evolution. In this article we briefly trace the history of the concept and then discuss theoretical models that have newly employed genetic assimilation in a variety of contexts. We propose a typical scenario of evolution of genetic assimilation via an intermediate stage of phenotypic plasticity and present potential examples of the same. We also discuss a conceptual map of current and future lines of research aimed at exploring the actual relevance of genetic assimilation for evolutionary biology.

Phenotypic integration: studying the ecology and evolution of complex phenotypes (Ecology Letters, 2003).

Phenotypic integration refers to the study of complex patterns of covariation among functionally related traits in a given organism. It has been investigated throughout the 20th century, but has only recently risen to the forefront of evolutionary ecological research. In this essay, I identify the reasons for this late flourishing of studies on integration, and discuss some of the major areas of current endeavour: the interplay of adaptation and constraints, the genetic and molecular bases of integration, the role of phenotypic plasticity, macroevolutionary studies of integration, and statistical and conceptual issues in the study of the evolution of complex phenotypes. I then conclude with a brief discussion of what I see as the major future directions of research on phenotypic integration and how they relate to our more general quest for the understanding of phenotypic evolution within the neo-Darwinian framework. I suggest that studying integration provides a particularly stimulating and truly interdisciplinary convergence of researchers from fields as disparate as molecular genetics, developmental biology, evolutionary ecology, palaeontology and even philosophy of science.

Selection in a model system: ecological genetics of flowering time in Arabidopsis thaliana (Ecology, 2003).

Arabidopsis thaliana and some of its close allies have been a model system for genetics, developmental biology, and molecular biology for some time. More recently, they have been adopted by an increasing number of laboratories involved in evolutionary ecological research. In this paper, I illustrate some of the methods and advantages concerning the use of Arabidopsis to study selection and the constraints imposed on it by the genetic architecture underlying morphological and life history traits. Populations of A. thaliana and closely related species show a wider ecological variance than had been suspected, and it is increasingly clear that even such a relatively simple organism presents endless challenges to ecologists and evolutionary biologists. The study of the evolution of life history traits in this group also provides us with an invaluable opportunity to advance our search for ways to integrate biological knowledge at the organismal and molecular levels. At the same time, these efforts also yield a better understanding of the type of research that can be carried out independently at these two levels of the biological hierarchy.

Species as family resemblance concepts: the (dis-)solution of the species problem? (BioEssays, 2003).

The so-called ‘‘species problem’’ has plagued evolution- ary biology since before Darwin’s publication of the aptly titled Origin of Species. Many biologists think the problem is just a matter of semantics; others complain that it will not be solved until we have more empirical data. Yet, we don’t seem to be able to escape discussing it and teaching seminars about it. In this paper, I briefly examine the main themes of the biological and philosophical literatures on the species problem, focusing on identifying common threads as well as relevant differences. I then argue two fundamental points. First, the species problem is not primarily an empirical one, but it is rather fraught with philosophical questions that require—but cannot be settled by—empirical evidence. Second, the (dis-)solution lies in explicitly adopting Wittgenstein’s idea of ‘‘family resemblance’’ or cluster concepts, and to consider spe- cies as an example of such concepts. This solution has several attractive features, including bringing together apparently diverging themes of discussion among bio- logists and philosophers. The current proposal is conceptually independent (though not incompatible) with the pluralist approach to the species problem advocated by Mishler, Donoghue, Kitcher and Dupre ́, which implies that distinct aspects of the species question need to be emphasized depending on the goals of the researcher. From the biological literature, the concept of species that most closely matches the philosophical discussion presented here is Templeton’s cohesion idea.

Evolution of phenotypic plasticity: where are we going now? (Trends in Ecology & Evolution, 2005).

The study of phenotypic plasticity has progressed significantly over the past few decades. We have moved from variation for plasticity being considered as a nuisance in evolutionary studies to it being the primary target of investigations that use an array of methods, including quantitative and molecular genetics, as well as of several approaches that model the evolution of plastic responses. Here, I consider some of the major aspects of research on phenotypic plasticity, assessing where progress has been made and where additional effort is required. I suggest that some areas of research, such the study of the quantitative genetic underpinning of plasticity, have been either settled in broad outline or superseded by new approaches and questions. Other issues, such as the costs of plasticity are currently at the forefront of research in this field, and are likely to be areas of major future development.

Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions (with C.L. Richards, O. Bossdorf, N.Z. Muth and J. Gurevitch, Ecology Letters, 2006).

Invasion biologists often suggest that phenotypic plasticity plays an important role in successful plant invasions. Assuming that plasticity enhances ecological niche breadth and therefore confers a fitness advantage, recent studies have posed two main hypotheses: (1) invasive species are more plastic than non-invasive or native ones; (2) populations in the introduced range of an invasive species have evolved greater plasticity than populations in the native range. These two hypotheses largely reflect the disparate interests of ecologists and evolutionary biologists. Because these sciences are typically interested in different temporal and spatial scales, we describe what is required to assess phenotypic plasticity at different levels. We explore the inevitable tradeoffs of experiments conducted at the genotype vs. species level, outline components of experimental design required to identify plasticity at different levels, and review some examples from the recent literature. Moreover, we suggest that a successful invader may benefit from plasticity as either (1) a Jack-of-all-trades, better able to maintain fitness in unfavourable environments; (2) a Master-of-some, better able to increase fitness in favourable environments; or (3) a Jack-and-master that combines some level of both abilities. This new framework can be applied when testing both ecological or evolutionary oriented hypotheses, and therefore promises to bridge the gap between the two perspectives.

Do we need an extended evolutionary synthesis? (Evolution, 2007).

The Modern Synthesis (MS) is the current paradigm in evolutionary biology. It was actually built by expanding on the conceptual foundations laid out by its predecessors, Darwinism and neo-Darwinism. For sometime now there has been talk of a new Extended Evolutionary Synthesis (EES), and this article begins to outline why we may need such an extension, and how it may come about. As philosopher Karl Popper has noticed, the current evolutionary theory is a theory of genes, and we still lack a theory of forms. The field began, in fact, as a theory of forms in Darwin’s days, and the major goal that an EES will aim for is a unification of our theories of genes and of forms. This may be achieved through an organic grafting of novel concepts onto the foundational structure of the MS, particularly evolvability, phenotypic plasticity, epigenetic inheritance, complexity theory, and the theory of evolution in highly dimensional adaptive landscapes.

Finding the way in phenotypic space: the origin and maintenance of constraints on organismal form (American Journal of Botany, 2007).

One of the all-time questions in evolutionary biology regards the evolution of organismal shapes, and in particular why certain forms appear repeatedly in the history of life, others only seldom and still others not at all. Recent research in this field has deployed the conceptual framework of constraints and natural selection as measured by quantitative genetic methods. In this paper I argue that quantitative genetics can by necessity only provide us with useful statistical summaries that may lead researchers to formulate testable causal hypotheses, but that any inferential attempt beyond this is unreasonable. Instead, I suggest that thinking in terms of coordinates in phenotypic spaces, and approaching the problem using a variety of empirical methods (seeking a consilience of evidence), is more likely to lead to solid inferences regarding the causal basis of the historical patterns that make up most of the data available on phenotypic evolution.

Epigenetics for ecologists (with O. Bossdorf and C.L. Richards, Ecology Letters, 2008).

There is now mounting evidence that heritable variation in ecologically relevant traits can be generated through a suite of epigenetic mechanisms, even in the absence of genetic variation. Moreover, recent studies indicate that epigenetic variation in natural populations can be independent from genetic variation, and that in some cases environmentally induced epigenetic changes may be inherited by future generations. These novel findings are potentially highly relevant to ecologists because they could significantly improve our understanding of the mechanisms underlying natural phenotypic variation and the responses of organisms to environmental change. To understand the full significance of epigenetic processes, however, it is imperative to study them in an ecological context. Ecologists should therefore start using a combination of experimental approaches borrowed from ecological genetics, novel techniques to analyse and manipulate epigenetic variation, and genomic tools, to investigate the extent and structure of epigenetic variation within and among natural populations, as well as the interrelations between epigenetic variation, phenotypic variation and ecological interactions.

Is evolvability evolvable? (Nature Reviews Genetics, 2008).

In recent years, biologists have increasingly been asking whether the ability to evolve — the evolvability — of biological systems, itself evolves, and whether this phenomenon is the result of natural selection or a by-product of other evolutionary processes. The concept of evolvability, and the increasing theoretical and empirical literature that refers to it, may constitute one of several pillars on which an extended evolutionary synthesis will take shape during the next few years, although much work remains to be done on how evolvability comes about.

The proper role of population genetics in modern evolutionary theory (Biological Theory, 2008).

Evolutionary biology is a field currently animated by much discussion concerning its conceptual foundations. On the one hand, we have supporters of a classical view of evolutionary theory, whose backbone is provided by population genetics and the so-called Modern Synthesis (MS). On the other hand, a number of researchers are calling for an Extended Synthesis (ES) that takes seriously both the limitations of the MS (such as its inability to incorporate developmental biology) and recent empirical and theoretical research on issues such as evolvability, modularity, and self-organization. In this article, I engage in an in-depth commentary of an influential paper by population geneticist Michael Lynch, which I take to be the best defense of the MS-population genetics position published so far. I show why I think that Lynch’s arguments are wanting and propose a modification of evolutionary theory that retains but greatly expands on population genetics.

A comprehensive test of the ‘limiting resources’ framework applied to plant tolerance to apical meristem damage (with J.A. Banta and M.H.H. Stevens, Oikos, 2010).

Tolerance to apical meristem damage (AMD) is a form of plant defense against herbivory. Theoretical models come to different conclusions about the effects of inorganic soil nutrient levels on tolerance to AMD, and different plants have shown different relationships between these variables. To assign some order to these disparate patterns and to resolve conflicts among the models, the ‘limiting resources model’ (LRM) was developed. However, we believe that the LRM is actually comprised of several different models, which we describe. Our study marks the first comprehensive and simultaneous test of the entire LRM framework, treating it explicitly as separate models, which also evaluates the models’ underlying assumptions. We studied tolerance to AMD in laboratory-reared natural populations of Arabidopsis thaliana from three different regions of Europe, spanning a wide latitudinal gradient. We show that, in different populations of this species, basic responses to nutrients and damage are best described by different models, which are based on different assumptions and make different predictions. This demonstrates the need for complexity in our explanations, and suggests that no one existing model can account for all relationships between tolerance to AMD and nutrients. Our results also demonstrate that fruit production can provide a misleading approximation of fitness in A. thaliana, contrary to the common assumption in the literature.

Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana (with O. Bossdorf, D. Arcuri and C.L. Richards, Evolutionary Ecology, 2010).

Heritable phenotypic variation in plants can be caused not only by underlying genetic differences, but also by variation in epigenetic modifications such as DNA methylation. However, we still know very little about how relevant such epigenetic variation is to the ecology and evolution of natural populations. We conducted a greenhouse experiment in which we treated a set of natural genotypes of Arabidopsis thaliana with the demethylating agent 5-azacytidine and examined the consequences of this treatment for plant traits and their phenotypic plasticity. Experimental demethylation strongly reduced the growth and fitness of plants and delayed their flowering, but the degree of this response varied significantly among genotypes. Differences in genotypes’ responses to demethylation were only weakly related to their genetic relatedness, which is consistent with the idea that natural epigenetic variation is independent of genetic variation. Demethylation also altered patterns of phenotypic plasticity, as well as the amount of phenotypic variation observed among plant individuals and genotype means. We have demonstrated that epigenetic variation can have a dramatic impact on ecologically important plant traits and their variability, as well as on the fitness of plants and their ecological interactions. Epigenetic variation may thus be an overlooked factor in the evolutionary ecology of plant populations.

Selection dynamics in native and introduced Persicaria species (with K.L. O’Donnell, International Journal of Plant Science, 2010).

Plant invasions represent natural experiments that allow us to both explore the dynamics of natural selection in the wild and examine the evolution of an invader on contemporary timescales. We conducted a study of 10 natural populations of two invasive species (Persicaria lapathifolia and Persicaria cespitosa) and one native species (Persicaria pensylvanica) to quantify the amount of natural selection acting on these species to compare the selection dynamics to which each is exposed. We also conducted a germination trial to compare the potential for invasion determined by germination rate. A Lande-Arnold-style multiple regression selection analysis was performed on five morphological traits (height, stem diameter, leaf number, leaf shape, and leaf area) using flower number as our fitness proxy. Most selection was indirect and caused by correlations with other traits under selection. However, there was significant direct selection for increased leaf number in both natives and invasives and for thicker stems in just the invasives. The germination test showed that not only do the invasive plants have a significantly higher germination rate (>60% compared with 3% for the noninvasives) but they also germinate significantly faster; both findings have large implications for the ability of these two invasive species to spread.

Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation (with C.L. Richards and A.W. Schrey, Ecology Letters, 2012).

The expansion of invasive species challenges our understanding of the process of adaptation. Given that the invasion process often entails population bottlenecks, it is surprising that many invasives appear to thrive even with low levels of sequence-based genetic variation. Using Amplified Fragment Length Poly- morphism (AFLP) and methylation sensitive-AFLP (MS-AFLP) markers, we tested the hypothesis that differentiation of invasive Japanese knotweed in response to new habitats is more correlated with epigenetic variation than DNA sequence variation. We found that the relatively little genetic variation present was differentiated among species, with less differentiation among sites within species. In contrast, we found a great deal of epigenetic differentiation among sites within each species and evidence that some epigenetic loci may respond to local microhabitat conditions. Our findings indicate that epigenetic effects could con- tribute to phenotypic variation in genetically depauperate invasive populations. Deciphering whether differences in methylation patterns are the cause or effect of habitat differentiation will require manipulative studies.

On the different ways of ‘‘doing theory’’ in biology (Biological Theory, 2012).

‘‘Theoretical biology’’ is a surprisingly heterogeneous field, partly because it encompasses ‘‘doing theory’’ across disciplines as diverse as molecular biology, systematics, ecology, and evolutionary biology. Moreover, it is done in a stunning variety of different ways, using anything from formal analytical models to computer simulations, from graphic representations to verbal arguments. In this essay I survey a number of aspects of what it means to do theoretical biology, and how they compare with the allegedly much more restricted sense of theory in the physical sciences. I also tackle a recent trend toward the presentation of all-encompassing theories in the biological sciences, from general theories of ecology to a recent attempt to provide a conceptual framework for the entire set of biological disciplines. Finally, I discuss the roles played by philosophers of science in criticizing and shaping biological theorizing.

My best papers: Biology, part I (1993-1999)

by Massimo Pigliucci

So, I'm about to reach half a century of existence on this planet. An arbitrary threshold, for sure, but one that nonetheless has some psychological resonance for most human beings. In order to mark the occasion, therefore, I decided to post summaries of what I think are the most interesting technical papers I published so far (if you are actually interested in the details, feel free to drop me an email and I'll send you the full pdf; the full list of my publications is here). I welcome comments on any or all of the subject matters touched therein. I am beginning with my first academic career, in biology (I may get to my philosophical output in a few more years, it’s too short right now). You'll notice that the majority of the entries below are about conceptual, rather than empirical, papers. That's for three reasons: i) they are more likely to be of interest to a general readership; ii) they reflect my own intellectual trend, which eventually led me full time to philosophy; iii) empirical papers tend to make very local contributions to the edifice of knowledge, unless they are about spectacular discoveries (e.g., the structure of DNA, the Higgs boson), and alas mine don't fall into that category. Still, you will see examples of my empirical work nonetheless. Entries are in chronological order, this first installment basically covering the period from my PhD at the University of Connecticut (which I began in 1990) to my postdoc at Brown. Enjoy, I hope.

Control of phenotypic plasticity via regulatory genes (with C.D. Schlichting, American Naturalist, 1993).

There is no formal abstract for this, which was not a full paper, but a note in response to a provocative paper by Sara Via (notice the pun in the title of our paper...). Via was arguing that so-called phenotypic plasticity (i.e., the property of a genotype to produce different phenotypes in response to different environments) is in some sense not a real biological phenomenon, but rather a byproduct of natural selection within distinct environments. My then PhD advisor and I responded that there were clear cases were Via's scenario simply did not account for the data, i.e. true cases of selection favoring directly the ability of an organism to respond flexibly to heterogeneous environments.

Gene regulation, quantitative genetics and the evolution of reaction norms (with C.D. Schlichting, Evolutionary Ecology, 1995).

The ideas of phenotypic plasticity and of reaction norm are gaining prominence as important components of theories of phenotypic evolution. Our understanding of the role of phenotypic plasticity as an adaptation of organisms to variable environments will depend on (1) the form(s) of genetic and developmental control exerted on the shape of the reaction norm and (2) the nature of the constraints on the possible evolutionary trajectories in multiple environments. In this paper we identify two categories of genetic control of plasticity: allelic sensitivity and gene regulation. These correspond generally to two classes of response by the developmental system to environmental change: phenotypic modulation, in which plastic responses are a continuous and proportional function of environmental stimuli and developmental conversion, where responses tend to be not simply proportional to the stimuli. We propose that control of plasticity by regulatory actions has distinct advantages over simple allelic sensitivity: stability of phenotypic expression, capacity for anticipatory response and relaxation of constraints due to genetic correlations. We cite examples of the extensive molecular evidence for the existence of environmentally-cued gene regulation leading to developmental conversion. The results of quantitative genetic investigations on the genetics and evolution of plasticity, as well as the limits of current approaches are discussed. We suggest that evolution of reaction norms would be affected by the ecological context (i.e. spatial versus temporal variation, hard versus soft selection, and fine versus coarse environmental grain). We conclude by discussing some empirical approaches to address fundamental questions about plasticity evolution.

Lost in Phenotypic Space: Environment-Dependent Morphology in Phlox drummondii (Polemoniaceae) (with C.D. Schlichting, International Journal of Plant Sciences, 1995).

Two questions on the multivariate relationships among traits and their plastic responses were analyzed in an experiment on the phenotypic plasticity of plants from seven natural populations of Phlox drummondii from Texas to five greenhouse environments. (1) Do different environmental stresses (herbivory, low nutrients, small pot, and low water) result in similar changes among suites of traits? (2) Are the differences in plastic responses among populations large enough to alter their phenetic interrelationships? Our results indicate that the responses of plants to macroenvironmental variables are specific to that environment, evoking not only quantitative (size) but also qualitative (shape and allocation) phenotypic differences. Further, the overall phenetic similarity among populations changes radically depending upon the environment in which they are compared; i.e., apparent phenetic relationships vary with the treatment. These results demonstrate both trait- and environmental-specificity of plastic responses, leading to the production of distinct whole-plant phenotypes in different environments.

Reaction norms of Arabidopsis. I. Plasticity of characters and correlations across water, nutrient and light gradients (with J. Whitton and C.D. Schlichting, Journal of Evolutionary Biology, 1995).

The univariate and multivariate study of variation for phenotypic plasticity is central to providing a clear understanding of hypotheses about the genetic control and evolution of reaction norms in natural populations. Arabidopsis thaliana is an ideal organism for the study of Genotype × Environment interactions (i.e., genetic variation for plasticity), because of the ease with which it can be grown in large numbers and due to the amount of information already available on its genetics, physiology and developmental biology. In this paper, we report on the plasticity, genetic variation and G×E interactions of four populations of A. thaliana in response to three environmental gradients (water, light and nutrients), each characterized by four levels of the controlled parameter. We measured nine traits and obtained their reaction norms. Path analysis was used to study the plasticity of character correlations. We found a tendency for A. thaliana reaction norms to be linear (either flat, i.e. no plasticity, or with a significant slope), in accordance with previous studies. We detected substantial amounts of genetic variation for plasticity in the light and nutrient gradients, but not in the water gradient. Dramatic restructuring of character correlations was induced by changes in environmental conditions, although some paths tended to be stable irrespective of the environment, thereby suggesting some degree of canalization.

Developmental Reaction Norms: the Interactions among Allometry, Ontogeny and Plasticity (with C.D. Schlichting, C.S. Jones and K. Schwenk, Plant Species Biology, 1996).

How micro- and macroevolutionary evolutionary processes produce phenotypic change is without question one of the most intriguing and perplexing issues facing evolutionary biologists. We believe that roadblocks to progress lie A) in the underestimation of the role of the environment, and in particular, that of the interaction of genotypes with environmental factors, and B) in the continuing lack of incorporation of development into the evolutionary synthesis. We propose the integration of genetic, environmental and developmental perspectives on the evolution of the phenotype in the form of the concept of the developmental reaction norm (DRN) The DRN represents the set of multivariate ontogenies that can be produced by a single genotype when it is exposed to environmental variation. It encompasses: 1) the processes that alter the phenotype throughout the ontogenetic trajectory, 2) the recognition that different aspects of the phenotype are (and must be) correlated and 3) the ability of a genotype to produce phenotypes in different environments. This perspective necessitates the explicit study of character expression during development, the evaluation of associations between pairs or groups of characters (e.g., multivariate allometries), and the exploration of reaction norms and phenotypic plasticity. We explicitly extend the concept of the DRN to encompass adjustments made in response to changes in the internal environment as well. Thus, ‘typical’ developmental sequences (e.g., cell fate determination) and plastic responses are simply manifestations of different scales of ‘environmental’ effects along a continuum. We present: (1) a brief conceptual review of three fundamental aspects of the generation and evolution of phenotypes: the changes in the trajectories describing growth and differentiation (ontogeny), the multivariate relationships among characters (allometry), and the effect of the environment (plasticity); (2) a discussion of how these components are merged in the concept of the developmental reaction norm; and (3) a reaction norm perspective of major determinants of phenotypes: epigenesis, selection and constraint.

How organisms respond to environmental changes: from phenotypes to molecules (and vice versa) (Trends in Ecology & Evolution, 1996).

The ability of organisms to produce different phenotypes under different environmental conditions (phenotypic plasticity) has been an object of evolutionary and ecological studies since the neodarwinian synthesis. Yet, until lately, our knowledge in this field was limited to statistical approaches based on the classical tools of quantitative genetics. In recent years, however, a new dialog between organismal biologists and researchers interested in uncovering the mechanistic details of physiological and phenotypic responses has yielded several new insights. Some classic examples of phenotypic plasticity have now been traced to specific alterations in DNA transcription and RNA translation rates, and to changes in patterns of protein expression. Conversely, the explicit use of evolutionary and ecological theory is helping us to put a panoply of molecular data into a coherent historical and organismal perspective.

On the limits of quantitative genetics for the study of phenotypic evolution (with C.D. Schlichting, Acta Biotheoretica, 1997).

During the last two decades the role of quantitative genetics in evolutionary theory has expanded considerably. Quantitative genetic-based models addressing long term phenotypic evolution, evolution in multiple environments (phenotypic plasticity) and evolution of ontogenies (developmental trajectories) have been proposed. Yet, the mathematical foundations of quantitative genetics were laid with a very different set of problems in mind (mostly the prediction of short term responses to artificial selection), and at a time in which any details of the genetic machinery were virtually unknown. In this paper we discuss what a model is in population biology, and what kind of model we need in order to address the complexities of phenotypic evolution. We review the assumptions of quantitative genetics and its most recent accomplishments, together with the limitations that such assumptions impose on the modelling of some aspects of phenotypic evolution. We also discuss three alternative approaches to the theoretical description of evolutionary trajectories (nonlinear dynamics, complexity theory and optimization theory), and their respective advantages and limitations. We conclude by calling for a new theoretical synthesis, including quantitative genetics and not necessarily limited to the other approaches here discussed.

Ontogenetic phenotypic plasticity during the reproductive phase in Arabidopsis thaliana (Brassicaceae) (American Journal of Botany, 1997).

While phenotypic plasticity has been the focus of much research and debate in the recent ecological and evolutionary literature, the developmental nature of the phenomenon has been mostly overlooked. A developmental perspective must ultimately be an integral part of our understanding of how organisms cope with heterogeneous environments. In this paper I use the rapid cycling Arabidopsis thaliana to address the following questions concerning developmental plasticity. (1) Are there genetic and/or environmental differences in parameters describing ontogenetic trajectories? (2) Is ontogenetic variation produced by differences in genotypes and/or environments for two crucial traits of the reproductive phase of the life cycle, stem elongation and flower production? (3) Is there ontogenetic variability for the correlation between the two characters? I found genetic variation, plasticity, and variation for plasticity affecting at least some of the growth parameters, indicating potential for evolution via heterochronic shifts in ontogenetic trajectories. Within-population differences among families are determined before the onset of the reproductive phase, while among-population variation is the result of divergence during the reproductive phase of the ontogeny. Finally, the ontogenetic profiles of character correlations are very distinct between the ecologically meaningful categories of early- and late-flowering ‘‘ecotypes’’ in this species, and show susceptibility to environmental change.

Ecological and evolutionary genetics of Arabidopsis (Trends in Ecology and Evolution, 1998).

The crucifer Arabidopsis thaliana has been the subject of intense research into molecular and developmental genetics. One of the consequences of having this wealth of physiological and molecular data available, is that ecologists and evolutionary biologists have begun to incorporate this model system into their studies. Current research on A. thaliana and its close relatives ably illustrates the potential for synergy between mechanistic and organismal biology. On the one hand, mechanistically oriented research can be placed in an historical context, which takes into account the particular phylogenetic history and ecology of these species. This helps us to make sense of redundancies, anomalies and sub-optimalities that would otherwise be difficult to interpret. On the other hand, ecologists and evolutionary biologists now have the opportunity to investigate the physiological and molecular basis for the phenotypic changes they observe. This provides new insight into the mechanisms that influence evolutionary change.

Genetics and evolution of phenotypic plasticity to nutrient stress in Arabidopsis: drift, constraints or selection? (with N. Byrd, Biological Journal of the Linnean Society, 1998).

To better understand the genetic basis and evolution of phenotypic plasticity, we have investigated how the model plant Arabidopsis thaliana (Brassicaceae) responds to nutrient stress. A preliminary experiment showed that two populations that are very closely related genetically tended to respond in a similar fashion to a variety of nutrient stresses. We then asked if there is a general relationship between the degree of genetic differentiation of 16 natural populations of A. thaliana and the similarity in the way they cope with a fundamental nutrient stress, nitrogen limitation. We also grew plants from four mutant lines known to be affected in nitrogen uptake and metabolism, using their background isogenic line as a control. This last experiment tested whether or not defects in major genes involved in nitrogen bio- processing affect the intensity or pattern of phenotypic plasticity. We found a high degree of genetic differentiation among populations for the ability to respond to nitrogen stress. However, we detected no significant correlation between the genetic distance among natural populations and the similarity of their response to low nitrogen availability. Since the genetic distances among populations were measured using neutral molecular markers, this suggests that random genetic drift and other non-deterministic evolutionary phenomena were not the driving force shaping differences among populations in the response to stress. On the other hand, several characters were highly correlated in their responses to nitrogen limitation, suggesting either that they were modified by natural selection in a like manner, or that they are influenced by similar genetic constraints (due to either pleiotropy or tight linkage). Finally, the mutants did not differ from the parental wild type strain in their pattern of nitrogen- induced stress response. Therefore, although the genes defective in the mutants are part of the biochemical pathway that uptakes and metabolizes nitrates, we conclude that they are not involved in the control of phenotypic plasticity to nitrogen limitation in this species.

Evolution of phenotypic plasticity a comparative approach in the phylogenetic neighbourhood of Arabidopsis thaliana (with K. Kammell and J. Schmitt, Journal of Evolutionary Biology, 1999).

The evolution of phenotypic plasticity has rarely been examined within an explicitly phylogenetic framework, making use of modern comparative techniques. Therefore, the purpose of this study was to determine phylogenetic patterns in the evolution of phenotypic plasticity in response to vegetation shade (the `shade avoidance' syndrome) in the annual plant Arabidopsis thaliana and its close relatives. Specifically, we asked the following questions: (i) Do A. thaliana and related species differ within or among clades in the magnitude and/or pattern of plasticity to shade? (ii) Are the phenotypic variance-covariance matrices (phenotypic integration) of these taxa plastic to the changes in light quality induced by the presence of a canopy? (iii) To what extent does the variation in uni- and multivariate plasticity match the phylogeny of Arabidopsis? In order to address these questions we grew individuals from six taxa of known phylogenetic relationship in a greenhouse under full sun and under a grass canopy. Taxa differed in the magnitude, but not in the pattern, of plasticities for all traits. At the univariate level, the late flowering species, A. pumila and A. griffithiana, as well as the late flowering Moscow ecotype of A. thaliana, showed greater plasticity for allocation to vegetative and reproductive meristems. At the multivariate level, several taxa displayed a very low stability of their variance-covariance structures to environmental change, with only one taxon sharing as many as three principal components across environments. We conclude that both univariate and multivariate plasticities to vegetation shade can evolve rapidly within a genus of flowering plants, with little evidence of historical constraints (phylogenetic inertia).

Genes affecting phenotypic plasticity in Arabidopsis: pleiotropic effects and reproductive fitness of photomorphogenic mutants (with J. Schmitt, Journal of Evolutionary Biology, 1999).

Many plants exhibit characteristic photomorphogenic shade ’avoidance’ responses to crowding and vegetation shade; this plasticity is often hypothesized to be adaptive. We examined the contribution of specific photomorphogenic loci to plastic shade avoidance responses in the annual crucifer Arabidopsis thaliana by comparing single-gene mutants defective at those loci with wild type plants exhibiting normal photomorphogenesis. The hy1 and hy2 mutants, deficient in all functional phytochromes, were less plastic than the wild type in response to a nearby grass canopy or to a low-red/far-red light ratio characteristic of vegetation shade. These mutants displayed constitutively shade-avoiding phenotypes throughout the life cycle regardless of the treatment: they bolted at an earlier developmental stage and were characterized by reduced branching. In contrast, the hy4 mutant, deficient in blue light reception, exhibited greater plasticity than the wild type in response to vegetation shade after the seedling stage. This mutant produced more leaves before bolting and more basal branches under normal light conditions when compared to the wild type. These results indicate that specific photomorphogenic loci have different and sometimes antagonistic pleiotropic effects on the plastic response to vegetation shade throughout the life cycle of the plant. The fitness of the constitutively shade-avoiding phytochrome-deficient mutants was lower than that of the plastic wild type under normal light, but was not different in the vegetation shade treatments, where all genotypes converged toward similar shade avoidance phenotypes. This outcome supports one key prediction of the adaptive plasticity hypothesis: that inappropriate expression of shade avoidance traits is maladaptive.

Manipulative Approaches to Testing Adaptive Plasticity: Phytochrome-Mediated Shade-Avoidance Responses in Plants (with J. Schmitt and S.A. Dudley, American Naturalist, 1999).

Phenotypic plasticity is often assumed to be adaptive, but this hypothesis has rarely been tested. To support the hypothesis, it is necessary to demonstrate that the phenotype induced in each relevant environment confers high fitness in that environment, relative to alternative phenotypes. Unfortunately, such tests are difficult to perform because plasticity prevents the expression of "inappropriate" phenotypes within each environment. Genetic and physiological manipulation can be used very effectively to extend the range of phenotypes within environments and thus provide powerful tools for testing the adaptive plasticity hypothesis. The expression of specific genes involved in cue perception or signal transduction can be altered by mutation or the introduction of transgenes, thus altering the plastic response of an organism to environmental cues. It is also possible to alter the cue itself or to manipulate the developmental response physiologically so as to obtain alternative phenotypes. The relative fitness of these alternative phenotypes can then be measured in each relevant environment. However, these techniques will be most useful when combined with techniques such as phenotypic selection analysis to identify the specific traits under selection in natural populations. We illustrate these approaches using phytochrome-mediated “shade avoidance” responses in plants as a model system. We review the genetic and physiological mechanisms underlying these responses, illustrate how genetic manipulation can elucidate their adaptive value, and discuss the use of physiological manipulation to measure natural selection on plasticity in the wild.

Mutational contributions to genetic variance-covariance matrices: an experimental approach using induced mutations in Arabidopsis thaliana (with M.D. Camara, Evolution, 1999).

Genetic potential for evolutionary change and covariational constraints are typically summarized as the genetic variance-covariance matrix G, and there is currently debate over the extent to which G remains effectively constant during the course of adaptive evolution. However, G provides only a temporally restricted view of constraints that ignores possible biases in how new mutations affect multivariate phenotypes. We used chemical mutagenesis to study the effect of mutations as summarized by the mutational covariance matrix, M, in Arabidopsis thaliana. By introducing mutations into three isogenic strains of A. thaliana, we were able to quantify M directly as the genetic variance-covariance matrix of mutagenized lines. Induced mutations generally did not alter the means of the six morphology and life-history traits we measured, but they did affect the levels of available genetic variation and the covariances among traits. However, these effects were not consistent among the three isogenic lines; that is, there were significant differences among the lines in both the number of mutations produced by ethyl-methane-sulfonate treatment and the M matrices they induced. The evolutionary implications of the dependence of M on the number of mutations, the particular genetic background, and the mutagenic sampling of loci in the genome are discussed in light of commonly applied models of multivariate evolution and the potential for the genetic architecture itself to change in ways that facilitate the coordinated evolution of complex phenotypes.

(To Be Continued...)

Evolutionary psychology, Jerry Coyne, Robert Kurzban, and the so-called creationism of the mind

by Massimo Pigliucci

Time to take a break from philosophy of mind and get back to evolutionary psychology. The occasion originates from a recent post by evopsych researcher Robert Kurzban, on what he calls "creationism of the mind." There Kurzban excoriates our good old friend, PZ Myers for some apparently silly criticisms he leveled at the field. Kurzban goes on commending Jerry Coyne for having recently seen the light, becoming a supporter of the field. Contra to what some of my seasoned readers may expect, this is going to be neither a defense of PZ, nor an attack on Coyne. But I doubt Kurzban is going to like it anyway (about Jerry, I'm not taking bets).

Let's start with Kurzban's criticism of Myers, whom he tags with the obviously disdainful label of creationist of the mind. According to Kurzban, the latter is someone who subscribes "to the view that the theory of evolution by natural selection ought to be used to inform the study of the traits and behaviors of every living thing on the planet except the bits of the human mind that cause behavior, especially social behavior." I'm pretty sure no evolutionary biologist actually subscribes to this rather strawmanly view, including PZ, but let's proceed. Kurzban further characterizes this brand new type of "creationists" thusly: "Like creationists full stop, creationists of the mind take their positions for reasons other than looking at the relevant evidence. This is clear from the emotion that pervades their remarks about the discipline." Uhm, ok, though it is worth noting that this bit of rhetoric comes from someone who has by this point indulged in a pretty emotional characterization of his own opponents. [Note: I've got nothing against being emotional; to me it means one gives a damn. But you ought not to belittle your opponents for the same kind of behavior you yourself indulge in.]

What exactly did Myers say that so railed Kurzban? Apparently he stated that evolutionary biologists assume a one-to-one causal mapping of genes to behavior, proceeding to dismiss the field on the grounds that such an assumption is in fact ridiculously simplistic (it is). Well, if PZ did say that, he was also attacking a straw man. But the problem of genotype-phenotype mapping is, in fact, a rather big one for evopsych researchers, more so than for pretty much any other evolutionary biologist, because such mapping (i.e., the details of how phenotypes are causally related to genotypes) is made much more complex in humans by the existence of an enormous amount of behavioral plasticity, much of which is induced by a pesky little thing called culture, and all of which makes it pretty difficult (though not necessarily impossible) to test adaptive hypotheses about modern human behavior.

After having dismissed Myers, Kurzban moves on to some good news for evopsych: Jerry Coyne's alleged "conversion" to the field: "Jerry Coyne’s conversion I think serves as a powerful example. His journey from staunch critic to defender of the discipline illustrates that smart people who know a lot about biology can be persuaded. Some of the field’s critics might be induced to read the primary literature, as Coyne did. More deeply, Coyne’s public change of heart, I think, will make it easier for others to say they were wrong." (Note the use of religiously inspired terminology, such as "conversion" and "journey.")

But did Jerry change his position so dramatically? I went and checked what he actually wrote, and it doesn't sound at all like what Kurzban so enthusiastically described. Jerry confirms his (harsh) criticism of evopsych researchers like Randy Thornhill and Craig Palmer (them of "rape is an adaptive strategy" fame), as well as of much of "pop" evopsych (citing as one of the most ridiculous recent examples David Brooks' latest book - essentially a Republican fantasy of how things are and therefore ought to be in the world).

Nonetheless, Coyne continues, the field is, ahem, evolving, and getting better. There are some serious researchers who actually pay attention to the testability of their hypotheses, and who try to be careful about what they say when they write for the public. I don't know many critics - either within biology or in philosophy of science - who would disagree with that kind of cautious assessment. When Jonathan Kaplan and I wrote about evopsych in our Making Sense of Evolution we were careful to draw exactly the same distinctions that Jerry draws. I know there are misguided postmodernists out there who reject evopsych no matter what, but most thoughtful commentators have never done that, just like current critics of the excesses of neuroscience do not thereby dismiss it as phrenology.

That said, I still don't think Jerry's criticism of evopsych goes far enough, for one very important - but also, I would think, very obvious - reason: human beings really do present special challenges when it comes to the scientific study of their behavior, especially of the evolution of that behavior.

To get us started, let's look at some of the entries in Jerry's list of recent successes (or at least examples of progress) in evopsych. Some are obvious and hard to dispute: incest avoidance, innate fear of dangerous animals, parent-offspring conflicts, and the like. As Kaplan and I (and plenty of others) have pointed out, these are the areas where evopsych is at its strongest because the target behaviors are common among mammals, or at least primates. Which means that phylogenetic comparative analyses - one of the best hypothesis testing tools at the disposal of evolutionary biologists - work well.

Other examples are a bit odd. Jerry mentions, for instance, the evolution of sexual dimorphism (differences in size between male and female) and the evolution of concealed ovulation in human females. These are actually morphological, not behavioral traits, though they certainly influence behavior (and perhaps have been historically influenced by behavior). One needs to be careful about not unduly expanding the domain of evopsych to include every human trait, or it becomes too easy to claim success. (For instance: yeah, human females evolved larger breasts than men because they nurse their babies. I doubt even a postmodernist would try to culturally relativize that one!)

Jerry also mentions traits that are variable within the human species (as opposed to the classical focus of evopsych, human universals), for instance offspring numbers across societies, or physical and physiological differences among ethnic groups (though, again, why would the latter count as behavior is a bit puzzling). Kaplan and I also highlighted this area (systematic variation within Homo sapiens) as potentially fruitful for evopsych, though caution needs to be exercised because some of these traits (e.g., offspring number) could vary at least in part as a result of cultural forces, not genetic evolution (just think of the differences between, say, some fundamentalist religious groups and many mainstream ones: in societies where the former are in significant numbers the birthrate will be much higher than in societies where religious fundamentalism is numerically insignificant, but I would guess that culture, rather than genetics, is doing much of the work here).

Jerry also counts as a success for evopsych research on gene-culture co-evolution, as in the famous case of lactose intolerance. Which is odd, because that approach is usually seen as significantly distinct from evopsych (it's based on the extension of standard population genetics models to cultural evolution), and at any rate has had somewhat limited success (there aren't that many documented cases around, other than the oft-cited lactose intolerance).

Things become seriously iffy with yet another group of examples advanced by Jerry as positive entries in the evopsych column: the evolution of language and the evolution of morality. Steven Pinker's interesting speculations aside, we really don't have much of a hold on the evolution of language, for the simple reason that it is a classical worst case scenario for evopsych: it is unique to humans (yes, yes, other animals communicate, but language is a whole different beast) and not really variable within humans - except for pathologies - which means that comparative phylogenetic studies are out; so, of course, is the fossil record (except insofar that tells us when we evolved the anatomy necessary for language); and, needless to say, we have no access to direct measurements of relevant selective pressures. Yes, something can be learned by the study of the (very complex) genetics underlying language abilities, but it is hard to see how one can significantly move away from the sort of "just-so" stories for which evopsych is infamous. (If these stories are instead presented as untested but reasonable scenarios, then it's a different matter.)

As for morality, I am the first to agree that Frans de  Waal-type studies with other primates provide the basis for interesting speculations on how it evolved, but let's remember that his comparative studies are based on an extremely reduced number of species, that these species are pretty distantly related to us, and that they show very significant differences among themselves in terms of prosocial and pre-moral behavior. Not to mention that human morality is exceedingly more complicated than any animal equivalent because, you guessed it, of cultural evolution.

Which brings me to the crucial point where I disagree with Jerry about evopsych, in this case (which is unusual, believe me) in the sense that I am more conservative than he is. As Jerry puts it in his post: "My position has always been that good evolutionary psychology should
meet the evidentiary standards of papers on the evolutionary significance of behavior in other animals ... Those who dismiss evolutionary psychology on the grounds that it’s mere 'storytelling' ... if they are to be consistent, they must also dismiss any studies of the evolutionary basis of animal behavior."

Well, no, that's really moving the bar too low. Sure, evopsych research has to meet at the very least the standards of research on animal behavior (and believe me, a number of evopsych studies don't, though some certainly do). But human beings are far more complex and flexible (the technical term is plastic) in their behavior, and far less beholden to their genetic leash, than any other species on the planet, largely of course because of the power of cultural evolution. That means that evopsych researchers need to be much more careful in their studies than animal behaviorists, for precisely the same reasons that research psychologists get a lot more headaches while carrying out their work than their colleagues studying mice or fruit flies.

So, I agree with Jerry that it is silly to reject evopsych outright. It is a borderline field that can easily produce crap as well as good stuff. Therefor, criticism from the outside is vital in keeping evopsych tilting away from the former and increasingly toward the latter. But a rejection of certain conclusions alleged by evopsych does not at all require an equal rejection of animal behavior research. The standards ought to be higher.

Disobedience Succeeds Essence

by Steve Neumann

There is much that life esteems more highly than life itself... — Nietzsche, Thus Spoke Zarathustra

Jean-Paul Sartre distilled his existentialism into the maxim “existence precedes essence.” He meant that the human being has no predetermined nature, divinely-ordained or otherwise, and that each human being is solely responsible for defining herself. Sartre said that the first principle of (his) existentialism is that “man is nothing else but what he makes of himself.”

University of Washington psychology professor David Barash recently published a nice meditation on the notes of consonance between evolution and existentialism in The Chronicle of Higher Education. Barash ultimately concludes that a 

...philosophy of “human meaning’ can coexist quite well with a science of “genetic influence.” 

Happily, Barash’s notion of human meaning includes the idea that, even though we are completely natural creatures shaped by evolutionary processes, we still retain a unique human freedom. I say happily because Barash doesn’t conclude that humans have contra-causal free will, nor does he jump to the opposite, fatalistic conclusion that no matter what we do, the outcome will be the predetermined same, so why bother. His idea of human agency is roughly the same as mine. As he says:

Within a remarkable range, our evolutionary bequeathal is wildly permissive.

I like Barash’s word choice of “wildly” here. Ironically, though much of my free time is spent thinking about how to persuade people that the difference between us and other animals — even dogs — is a difference of degree and not of kind, I often worry about us forgetting how dissimilar we are to all other animals, at least in one significant regard: that is, freedom. And what I like most about Barash’s article is the notion of freedom as the freedom to disobey. As Agent Smith puts it to Neo in the second Matrix film:

Smith: I killed you, Mister Anderson, I watched you die — with a certain satisfaction, I might add. And then something happened; something that I knew was impossible, but it happened anyway: you destroyed me, Mister Anderson. Afterward, I knew the rules, I understood what I was supposed to do but I didn’t. I couldn’t. I was compelled to stay, compelled to disobey. And now here I stand because of you, Mister Anderson, because of you I’m no longer an agent of the system, because of you I’ve changed — I’m unplugged — a new man, so to speak, like you, apparently free.

Neo: Congratulations.

Agent Smith disobeyed his programmed nature and found out what he really wanted: in his case, the destruction of the Matrix (and of all life, unfortunately). Barash also specifically argues for a type of contra-natural disobedience:

On the basis of evolutionary existentialism, I would therefore like to suggest the heretical and admittedly paradoxical notion that, in fact, we need to teach more disobedience. Not only disobedience to political and social authority but especially disobedience to some of our troublesome genetic inclinations.

Disobedience has a long history in the human species. Even the ancient Hebrews, it can be argued, intuited the need for disobedience by sneaking the wily, skeptical serpent into their creation story. They had their god include the serpent in that paradisal garden, where his new and naive human creations were within arm’s reach of the fruit of both god-like knowledge and immortality. Now, the common Christian response is that God wanted his creations to have the possibility of disobedience — that is, free will — to freely love Him or reject Him, and which would presumably have more authenticity thereby. But I don’t think having the freedom of disobedience need be interpreted in terms of love, in a religious context or not. Disobedience, in my opinion, is first and foremost a route to knowledge, particularly self-knowledge. And it’s self-knowledge the existentialists have traditionally been most concerned with, seeing how it leads to one’s having the ability to define oneself. But Sartre (and existentialists in general) countenances an extreme freedom of the will as the driver behind the quest for self-knowledge, so much so that he assigns ultimate responsibility — and blame. As he says:

If people throw up to us our works of fiction in which we write about people who are soft, weak, cowardly, and sometimes even downright bad, it’s not because these people are soft, weak, cowardly, or bad; because if we were to say... that they are that way because of heredity, the workings of the environment, society, because of biological or psychological determinism, people would be assured.

As a quick aside, I think it’s interesting to note here that Sartre brings up this particular objection back in the cultural backdrop of 1946. It sounds more like the pejorative Twinkie Defenses of the late 1970’s and onward. But I digress. Sartre goes on to say that

...when the existentialist writes about a coward, he says that this coward is responsible for his cowardice... he’s like that because he has made himself a coward by his acts.

From a certain perspective, this is undeniably true: a human being can’t become anything without acting in some sense; but the real crux of the issue is how responsible the individual is, if at all, for who she has become. Like Barash, I think existentialism of a certain strain is compatible with our condition as evolved biological animals. And it’s the idea of disobeying our nature that gives us both the opportunity and the freedom to become what we want. As Nietzsche put it in an early fragment (1872), “Homer’s Contest”:

When one speaks of humanity, the idea is fundamental that this is something that separates and distinguishes man from nature. In reality, however, there is no such separation: “natural” qualities and those properly called “human” are indivisibly grown together. Man, in his highest and most noble capacities, is wholly nature... Those of his abilities which are awesome and considered inhuman are perhaps the fertile soil out of which alone all humanity... can grow.

Here, as I see it, the concept of “humanity” is the result of the exploitation of the “wildly permissive” freedom bequeathed us by our evolutionary history, as Barash notes. The individual human being needn’t be metaphysically free in the existentialist’s sense in order to cultivate her animal nature. And while it may be prudent to assign a certain degree of responsibility for the way people “create” themselves, I don’t agree that the coward, for instance, has made himself into a coward on purpose, so to speak. So, for me, something like cowardice isn’t necessarily a fault of the individual so much as the result of a weak will. And I think one’s will can be educated and strengthened, because even the weak-willed individual has, thanks to the evolutionary bequeathal, the freedom to disobey his essence. Of course, the question is exactly how does that happen — how does the weak-willed person educate and strengthen his will? Traditionally, various modes of asceticism have been employed. But there is also a good amount of simple luck involved: one may or may not be exposed to an array of interpersonal and environmental experiences that likewise may or may not sway one’s motivation to do or not do something conducive to educating or strengthening one’s will. 

In a note from 1887 Nietzsche had this to say about asceticism:

I also want to make asceticism natural again: in place of the aim of denial, the aim of strengthening...

To make asceticism natural again is to expropriate it away from its religious roots, where the goal was to tame the human animal and make it obedient to both celestial and terrestrial authority, and now to use it to educate one’s will by imposing restraints on one’s genetically-influenced impulses. So, in a sense, making asceticism natural again involves paradoxically making one’s nature obedient in some ways in order to disobey that nature in other ways. And these other ways relate to the existential quest for human meaning and self-creation. I suppose you could also look at it as a more refined type of asceticism: instead of bludgeoning one’s entire natural endowment into submission, one can pick and choose which impulses to quash and which ones to amplify. And even if one’s life circumstances are stifled or constricted, one still possesses the capacity for disobedience, or what we might call “revolt” in Albert Camus’ parlance. 

In Camus’ The Myth of Sisyphus, we see that the absurd Greek hero is  condemned to “ceaselessly rolling a rock to the top of a mountain, whence the stone would fall back of its own weight”; and Camus explicitly ties Sisyphus’ plight to that of the proletarian worker of his day. Revolt or “scorn” at circumstances is still possible even if one has no hope for a different future. And while Camus seems to believe that even freedom from creating meaning in one’s life is a good thing when seen in a certain light, I think you could also argue that the hour where Sisyphus contemplates his fate, which is what Camus says interests him most, is the timeless moment in which meaning can be created. Our own Sisyphean disposition can allow us to contemplate all kinds of strategies and “games” while toiling at moving one’s rock to the top of the mountain. In fact, in a way we could play with the existentialist’s own phrasing and say that one is condemned to be creative. Consider this: the human brain is a veritable whim-generating machine; we can’t stop thoughts from occurring to us, nor can we stop thinking altogether. When Camus says that “the struggle itself toward the heights is enough to fill a man’s heart” and that therefore we must “imagine Sisyphus happy,” I would say that it is precisely the brain’s propensity for spontaneous activity that is the source of the human — and even animal — impulse to play. 

What is play? The essence of play is, to my mind, the compulsion to experiment and explore; or, in other words, to revolt and discover. Not only does play merely pass the time, but the imagination can create worlds within worlds. Consider what the human imagination has produced thus far: philosophies, religions, artistic vistas, staggering technologies, etc. As William Blake noted: “what is now proved was once only imagined.” The act of imagining something new does a certain violence to what already exists: it destroys, betrays or at least dispenses with what has already been established. In a sense, the imagination disobeys the essence of what already exists, the accumulated and codified mores that are generally accepted. Combining the imagination and a revised asceticism involves a great deal of courage: the courage to disobey interpersonal, cultural, and biologically-determined patterns of thought and behavior, thereby incurring or inviting the wrath and opprobrium of one’s milieu — and possibly even of Nature herself.

And psychological harm is not the only danger: just as Nietzsche said that life oftentimes values more than existence itself, one may very well lose one’s life through stratagems of disobedience. But isn’t the value of one’s life, the meaning of one’s life, more important than the mere duration of it? Essence doesn’t precede existence, and neither does existence precede essence; they’re contemporaneous and they grow or perish together. But disobedience, properly executed, succeeds both essence and existence. 

I’ll leave you with our modern-day, popular culture Sisyphus, Neo, near the end of the final installment of The Matrix Trilogy:

Smith: Why, Mr. Anderson, why? Why do you do it? Why get up? Why keep fighting? Do you believe you’re fighting for something, for more than your survival? Can you tell me what it is? Do you even know? Is it freedom, or truth — perhaps peace? Could it be for love? Illusions, Mr. Anderson, vagaries of perception, temporary constructs of a feeble human intellect trying desperately to justify an existence that is without meaning or purpose — and all of them as artificial as the Matrix itself. Although, only a human mind can invent something as insipid as love. You must be able to see it, Mr. Anderson, you must know it by now. You can’t win, it’s pointless to keep fighting. Why, Mr. Anderson, why — why you persist??

Neo: Because I choose to.

On the species of species

by Leonard Finkelman

So the story goes: it was a bright and sunny afternoon in ancient Athens, ca. 360 BCE, when Plato delivered his opening remarks in a public lecture about “The Good.” Everyone who was anyone in the city had turned out: the landowners (who wanted to know how to be good landowners); the merchants (who wanted to know how to be good merchants); the wealthy layabouts (who thought that the advertisement about “wrestling with ignorance” entailed a different sort of entertainment); the grad students (then, as now, society’s obvious crème de la crème). As civilization’s greatest philosopher droned on about geometry and nothing else, he began to lose the crowd. First the merchants left. Next went the landowners. Some students lingered, but eventually most of them left, too, realizing that they still had scrolls to grade. By the time Plato ended the talk, one student remained in attendance. That student went home, lit a candle, and began writing a scathing critique of the lecture. His name was Aristotle; his work became known as the Metaphysics. (No one knows what became of the wealthy layabouts.)

Although I haven’t checked, I’m pretty sure that the dictionary entry for “apocryphal” now includes a picture of an Ancient Philosophy professor relating the above story. It never happened. Still, it’s what immediately came to mind when I read some of our illustrious host’s recent essays.

It’s no secret that Massimo is my dissertation adviser, making him one of five people in all time and space who will suffer through my fanatical ravings about the intersection of the species problem and the levels-of-selection debate. Buried within the 66,052 words of my thesis are three arguments: first, that species are natural kinds if and only if species selection is possible; second, that (some) species are natural kinds; third, that species selection is possible. (I do try to cover my bases.) So when Massimo wrote that species selection “is not selection, but … sorting,” I felt the sort of apprehension one only feels upon learning that a friend has reunited with an ex-significant other. We had talked this over, I thought; surely you saw the reasons to move on!

I don’t want to overstate things. We may just be looking at the most serious philosophical falling out since Aristotle responded to Plato [1]. Before it comes to that, let’s review the issues involved and see if we can’t pull Massimo back from the Dark Side.

First, we should sort out sorting and selection. The distinction here can be made through a delicious series of experiments. Take two groups of hungry volunteers and two bags of MandMs for each group: one with dark chocolate  MandMs and one with peanut Hanukkah MandMs . In one group of volunteers, empty the bags into a bowl and then ask the volunteers to select candies on the basis of color preference. In the other group, ask the volunteers which bag to open and serve first on the basis of flavor. Here’s what would probably happen in the first experiment: color preference is very heavily biased towards blue and against brown, and so the last remaining  MandMs will probably be brown; since the Hanukkah  MandMs  only come in blue and white, the remaining  MandMs will be dark chocolate ones. Here’s what would probably happen in the second experiment: peanut  MandMs are more popular than dark chocolate  MandMs, and so the volunteers will likely ask to open the Hanukkah bag first. In both cases, dark chocolate  MandMs “survive,” but the explanation for the flavor’s persistence in the first case is sorting while the explanation in the second case is selection.

The distinction between sorting and selection is drawn by the level of selection. In the first experiment above, volunteers select individual  MandMs, and the association of colors with flavors leads to the sorting of flavors. In the second experiment, volunteers select a whole bag of candy, leading to the persistence of one flavor; the individual  MandMs are just along for the ride. Similarly, species sorting would be the differential persistence of collections of organisms due to the properties of organisms in those collections, and species selection would be the differential persistence of collections of organisms due to properties of the collections themselves [2].

When Massimo says that purported examples of species selection are actually cases of species sorting, what he’s expressing is the majority view among evolutionary theorists and philosophers of biology: that the levels of selection have their ceiling below the species level, and any differential speciation or extinction (i.e., reproduction or death of species) is the result of selection of genes, organisms, or local populations. Species seem to be more abstract (at best) and ephemeral (at worst) than any of those, and so the consensus view is that they’re not the sorts of things that can bear properties necessary for selection.

Cue record scratch: or are they?

Part of the problem with any discussion of species is the fact that we so rarely make it clear what it is we’re talking about. I don’t simply mean that there’s debate over how to define species — the “species problem” that so concerns philosophers of biology — but more that disputants in that debate often talk right past one another. In the past century alone, the word “species” has been used regularly in at least half a dozen different senses [3]. The bottom line: when Massimo says that species aren’t targets of selection and I say that they are, we might not be contradicting each other.

When you learn biology in high school, or as an undergraduate, the subject tends to be presented as a monolithic combination of physiology, ecology, zoology, botany, genetics, paleontology, evolutionary theory, and taxonomy. This view of the discipline is an historical accident. Before the first half of the twentieth century, each of these fields carried on mostly independent of the others; it was only through the efforts of theorists such as R.A. Fisher, J.B.S. Haldane, Julian Huxley, Theodosius Dobzhansky, Ernst Mayr, and G.G. Simpson that the theory of natural selection came to be viewed as a unifying explanation that could tie the life sciences together. Still, one can be a taxonomist and (justifiably or not) remain largely oblivious to the work being done in, say, genetics [4].

To a great extent, debate over the species problem is an attempt to resolve the cross-talk between different disciplines in biology. In particular, taxonomists are concerned with the grouping of organisms into species by some standard of similarity where evolutionary theorists are concerned with the study of populations that evolve; much of the work done on the species problem involves the attempt to find a similarity standard for the units of taxonomy that would identify them with the units of evolution [5]. Species selection would add a new wrinkle to this problem: not only would the units of taxonomy have to be identifiable with units of evolution, but both would have to be identifiable with a unit of selection.

The big, seemingly insurmountable problem: as I’ve already noted elsewhere (and as Massimo similarly acknowledged), natural selection can only “target” individuals, and only collections of individuals can evolve. Species selection would require that species are individuals and collections of individuals, and that taxonomy can somehow reflect the idea that one thing can be identical to many things.

Really, it’s enough to make even the most patient and careful philosopher of biology just throw up her hands and give up on all this nonsense. But which nonsense? Some biologists have recently suggested that we just ditch the idea of species; however, by far the more common alternative is to give up on species selection.

Of course, one should never underestimate the gumption and stubbornness of a dissertation-level grad student. Biology, you see, is chock full of things that are individuals in one sense and collections of things in another. Hell, just look in the mirror: not only is your body dependent on trillions of bacteria that call your insides “home,” but each of your own cells is descended from some ancient unicellular organism, thus making you both one thing and many things. This should be a fairly uncontroversial point. If we accept evolution, then we should accept that before there were multicellular organisms there should have been unicellular organisms, and before unicellular organisms there should have been genes, and so on. New kinds of individual have emerged throughout evolutionary history.

Emergence is a thorny philosophical issue. I want to avoid it to whatever extent I can. Luckily, the practice of evolutionary biology seems to offer a nice way out. By what standards do biologists recognize the emergence of a new sort of biological individual [6]? Why do we say that a human being, apart from having hundreds of trillions of cells, is a single organism, whereas a biofilm is just a collection of individual microbes? Most considerations of the question seem to settle on two criteria: division of labor between parts and intrinsic maintenance of functional integration [7]. In other words, something is considered a biological individual if its different parts do different things, and all the different parts are organized towards a common goal.

We see these two criteria satisfied by genomes, given the distinction between regulatory and structural genes and their integration in development. We see the criteria satisfied by cells, given the distinction between organelles and the unification of their disparate roles in cellular function. Organisms satisfy the criteria, too, as noted above. And that’s where most biologists stop, except for the few who point to insect colonies with one hand and make rude gestures towards Richard Dawkins with the other.

But there’s a good reason not to stop there, because there are other things in the living world that have a fundamental division of labor and mechanisms for maintaining functional unity. Those things are sexually reproducing species. Think about it: a sexual species requires both males and females (or at least differentiation between gametes), and hybrid sterility (generally) ensures that those males and females can only reproduce viably with members of their own species. In the same way that organisms represented a major evolutionary transition from individual cells, so too may sexual species represent a major evolutionary transition from individual organisms [8].

Here is where I take a rare departure from my mentor. Massimo denies that a theory of multilevel selection should be extended upward to include species selection because he thinks of species as units of taxonomy to be identified with units of evolution. To his credit, this view — that species are collections of organisms and not functional individuals — predominates among practicing biologists (if not philosophers of biology; see note 3). I believe that there is no reason not to extend multilevel selection upward, and that some (but not all) units of taxonomy — particularly, those identified with units of evolution whose members reproduce sexually — can be identified with potential units of selection.

To return to an earlier point: the depths of our agreement are obscured by a poverty of language. I agree that many, and perhaps most, cases of “species selection” could be explained by species sorting, and that what looks for all the world like nature picking whole bags of  MandMs is probably just selection of particular colors. But I suggest that while most collections of organisms that we call “species” do not represent a major evolutionary transition, one particular kind does, and that we use the word “species” equivocally in labeling this kind of collection. Sexual species are units of evolution identifiable with units of taxonomy, but they are also units of selection that emerge out of the units of evolution, by the same criteria according to which biological individuals emerge at lower levels of selection. Species selection, as distinct from species sorting, is therefore (at least) possible. We just have to use the word “species” in a different way.

As far as I can tell, I’m not playing Calvinball here (i.e., making up new rules and defining myself into being right); I’m still in the sandbox, playing by the sandbox’s previously established rules. I just want to get Massimo to recognize a new way of seeing those rules. After all, philosophy can ill afford another split as epochal as the one that started when Aristotle took his proverbial ball and went home [9] [10].

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[1] Before anyone accuses me (or Massimo) of hubris: this is what we sometimes refer to as “hyperbole,” or an exaggeration potentially used to comedic effect. I would never dream of comparing myself to Aristotle, nor does Massimo consider himself a Plato analogue. After all, Plato and Aristotle were amateurs compared to us. (Again: joke.)

[2] Technically speaking, all differential propagation is sorting, and so selection itself would be a type of sorting; however, within the context of the current debate, “sorting” tends to mean “types of sorting that aren’t selection,” and so that’s the sense I’ll go with here.

[3] To wit: following Aristotle, logicians use “species” as a mark of logical distinction; following Owen and Agassiz, neo-Platonists use “species” to describe abstract organic forms; following Linnaeus, taxonomists use “species” as a category for organizing living things; following Darwin, evolutionary theorists use “species” to describe branches on the evolutionary tree; following Dobzhansky, ecologists and population geneticists use “species” to distinguish reproductively isolated groups of organisms; following Ghiselin and Hull, philosophers of biology use “species” to describe conceptually individuated evolving groups.

[4] This is why, for example, taxonomists argue that giant pandas and red pandas should be included in their own taxonomic group, geneticists argue that giant pandas are bears and red pandas are distant relatives of raccoons, and people trying to make interesting conversation at dinner sometimes say things like, “Some pandas aren’t pandas!” (All I know is that both species are incredibly lucky that no one finds them tasty.)

[5] An important exception to this generalization is Philip Kitcher, whose pluralist account is best summed up as: “Hey, bygones.”

[6] Some philosophers of biology — Alex Rosenberg, for example — deny biological emergence altogether. But (as Rosenberg himself points out) this is not how biologists actually engage their field of work. Biologists themselves may be more or less consistent in their antireductionism, but at least within the context of the field we can discuss their reasons for accepting the view.

[7] Full disclosure: there are plenty of sources — Leo Buss being my personal favorite — who cite additional criteria; however, the two I’ve listed are recognized as necessary by most (if not all), and as sufficient by some. To quote Krusty the Clown, it’s not just good; it’s good enough!

[8] And for those who wondered what happened to the talk of natural kinds: since natural kinds are collections that bear many of the same metaphysical characteristics as individuals, emergent species would be natural kinds.

[9] Just in case the point needs to be reiterated, see note 1 above.

[10] For all the Lawrence Krausses out there (as if one wasn’t sufficient): the preceding conceptual analysis is precisely the sort of thing that philosophy can do and science can’t. What sort of empirical evidence can settle the question of how to define the word “species”? Which experiment will decide whether species are real biological things or merely nominal aggregates of other biological things? And most importantly: isn’t it clear how these philosophical questions can have an effect on the actual study of the relevant science?