(12/09/2012)

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Frédéric Bouchard

Département de philosophie

Université de Montréal

f.bouchard@umontreal.ca

PIONEERING PARADIGMS AND MAGNIFICENT MANIFESTOS - LEIGH VAN VALEN’S PRICELESS CONTRIBUTIONS TO EVOLUTIONARY BIOLOGY

FINAL VERSION IN    EVOLUTION VOL 65 (4) PP.917-922

DOI: 10.1111/J.1558-5646.2011.01242.X

http://onlinelibrary.wiley.com/doi/10.1111/j.1558-5646.2011.01242.x/abstract

Liow, L. H. Center for Ecological and Evolutionary Synthesis (CEES), Department of Biology, University of Oslo, Oslo, Norway

Simpson, C. Museum für Naturkunde,  Humboldt University Berlin, Berlin, Germany

Bouchard, F. Département de philosophie, Université de Montréal, Montréal, Québec, Canada

Damuth, J. Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, California, USA

Hallgrimsson, B. Department of Cell Biology & Anatomy, University of Calgary, Alberta, Canada

Hunt, G. Department of Paleobiology, Smithsonian Institution, Washington, District of Columbia, USA

McShea, D. W. Department of Biology, Duke University, Durham, North Carolina, USA

Powell, J.R. Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, USA

Stenseth, N.C. Center for Ecological and Evolutionary Synthesis (CEES), Department of Biology, University of Oslo, Oslo, Norway

Stoller, M. K. Biological Sciences Collegiate Division, University of Chicago, Chicago, Illinois, USA

Wagner, G. Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, USA

n.b. I am not the official contact author, but if you have questions or comments: FRÉDÉRIC BOUCHARD

Département de Philosophie, Université de Montréal, P.O. Box 6128, Station Centre-ville, Montréal, Québec, Canada H3C 3J7; email: f.bouchard@umontreal.ca; www.fredericbouchard.org

INTRODUCTION

Evolutionary biology lost a unique, broad, creative and influential thinker when Leigh Van Valen[1] passed away on Oct 16 2010 in Chicago at the age of 75. He was Professor Emeritus of Ecology and Evolution at the University of Chicago and served on the Committees on Evolutionary Biology, Conceptual Foundations of Science and Genetics. Unwritten ideas still coursed through his ceaselessly active mind as he fought and lost his last battle against phylogenetically distant and diverse microbes.

We are a multi-flavored group who want to honor this extraordinary thinker and teacher, and to bring broad attention to Leigh’s life’s work, much of which was ahead of his times. We reflect briefly on his work on mammal evolution, energy as an organizing principle in ecology and evolution, adaptation, evo-devo, homology and complexity, even though his “interests go beyond what this blurb indicates,” quoting directly from his homepage. Leigh’s niche in biology has been to open up new areas of research without attempting to provide final answers to the novel questions he identified. He synthesized empirical observations into a cohesive paradigm that often unified traditional disciplines.

Mammals: bridging neontology and paleontology

Though Leigh contributed to virtually every aspect of the “evolutionary half of biology”[2] , and addressed issues involving the widest range of taxa, his “main group” was the Mammalia. He used mammals extensively as examples of and sources of insight for much of his conceptual research. Leigh was also an active participant in attempts to clarify the origins and systematics of early mammals, topics vigorously debated at the beginning of his career in the 1960’s and 1970’s . Far from solely solving systematic puzzles, Leigh applied neontological quantitative techniques for measuring natural selection, variation, and life history to fossil mammals — bridging the conceptual gap between neontology and paleontology that characterized the early years of the Modern Synthesis . Leigh showed how fossil species can exemplify the same evolutionary processes that are observed in extant species. The fact that today we regard this fact as unsurprising is testament to the application of quantitative theory to paleobiology by Leigh and others at a time when such an approach was a new idea.

The mammalian fossil record offered for Leigh the most informative direct evidence for how evolution occurred over long time spans. Leigh felt that a true understanding of macroevolution required causal explanations and mechanisms, and he sought them at a variety of scales. He regarded mammalian orders (and other such taxa) as having, at any given time, an adaptive and ecological unity that allowed them to participate in macroevolutionary processes . Indeed, it is difficult to separate Leigh’s most persistent and broad-scale theoretical efforts —selective processes at multiple levels, reformulation of evolutionary processes in terms of energy relations, evolution of whole biotas — from the need to formulate a conception of evolution that was sufficiently general to bring the fossil record into the embrace of a causal evolutionary theory. The Red Queen is a prime example of this effort.

Red Queen: energy as common currency

Leigh’s most widely-cited and perhaps most misunderstood work, concerns evolution within adaptive zones and communities. He observed that the extinction probabilities of fossil organisms were age-independent, i.e. lineages do not become more extinction-resilient over time. The Red Queen’s Hypothesis  is a conceptual paradigm for explaining this observation, and is extendable to communities of interacting entities. The Red Queen states that any gain in the control of energy by a species or higher taxon necessarily means a joint equivalent loss for all other co-occurring taxa in the adaptive zone. Energy as the driving force in evolution is a common thread though many of Leigh’s ideas. The Red Queen also reflects the somewhat controversial idea, that competition is important in evolution at all time-scales. Viewing energy as a common currency for ecological analyses is a currently rapidly growing perspective  but a cohesive application of Leigh’s energy framework to evolutionary analysis is still lacking.

Leigh’s work on origination and extinction rates was contemporaneous with other such work , but his view uniquely synthesized the interactions between the biological and the physical world . He found that origination rates of families have declined through the Phanerozoic, although extinction rates have been relatively stable , corroborating his view that “extinction rates measure degree of resistance and external stresses” while “origination rates measure the ease of adaptive change” . The resilience of a species (or higher taxon) evolves but does not improve temporally because its effective environment declines: this is the Red Queen in action. On the other hand, the ease of adaptive change declines as adaptive zones fill. Since then, prominent studies  have brought more attention to large-scale patterns of turnover rates, attracting overdue research on mechanistic explanations. The Red Queen continues to fuel debates on whether evolution on geological time scales is driven by biotic or abiotic forcings . We note, however, that Leigh never intended to exclude physical factors as agents of biotic change, or to attribute evolution to only biotic drivers. Leigh saw that physical forces that can reset equilibrial processes , although he thought “most environmental pressure is biotic rather than physical” .

Leigh’s discussion on “bloom phases, initial crunches, exclusion and saturation” described the macroevolutionary analogue of density-dependence . Recent papers that concern the current version of this model, describing early bursts of speciation and the slowing down of diversification rates as niche space fill ups , do not mention Leigh’s more fully conceptualized model stemming from Lyell and Simpson . Current research on diversity-dependent diversification will gain handsomely from Leigh’s crystal-clear reasoning on the separate contributions of origination and extinction processes to the net result of diversification.

Fitness and levels of selection

Leigh advocated a new and “heretical” notion of fitness, where the fundamental unit of selection is not tallied as the number of offspring, but as the control of free energy . Like Hamilton who proposed genes as the fundamental unit of selection , Leigh wanted to provide a common currency for fitness that can be used to traverse different levels of biological organization for unified analysis. Leigh often cited Egbert Leigh’s remark: “if life evolved elsewhere it would not necessarily need any of the specific chemical materials our life does, but it would need free energy” . Natural selection follows when organisms have differential control of limited free energy, summarized in Leigh’s third Law of Natural Selection , where “Natural Selection maximizes, at any level or time-scale, expansive energy.” Leigh divided fitness into three components, reflecting ways in which energy could be put to use evolutionarily, namely persistence, reproduction and expansion. Expansion is differential growth: a bryozoan colony crowding out another is natural selection because the relative energy amount of energy each colony controls changes. While reproduction leads to new adaptations, expansion and persistence confer stability . By characterizing fitness in terms of the control of energy, intra- and inter-specific fitness, and evolutionary success in compositionally different systems with diverse histories, heterogeneous parts and incommensurable ecology, even contemporaneous species, and different species sharing an adaptive zone at different times can be compared.

The independent and sometimes antagonistic nature of different levels of selection was a strong focus of Leigh’s work , at a time when this view was uncommon. For example, in mammals, large body size is selected for at the organismal level and against at the species level , resulting in an equilibrium body size. Body size is expressed in individual organisms but has consequences for long-term evolution due to its correlation with life history traits that increase extinction risk.  In this way body size illustrates how sometimes the level of selection (in this case the species) can be equivalent to long-timescale selection on organismal traits

Homology: the continuity of information

Thinking hard about mammals led Leigh not only to his reformulation of fitness and the Red Queen, but also to the conceptualization of homology of morphological characters. The first stage in the elaboration of tooth shape in the stem lineage of mammals is the three-cusped tooth. The common-place identification of the early mammalian major cusp with the single cusp of the reptilian tooth was embodied in then mainstream “premolar analogy theory” . However, Leigh showed using a detail in the evolution of horse teeth that this whole enterprise was conceptually flawed .

Molars appear to have been derived from premolars by the addition of cusps. However, apparently corresponding cusps among adjacent premolar teeth in Orohippus, an early horse genus, in fact arose from different positions. There was selection for increased grinding surface over the course of horse evolution where each premolar tooth added cusps in similar locations but had different derivations either de novo or from nearby ancestral cusps. Leigh interpreted this as a breakdown of homology assessment among tooth cusps, meaning that tooth cusps lack historical continuity beyond that among highly related species . Leigh’s interpretation is confirmed by recent work where “It is unlikely that there is a simple ‘gene to phenotype’ map for dental characters. Rather, the whole cusp pattern is a product of a dynamic developmental program manifested in the activation of the developmental modules” .

What Leigh recognized, earlier than most, was that homology only applies to body parts that are developmentally and genetically individualized. This is the first step in a long struggle towards understanding the mechanistic basis of homology. Leigh also proposed a new definition of homology, namely, correspondence based on continuity of information. He anticipated that this definition did not require homologous parts to be based on identical genetic information, a point now clear from comparative developmental genetics. He was a pioneer in realizing that the true challenge in understanding homology is identifying the molecular mechanisms that provide continuity to the phenotype in the midst of a sea of genetic change, but nobody had the means to follow his lead until 20 years after the publication of  “Homology and Causes.”

Information and developmental complexity

Deep in a paper on multivariate statistics in natural history lies a portal to the heart of developmental complexity ,  a measure called “information” or “non-redundancy.” Here, information is the number of degrees of independence in a multivariate dataset. In development, it is the number of independent factors needed to account for the observed phenotypic-developmental variation. For two measured variables, I = 2 – ρ^2, where I is information and ρ^2 is the squared correlation coefficient. I is maximal and equal to 2 when the correlation is zero and there are two underlying developmental factors. I is minimal and equal to 1 when the correlation is 1 and there is really only a single factor at work. Leigh also gave a multivariate version: I = 1 + (n – 1) (1 – ρn^2), where n is the number of measured variables and (1 – ρn^2) is the mean proportion of each variance that is independent of all the other variables.

So I is a count – albeit on a continuous scale – of independent factors. It is also, therefore, complexity (in one sense). The more independent factors, the greater the dimensionality of the space in which change occurs, and the greater the number of possible phenotypes. Evolutionary biology has long suspected that complexity may be hugely important in evolution, but we have lacked apt measures of it. Leigh’s I provides a measure, allowing us to ask questions, for example, about trends. Is a human more developmentally complex than a reptile? Is there a trend in developmental complexity within this or that group, or over the history of life?

Importantly, I is – unlike certain other measures of complexity – function-free, or adaptation-free. An organism with greater I may or may not be a better adapted one. Also, I is not a measure of “morphological integration” . For one thing, what I measures is not integration but dis-integration. For another, the goal is different: morphological integration is concerned with a range of issues, from the relationship between integration and speciation to the identification of specific developmental mechanisms. But the mission implicit in Leigh’s I is even more general, seeking not actual mechanisms, but a measure of the “diversity” of those mechanisms, the “generative diversity” of the organism.

Interestingly, there is a close connection between I and modern treatments of modularity and evolvability, some containing measures of independence that correspond closely with I . However, the concern in the modern treatment is with the effect of a character’s independence on its ability to respond to selection, not with complexity understood as a variable in its own right.

Variation: genetics, phenotypes and pioneering evo-devo

Leigh was uniquely co-mentored by arguably the greatest microevolutionist (Dobzhansky) and macroevolutionist (Simpson) alive at that time. This provided him with a seamless perspective of the evolutionary process that kept him from falling into traps not always avoided by some of his prominent contemporaries. However, despite having written five papers on Drosophila genetics in top ranking journals, Leigh’s research on the genetics of extant organisms, unlike his other contributions, has not been particularly enduring.

Leigh’s lasting contributions in this area focused on phenotypic rather than genetic variation.  In a series of early papers, Leigh measured selection on phenotypic traits in natural populations, including extinct ones .  Related works explored if wider niches correlated with more variable traits  and reviewed the genetics of variation in paleontology .  While the case studies in this latter paper have been almost entirely superseded by modern works, few of its main conclusions need to be altered. An early statistical paper on measuring multivariate variation and covariation  anticipated later problems arising in the study of morphological disparity , morphological integration, modularity and complexity, as noted above (see also ).  Leigh’s seminal work on fluctuating asymmetry (FA) also exemplifies the depth of his thinking on how phenotypic variation is related to underlying developmental processes .  A bibliographic search reveals about 7990 articles published with this phrase in their titles or abstracts since, much of which Leigh did not approve, because they pursue what he viewed as highly questionable correlations between asymmetry signals and fitness. The fundamental issue Leigh addressed originally is the precision of developmental processes and why natural selection has shaped developmental systems so as to minimize the noise that FA indirectly measures.

It is perhaps surprising that Leigh, the staunch adaptationist , was an early and influential advocate of incorporating development into evolutionary theory, since  much of the early work in evo-devo revolved around developmental constraints as alternatives to adaptation as explanations for evolutionary change.  Leigh’s perspective was however different, taking the view that development should be woven into the fabric of evolutionary explanation.  Leigh’s oft misquoted aphorism “…evolution is the control of development by ecology…”  was meant to point out that development (and ecology) had been short-changed in evolutionary biology.  Much of his earlier work shows an intense interest in the origination of variation through development.  For example, Leigh discussed the implications of dysmorphic incisor growth in rats for the characterization of  Rodentia  . In his analysis of developmental or morphogenetic fields in mammalian teeth , Leigh drew a prescient connection between the developmental field concept and homeotic mutations in Drosophila —decades before the homeobox gene story was revealed.

His combined interest in development and variation also led him to seize the significance of correlations among traits. Rediscovering Olson and Miller (1958), Leigh saw the implications of morphological integration for how developmental processes structure the expression of phenotypic variation .  He succinctly hypothesized that “The tendencies of functionally related structures to be similar in form or adjacent to each other explains developmentally only part of this relationship.  It seems necessary to postulate selection specifically for developmental patterns that affect functional complexes as a whole.” This concept is very close to current ideas on modularity and its importance in evolution, a theme that also runs through his work on serial homology .

Maladaptations: excesses and waste

The self-proclaimed adaptationist not only pioneered evo-devo and estimated that adaption is overwhelmingly prevalent in features of organisms , but also had long been interested in non-adaptations and apparently maladaptive traits  . Expanding his early treatment  on the mechanisms of non-adaptive evolution in a study of female reproduction , Leigh proposed that selection among oocytes explained two seemingly unrelated and maladaptive phenomena. What looks at birth to be i) an inexhaustible number of oocytes dwindles to zero in mid-life, followed by ii) decades of sterility (menopause). The energy used to produce the ill-fated eggs could presumably be used adaptively, and models that propose a fitness advantage to reproductive cessation are unconvincing. Using germ-cell counts across the lifespan, Leigh calculated an exponential decline in oocytes, culminating in menopause. With a constant probability of atresia per day, selection for additional germ cells is relatively ineffective in extending the reproductive life.  Menopause, then, is not an adaptation but a result of a trade-off between cost and reproductive lifespan.

Not just a biologist

Leigh wrote about the nature of interdisciplinary research, the role of laws in explanations, the types of laws that can be found in biology, the role of deduction in scientific reasoning, topics worthy of a professional philosopher  and is often quoted by philosophers of biology. Although other biologists (e.g. Dobzhansky, Mayr, Lewontin) had genuine philosophical interests, Leigh to a unique degree emphasized best the symbiosis between philosophical commitments and scientific hypotheses. Leigh’s philosophical discussions on ultimate processes in nature beyond consensual scientific approaches, include “Three paradigms of evolution” and “Biotal evolutional: manifesto” . Beyond the search for definitional and logical adequateness, his questioning of what is a biological individual and what to make of the fuzzy boundaries of entities expressed the types of ontological concerns that philosophers have been dealing with for centuries. Leigh cared about laws (universal statements that allow for deductions), but also deeply recognized that the role of induction and its relationship to causal inferences must not be minimized .  In going beyond common scientific intuitions to identify the most logically coherent theoretical approach, Leigh was a philosopher and a biologist.

Final utterances

Leigh left us with promising signposts in disparate fields but also many unanswered questions. Numerous portals he opened are still unexplored. The search for causal theory in macroevolution still remains; the full significance of energy in evolution still eludes us; conceptual gaps between neontology and paleontology still run deep. Leigh may no longer be among us, but his paradigms and manifestos remain to inspire many of us in our quest to understand the evolutionary biology.

Acknowledgements

D.W. McShea would like to thank P. Magwene for discussions.

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1. The website Leighvanvalen.com archives, with free access, all of Leigh’s papers and all issues of his journal, Evolutionary Theory.

2. Leigh regularly used this term to underscore the centrality of evolution for biology, and to describe the scope of his research interests. He contrasted the evolutionary "half" with those areas of biology where the focus is on how organisms work, but not on how or why they came to be that way. For Leigh, the evolutionary half includes systematics, comparative biology, ecology, paleontology, behavior, biogeography, population genetics, anatomy, and any other fields where evolution is the underlying theme. See, “Why misunderstand the evolutionary half of biology,” (Van Valen 1982b) for a fuller discussion.