Stand Alone Conference of the American Society of Naturalists
Asilomar Conference Grounds, Pacific Grove, California, 5-9 January 2018
Symposium II: 150 Years Of The American Naturalist
Sunday, 7 January 2018, 1:00-5:30 PM & Monday, 8 January 2018, 1:00-5:30 PM
The American Naturalist is the oldest scientific journal published in North America. Over its 150-year history, the journal has had a huge impact on how we understand the natural world. To celebrate the journal’s past impact, and chart its current course and future, we will hold a symposium at the Asilomar meeting, on the afternoons of January 7 and 8. Rather than organizing the symposium around a single theme, we will showcase some of the breadth of ideas published in the journal. Each talk will highlight one or more influential past papers published in The American Naturalist. The talks will trace the history of how the classic paper(s) have affected the field in general, the speaker’s own work, and the future of the field. We solicited applications for the talks, placing particular weight on attracting proposals by junior researchers. Applications were reviewed by a committee.
Sunday afternoon, 7 January 2017
Symposium: 150 Years of The American Naturalist
Organizers: Daniel I. Bolnick & Judith L. Bronstein
|S1||1:00||Joel Kingsolver||Levene and polymorphism|
|S2||1:30||Maria Rebolleda-Gomez||A relational view of life: moving past biological individuality|
|S3||2:00||Lukas Keller||Inbreeding: origins, tools, and tasks|
|S4||2:30||Arvid Ågren||The origin of the gene's-eye view of evolution|
|3:00||Coffee Break - Refreshments in Chapel|
|S5||3:30||Aleeza Gerstein||Experimental evolution and test tube naturalism as key innovations to study repeatability and the genetic basis of adaptation|
|S6||4:00||Julia Saltz||How to love and hate your neighbors: why animals seek out competitors|
|S7||4:30||Ambika Kamath||A broader legacy of Orians 1969|
|S8||5:00||Alex Jordan||Whither the Naturalist, in the age of computational ethology?|
Monday afternoon, 8 January 2018
Symposium: 150 Years of The American Naturalist
Organizers: Daniel I. Bolnick & Judith L. Bronstein
|S9||1:00||Marjorie Weber||Macroevolution of plant defense: a letter from the future to a pioneering woman in science|
|S10||1:30||Allison Barner||The missing theory of species co-occurrence in ecology|
|S11||2:00||Tadashi Fukami||John Sutherland's legacy and the current effort to embrace historical contingency in ecological and evolutionary community assembly|
|S12||2:30||Ophélie Ronce||Metapopulation Genetics and the evolution of dispersal: an homage to slow science and to a unique scientific character, Isabelle Olivieri|
|3:00||Coffee Break - Refreshments in Chapel|
|S13||3:30||Yoel Stuart||Parallel evolution through 150 years ofThe American Naturalist|
|S14||4:00||Stephen de Lisle||Ecological character displacement: from between to within species|
|S15||4:30||Erik Svensson||Evolution along latitudinal gradients: homage to Kirkpatrick and Barton|
|S16||5:00||Mathew Nielsen||Misinformation in a new climate: the role of reliable information in the evolution of phenotypic plasticity|
Building a Theory of Adaptation in Variable Environments: Levene (1953)
With a thousand words and a bit of algebra, Howard Levene (1953) produced a cornerstone of the theory of adaptation in heterogeneous environments. His concise and elegant Letter to the Editor first demonstrated how environmental variation can maintain genetic polymorphism in a population, and why the arithmetic mean can be the wrong metric of ‘average’ fitness in variable environments. In a series of American Naturalist papers in the 1960s, Richard Levins and collaborators built on this cornerstone to develop a theoretical framework for understanding adaptation in heterogeneous environments, exploring spatial and temporal variation, fine- and coarse-grained environments, and the roles of genetic polymorphism and phenotypic plasticity for adaptation.
In the decades since Levene and Levins, the consequences of environmental variation for genetic and fitness variation, adaptation, and evolutionary responses have become a central component of evolutionary biology. I will discuss how these papers influenced my own research career, and describe how they continue to inform current research programs on adaptation to novel environments and biological responses to climate change. I will also ask: What is the role of simple and ‘unrealistic’ models in our current era of big data, immense computational power, and large-scale research collaborations?
A Relational View Of Life: Moving Past Biological Individuality
Forty years ago Daniel H. Janzen asked: “What are dandelions and aphids?” to point out how evolutionary individuality of clonal organisms does not necessarily match our common conceptions of individuality. Botanists have long recognized that vertebrate-centric notions of individuality fail to describe modular organisms. Recent advances in microbiology that challenge our ideas about the ubiquity and importance of microbes in our bodies; coupled with the recognition that biological hierarchies are themselves the result of evolutionary process, has fueled renewed interest in the old question of what counts as an individual in biology. A central idea in these discussions has been the analysis of Richard Michod of the role of multi-level selection on transitions of individuality. Janzen and Michod emphasized the significance of life-histories and particular ecological conditions in the evolution of individuality, but the ecological drivers of individuality are still understudied. The emphasis has been on identifying the sort of units that can evolve by natural selection. Instead, I want to argue that there are many ways of parsing biologically relevant individuals. I want to move away from the question, “What is an individual?” toward an exploration of the ecological variables affecting the degree to which entities might act as evolutionary individuals. In this talk I will discuss the historical contexts for these two papers and the ways the individuality question has changed over time and finish by briefly discussing some future directions and emerging systems.
Inbreeding: Origins, Tools, and Tasks
Animal and plant breeders have used inbreeding for centuries. In a key series of papers in The American Naturalist, Raymond Pearl (1913, 1914, 1917) first applied Mendel’s laws to understand and quantify inbreeding and its effects. However, it was Sewall Wright’s seminal 1922 paper, also in The American Naturalist, that gave us a fully mechanistic understanding of inbreeding and its genetic consequences and the tool of path analysis for analyzing inbreeding in any pedigree. These breakthroughs let loose a remarkable sequence of theoretical and empirical papers on inbreeding and its consequences leading Richard Lewontin (1965) to remark that “every discovery in classical and population genetics has depended on some sort of inbreeding experiment.” Inbreeding research accelerated again in the late 20th century with growing interest in mating system evolution and the rapid development of molecular and, later, genomic markers. We can now measure inbreeding without pedigrees and probe deleterious mutations directly. Interestingly, genomic approaches have also resurrected Fisher’s 1949 theory of junctions. We have pursued inbreeding research since the mid 1990s and late 1970s, respectively. Our work on the role of inbreeding in evolutionary and conservation biology was inspired by the seminal work of Wright, leading us to publish our highly cited review paper in 2003. Our empirical and conceptual work on inbreeding continues and focuses on efforts to better understand how purging and fixation shift the architecture of the genetic load and how inbreeding affects individual and population fitness.
Hamilton 1963 And The Origin Of The Gene's Eye View Of Evolution
Darwin’s original theory of evolution by natural selection is focused on individual organisms as the central unit of selection. While Bill Hamilton’s short 1963 paper “The Evolution of Altruistic Behavior” is rightly remembered for introducing what we now refer to as Hamilton’s rule, it was also the starting point of something more radical: the gene’s-eye view of evolution. Moving away from the individual organism and instead focusing on gene survival opened up a whole new approach to the study of natural selection. One key way in which the gene’s-eye-view heuristic revolutionized evolutionary biology was that it helped unify the study of conflict and cooperation. Hamilton taught us that regardless of whether we are studying parent-offspring conflicts in animals or transposable element proliferation in plants, we are best off asking ourselves: if I were a gene, what would I do? Along with this comes a shift in formal theoretical modelling, where individual and genes can be modelled quite differently. In this talk, I will first trace how the gene’s-eye view has developed over the past half-century. Next, taking a starting point in studies of selfish genetic elements and genomic conflicts, I will review how this perspective has helped connect empirical observations from disparate parts of social evolution. Finally, I will explore how Hamilton himself over the years moved between this gene’s-eye perspective and his organism-centred inclusive fitness models, and how this reveals a long-standing tension in evolutionary theory over what the central unit of explanation should be.
Experimental Evolution A La Lenski
Lenski, R.E., M.R. Rose, M.R., S.C. Simpson, and S.C. Tadler. 1991. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. American Naturalist 138: 1315-1341.
Lenski et al. (1991) describes the start of a now-famous long-term evolution experiment (“the LTEE”): 12 populations of Escherichia coli initiated from the same ancestor were evolved in minimal medium by batch culture for 2000 generations. The LTEE has since continued (the lines just surpassed generation 67 000) and an entire sub-discipline of experimental evolution using diverse taxa across the kingdoms has sprung forth. The LTEE and related experiments enable the researcher to be a test tube naturalist, and to observe and quantify the genotypic and phenotypic variation that arises naturally. We have used similar experiments with fungal microbes to examine the influence of ploidy on adaptation. We uncovered and defined the phenomenon of ‘ploidy drive’, having demonstrated that diverse species tend to asexually revert back to their baseline ploidy level within 10-100s of generations. We have also shown that both ploidy and the environment can directly impact the effect of single mutations that confer a benefit to the antifungal drug nystatin in Saccharomyces cerevisiae: the mutations have a greater effect in haploids than diploids, their dominance properties are inconsistent across environments, and their epistatic interactions are environmentally dependent. The LTEE and related experiments, coupled with affordable whole genome resequencing, continue to produce results on the cutting edge of knowledge about the factors that constrain and promote how organisms adapt to their environment.
How To Love And Hate Your Neighbors: Why Animals Seek Out Competitors
I will discuss the 1988 paper “Conspecific Attraction and Aggregation in Territorial Species” by Judy Stamps, which was published in Am Nat almost exactly 30 years before the ASN 2018 meeting. The paper describes a field experiment on the territorial establishment decisions of juvenile Anolis lizards, finding, for the first time, that animals choose to establish next to other occupied territories, eschewing suitable (perhaps even more resource-rich) available territories that were farther away from conspecifics. This simple result has profound implications. For behaviorists, the paper contributed to a more nuanced view of sociality, in which territoriality, aggression, and conspecific attraction are all compatible behaviors that represent affiliative and antagonistic components of a single relationship. Further, the paper contributed to launching a now-thriving subfield of social information use. For ecologists, the paper demonstrated that animals may actively seek out, rather than avoiding, competitors. Most importantly for my own work, the paper showed that animals play an active role in determining the social and ecological environments that they experience, and that territoriality, aggression, and social attraction can be conceptually united as examples of social spacing mechanisms. My work has focused on the discovery and implications of genetic variation in these social spacing mechanisms; I have shown that such genetic variation has important consequences for the quantitative genetics and evolution of plastic traits. Some of these findings have been published in Am Nat (Saltz & Foley 2011, Foley, Saltz et al 2015). My ongoing and future work continues to focus on the tension between social attraction and social conflict and how these processes scale to produce heritable environments and to influence evolution.
A Broader Legacy Of Orians 1969
Orians (1969)—“On the evolution of mating systems in birds and mammals”—was crucial for framing the hypothesis that resource distributions determine animal mating systems, a widespread idea whose generality remains unevaluated. I began reviewing empirical evidence for this hypothesis, a project that was too ambitious to finish. However, beginning it led me to realize that Orians’ (1969) influence extended beyond birds and mammals. Key papers on Anolis lizards’ mating systems—Schoener and Schoener (1980) and Ruby (1984)—cite Orians’ (1969) description of mammals, where the absence of male parental care is linked to polygyny. This reference supported the description of anoles, which lack parental care, as territorial and polygynous. But this behavioral description of Anolis mating systems is inconsistent with recent genetic data that has repeatedly revealed that females mate with multiple males. By tracing behavioral evidence for territoriality and polygyny in a century of research on Anolis lizards, I found that early studies concluded that anoles are territorial based on flimsy evidence, leading subsequent studies to implicitly and explicitly assume territorial behavior, leaving them unlikely to detect behaviors that could facilitate polyandry. My empirical work on Anolis sagrei, which explicitly avoids assuming territoriality, reveals behavior consistent with female multiple mating. Such erratic and contingent research trajectories are likely not unique to anoles, and could explain similar inconsistencies between behavioral and genetic descriptions of mating systems in other animals. Orians’ (1969) legacy may therefore include more unanswered questions about the nature of animal mating systems than previously anticipated.
Whither the Naturalist, in the age of computational ethology?
For decades, studies of male color and ornamentation in the guppy (Poecilia reticulata) have generated great insight into the evolutionary process acting on secondary sexual traits. In particular, our understanding of the effects of predation, signaling environment, and competition has been boosted by the research on Trinidadian guppies, much of it published in The American Naturalist. The series of papers by Reznick et al. “Life History Evolution in Guppies” appearing in Am Nat over the past 20 years, as well as classic papers like Endler’s 1992 Am Nat piece “Signals, signal conditions, and the direction of evolution” are now keystone contributions to our understanding of sexual selection in natural contexts. These studies have been followed by regular subsequent pieces in Am Nat on guppy behaviour and evolution (Kodric-Brown, Gordon, Cole, Zajitschek, and many others), generating a wonderful body of work in the journal on this topic. One of the primary messages of these papers, and certainly that of Endler’s focus piece, is that the numerous interacting aspects of traits, signalling environments, behaviour, and natural history can generate “a bewildering diversity” of effects on secondary traits (Endler 1992). Effectively analysing this diversity requires novel technologies, and work in my group uses cutting-edge computational techniques to provide quantitative analyses of the interaction between ornamentation and behaviour in guppies. We use deep convolutional neural networks to identify ornamental traits and measure how they interact in visual space. In this way, we can identify trait combinations that may be undetectable using standard statistical or observational methods, and ask how these traits combine to influence mate choice processes. We then use behavioural decomposition (e.g. Berman 2013) to quantify the different elements of courtship display employed by males in different contexts. Finally, we use fully immersive 3D virtual reality environments to project both natural and generated ‘optimal’ ornament combinations onto artificial males performing different courtship behavioural patterns. We then measure how ornament and behaviour interact, how certain aspects of male ornaments may be accentuated through body posture interacting with the female visual system and light environment, and what effect this has on mate choice behaviour. By employing these high-end computational approaches, we have the opportunity to make sense of this bewildering diversity and help bring this series of studies appearing in The American Naturalist into the 21st century.
Macroevolution Of Plant Defense: A Letter From The Future To A Pioneering Woman In Science
More than 120 years ago, a female scientist named Helen Cecilia de Silver Abbott published an article in The American Naturalist introducing the then-radical idea that plant chemistry should be considered in light of macroevolution. Since her publication, the comparative study of plant defense has blossomed into a massive and highly productive field. The study of plant defense evolution has resulted in major research strides in coevolution, adaptation, and links between evolution and ecology. However, Abbott’s contribution has now been largely forgotten. This talk will pay homage to Abbott’s groundbreaking but largely overlooked paper, “Comparative Chemistry of Higher and Lower Plants,” spotlight Abbott’s important contribution to the field of chemical ecology, give her a much-deserved shout-out as an important early woman in science, and take stock of the incredible insights the field of comparative plant defense has produced since her time.
The Missing Theory Of Species Co-occurrence In Ecology
Special issue of The American Naturalist: “A round table on research in ecology and evolutionary biology”, American Naturalist 122, number 5. Includes papers by: Jonathan Roughgarden, James Quinn, Arthur Dunham, Catherine Toft, Patrick Shea, Daniel Simberloff, Donald Strong, Joseph Connell, George Salt.
In 1983, The American Naturalist published a special issue, the innocuously titled “A Round Table on Research in Ecology and Evolutionary Biology.” Embedded in this broad title was an attempt to address a roiling debate in ecology at the time: can the spatial arrangement of species on a landscape be used to infer the underlying community structuring mechanism? Specifically, can co-occurrence patterns signal underlying competition? The seven papers in this issue magnify the surprisingly expansive questions at the heart of this debate through a profound exploration of ecology, evolution, inference, and philosophy. In recent years, similar competition-inference methods have resurfaced into prominence, as ecologists increasingly estimate species interactions using large databases of spatial and temporal occurrences. However, the important debates of the 20th century have been largely ignored in the rapid adoption and current widespread implementation of new machine learning and network inferential methods. Further, foundational concepts shaped through debate have significant bearing not only on the inference of species interactions, but also on the many pattern-process inference methods that dominate modern community assembly theory. In this symposium, I will trace the origins of the idea that species interactions can be inferred from spatial patterns, highlighting the role of this often-overlooked 1983 special issue. Further, I will explore the modern landscape of these debates about pattern-process inference, highlighting empirical ground-truthing, simulation models, and new theoretical frameworks.
John Sutherland’s Legacy And The Current Effort To Embrace Historical Contingency In Ecological And Evolutionary Community Assembly
Sutherland’s (1974) experiment with marine fouling communities is one of the first that tested the hypothesis that ecological communities develop differently depending on the timing and order in which species arrive. The importance of such historical contingency had been articulated mathematically by Lewontin (1969), but it is Sutherland’s work that made the radical idea widely discussed against the then dominant view that community development is largely deterministic. This paper and several others in The American Naturalist (e.g., Connell and Sousa 1983, Drake 1991) have inspired me to study community assembly over the past 15 years. In this literature, however, historical idiosyncrasies, known today as priority effects, are usually viewed as a nuisance that hinders progress in community ecology. In our current research with plant and microbial communities, my colleagues and I are working to argue that this view is misguided and show how we can embrace historical contingency toward a general theory of community assembly. This effort involves identifying the ecological and evolutionary conditions under which history matters and those under which it does not. Key to this current research is the expansion of Sutherland’s original focus on multiple stable points to consider four overlooked aspects of community assembly that can be sensitive to historical contingency: compositional cycles, not just fixed stable points; long-term transient states, not just stable equilibria; eco-evolutionary and macroevolutionary dynamics, not just ecological population dynamics; and the function, in addition to the structure, of communities, and the feedback between the two.
Metapopulation Genetics and the evolution of dispersal: an hommage to slow science and to a unique scientific character, Isabelle Olivieri
In 1995, Isabelle Olivieri, Yannis Michalakis and Pierre-Henri Gouyon published in the American Naturalist a theoretical paper studying the evolution of dispersal rates in a metapopulation. In this paper, they focused on the ecological and evolutionary consequences of demographic disequilibrium generated by local extinction and recolonization. They showed that genotypes with high dispersal ability were selected at the level of the metapopulation, abundant in recently funded populations, but counter-selected within established populations, their frequency declining with time since foundation. This was described as a metapopulation effect. Today, this is still one of the most cited model about dispersal evolution. The 1990's were an era when the studies of metapopulations bloomed, deeply modifying our understanding of many ecological processes. This paper clearly showed that a metapopulation perspective could also deeply alter our understanding of evolution. I will show how this paper opened roads for an entirely new research programme for Isabelle Olivieri and others interested in the evolution of dispersal and more generally of life histories. I will also discuss how these ideas originally emerged and the long ten years it took to get the paper published in the American Naturalist. By doing so, I will reflect on the creativity of Isabelle Olivieri and how it emerged from her non-standard ways of doing science.
Toward A Continuum View Of Parallel Evolution
Those instances where independent species evolve similar phenotypes in similar environments—parallel evolution—are heralded in evolutionary biology as strong evidence for natural selection. Indeed, the most parallel traits in the most convergent species furnish textbook cases of adaptation (e.g., Darwin’s finches, rift lake cichlids). However, even in lineages famous for convergence, unique features of evolution often outnumber shared features. In anoles, for example, non-ecomorph diversity far exceeds ecomorph diversity. What can one make of this non-parallel diversity? What about the evolutionary process might be revealed by thinking of parallelism not as a binary phenomenon for selected traits, but rather as a quantitative continuum for multiple traits? Here, through 10 papers from the past 150 years of The American Naturalist, I trace the idea of ‘parallelism’ to ask whether and when the binary view of parallel evolution has been favored over the continuum view. I then report an empirical example from my work with lake-stream stickleback that takes the latter approach. Across 16 lake-stream pairs, for >80 traits, I find that the direction and magnitude of lake-stream phenotypic divergence varies depending on trait and population examined. To explain these deviations from parallel evolution, I investigated environmental and genetic variation among the 16 pairs, and inferred that non-parallel divergence in lake-stream stickleback arises through both adaptive and non-adaptive processes. This result underscores the benefits of embracing both unique and shared features of evolution in a single analytical framework.
Ecological Character Displacement: From Between To Within Species
Resource competition provides an intuitively appealing explanation for the origins of diversity, because co-occurring lineages with similar niches ought to evolve divergence in ecologically-relevant morphology (ecological character displacement, ECD). Yet decades of debate, often unfolding across the pages of Am Nat, suggests a universal role of competition cannot be assumed. Schluter and McPhail’s paper represents one critical turning point in studies of competition and ECD. They set forth criteria for empirical demonstration of ECD between species in the wild, and obtained such evidence from stickleback. The paper is influential by clarifying an approach to unambiguously assess the importance of competition in driving evolutionary change, and by setting the bar for such tests. My interest in this classic paper comes from a slightly different angle: how do we explain the evolution of ecological differences within species, and particularly between the sexes? In theory, sexual dimorphism in ecologicallyrelevant morphology, such as head shape in the newts I study (Fig 1), could be the outcome of intraspecific ECD. Using the literature on ECD between species as a guide, I proposed a framework for testing ecological causes of sexual dimorphism directly. My work has shown intraspecific competition can drive sexually-antagonistic selection, and that this within-species ECD may play an important role in ecological speciation across the genus of eastern newts. Embracing the idea that ECD may act alongside other causes of sexual dimorphism, such as sexual selection, suggests exciting scope for connecting ecology with evolution of sex roles, with important consequences for diversification.
Evolution Along Latitudinal Gradients: Homage To Kirkpatrick And Barton
This model predicts maladaptation at the range limits in contrast to adaptation at the core. Maladaptation at range limits arise because of asymmetric gene flow from centre to periphery. Peripheral populations at range margins are thus predicted to be sinks that are prevented from reaching their local optima because of maladaptive gene flow. This model has attracted considerable interest (688 ISI-citations), both because of its principal importance for fundamental evolutionary questions about limits to adaptation and because of concerns about ongoing climate change. Many species are now rapidly changing their ranges and move northwards because of global warming. In my own research, which takes place in Sweden, the Kirkpatrick-Barton model is both of local interest and principal importance as Fennoscandia is rapidly being invaded by an increasing number of southern European species that are establishing new northern populations. In this talk, I will discuss how latitudinal gradients and temperature influence ecological and evolutionary dynamics in a group of insects (Zygoptera: damselflies) that we have studied in my lab for almost two decades now. I will discuss how sexual conflict and sexual selection change with latitude, leading to clines in sexual phenotypes, the evolution of heat and cold tolerance along latitudinal gradients and the loss of premating isolation at range limits.
Misinformation In A New Climate: The Role Of Information In The Evolution Of Phenotypic Plasticity
Richard Levins (1963) developed a basic model for the evolution of plasticity as part of his broader theoretical work during the 1960s on evolution in varying environments. In doing so, he made a critical point: plasticity’s adaptive value depends on the ability to reliably predict the future environment from the developmental one. As plasticity theory developed over the subsequent decades, however, this environmental constraint was often ignored in favor of focusing on genetic constraints to plasticity. Fortunately, thirty years later, Nancy Moran (1992) revisited Levins’ work and the role of reliability in plasticity. She formalized Levins’ insight in the context of contemporary plasticity theory and provided clear predictions for the evolution of plasticity. I first read Moran’s work early in graduate school, and her distinction between cues and the selective environment has become a critical part of my own research on plasticity. Today, the reliability of cues has only become more relevant to plasticity because of the cue-environment mismatches created by anthropogenic change, particularly climate change (e.g. Mills et al. 2013). In particular, many animals use photoperiod as an indirect cue to predict seasonal temperature variation, but it is also the one variable climate change can’t alter. This has created exactly the kind of difference between the cue and the selective environment Levins and Moran discussed. By comparing contemporary reaction norms to specimens from natural history collections for a photoperiod-sensitive butterfly, I am now applying their predictions to determine whether evolution has been able to keep up with the misinformation created by climate change.