John Maynard Smith Prize
Every year the European Society for Evolutionary Biology distinguishes an outstanding young evolutionary biologist with the John Maynard Smith Prize.
The prize is named after John Maynard Smith (1920 – 2004), eminent evolutionary biologist, and author of many books on evolution, both for scientists and the general public. He was professor at the University of Sussex, UK, Fellow of the Royal Society, winner of the Darwin Medal, laureate of the Crafoord Prize of the Swedish Academy of Sciences, and President of ESEB. See the interview by Robert Wright for an account of his lifelong fascination with evolution, and here for a biography.
The next deadline will be announced in autumn 2019.
Current and previous winners of the JMS Prize are listed below.
Karl Grieshop – I research the role that sex-specific selection plays in the maintenance of genetic variance in fitness, and the maintenance of sexual reproduction. Specifically, I research the capacity for sexually antagonistic selection to maintain stable polymorphisms for fitness throughout the genome, and the capacity for strong (sexually concordant) selection in males to facilitate the purging of mutation load. I did my PhD with Göran Arnqvist at Uppsala University from 2012-2017, utilizing quantitative/statistical genetics and the seed beetle Callosobruchus maculatus. I am currently on a 3-year international postdoctoral fellowship from the Swedish Research Council to work with Aneil Agrawal at the University of Toronto, and Mattias Mannervik at Stockholm University. I continue to research sexually antagonistic polymorphisms for fitness, but I now use Drosophila melanogaster and my approach has broadened to include experimental evolution, genomics, transcriptomics, mathematical modeling, and genome editing.
Karl’s prize will be celebrated at the ESEB congress in Turku, Finland, where he will give the 2019 John Maynard Smith Prize Lecture on “Sexual conflict and the maintenance of genetic variance in fitness“.
Explaining the maintenance of genetic variance in fitness remains one of the most longstanding challenges for evolutionary biology. Mutation-selection balance cannot account for all of the genetic variance observed in nature, meaning that some form(s) of balancing selection must commonly ensue. Sexually antagonistic (SA) selection can generate balancing selection and maintain polymorphisms for fitness throughout the genome, wherein alternative alleles pose opposite fitness effects in the sexes. Despite growing evidence for SA genetic variation, I argue that its role in maintaining fitness variance may still be underestimated. I will review the relevant historical context, focusing on the evidence and perspectives surrounding the role of sex-specific dominance reversal (SSDR) – where the allele that benefits a given sex is also dominant in that sex. I will then present evidence of SSDR underlying SA polymorphisms for fitness throughout the genome of the seed beetle Callosobruchus maculatus, discuss potential molecular mechanisms of SSDR, and provide examples of the phenotypes that mediate SA genetic variation for fitness. Lastly, I will describe an ongoing effort to identify SA polymorphisms (and their dominance properties) in Drosophila melanogaster, and discuss why SA polymorphisms have proven so elusive.
Siobhan O’Brien – ETH Zurich, CH
“Understanding the ecology and evolution of microbial social interactions in a complex world”
Microbes are embedded within diverse communities comprising highly complex networks of social interactions. Consequently, predicting the evolution and ecology of a focal species in a single-species in vitro environment may not be indicative of what is happening in nature. This conundrum is difficult to address – because 1) communities are highly complex and interactions are difficult to decipher in situ, 2) observations from nature are generally correlative and determining causality requires experiments, 3) it is difficult to accurately recreate natural conditions in the lab and 4) many microbes are unculturable under standard laboratory conditions. My research aims to overcome these difficulties, by attempting to bridge the gap between single species in vitro experiments and data collected from natural populations. I will discuss how this approach has provided novel insights into our understanding of microbial communities, in both environmental (heavy metal contamination) and clinical (cystic fibrosis lung infections) contexts.
Amanda Kyle Gibson – Emory University, Atlanta, US
What use is sex?
Over forty years ago, John Maynard Smith inspired one of the outstanding problems in evolutionary biology: the maintenance of sexual reproduction. First, I’ll show that Maynard Smith’s simple model, the two-fold cost of males, holds in a natural system. I combined theory and experimental data to directly quantify the cost of sex in the freshwater snail Potamopyrgus antipodarum. Consistent with Maynard Smith’s prediction, the per-capita birth rate of asexual lineages is at least twice that of sexual lineages. So, in Maynard Smith’s terms: what use is sex? Second, I’ll present tests of the Red Queen hypothesis, which proposes that host-parasite coevolution maintains sex. Observations of a natural population, paired with experimental manipulations, show that coevolution can explain fine-scale spatial and temporal variation in the frequency of sexual snails. Field data spanning a fifteen-year period reveal a dynamic coevolutionary process, with parasites switching to select against sexual reproduction as asexual lineages become rare. Taken together, these results support coevolving parasites in maintaining coexistence of reproductive modes.
E. Keith Bowers – University of Memphis, US
Visit Keith Bowers’ website
Silver spoons, sexy sons, and constraints on sex allocation
One component of sex-allocation theory posits that sons and daughters are differentially affected by early rearing conditions, whereby the amount of parental care received has differing effects on the fitness of males and females. When this occurs, selection is expected to favor offspring sex-ratio adjustment according to anticipated fitness returns. Here, I describe a series of questions related to sex-by-environment effects on the development, survival, and future reproduction of offspring and associated variation in primary offspring sex ratios. What emerges is a pattern of consistent, and persistent, sex-specific effects of natal environmental conditions on offspring, thus favoring the adjustment of offspring sex ratios by mothers. However, increased sensitivity of males to environmental conditions should also contribute to shaping an optimal offspring sex ratio, with implications for the evolution of sex-ratio adjustment.
Matthew Hartfield – University of Toronto, Canada
Mathematical adventures in sex and disease evolution
Mathematical modelling has always played an important role in elucidating evolutionary phenomena. Here, I present an overview of various models I’ve worked on during my career. First, it has been postulated that sexual reproduction is beneficial by recombining genomes, thus recreating optimal genotypes. This hypothesis has faced renewed interest due to the ability to test hypotheses using next generation sequence data. I will show how strong selection for recombination, that can potentially maintain costly sex, appears if acting over hundreds of sites subject to selection. Major benefits to sex and recombination arise through disentangling beneficial mutations from deleterious backgrounds. Finally, I will also discuss my research into disease emergence. Specifically, I investigate how the spread of existing strains hampers the ability of mutated pathogens to emerge, by limiting the available pool of susceptible individuals.
Laurie Stevison – Auburn University, US
The Time-Scale Of Recombination Rate Evolution In Great Apes
We recently completed three linkage disequilibrium (LD) based recombination maps generated using whole genome sequencing of 10 Nigerian chimpanzees, 13 bonobos, and 15 western gorillas, collected as part of the Great Ape Genome Project (Prado Martinez et al. 2013). We also identified species specific recombination hotspots in each group using a modified LDhot framework, which greatly improves statistical power to detect hotspots at varying strengths. Using species specific PRDM9 sequences to predict potential binding sites in hotspot regions as compared to match cold spot regions, we identified an important role for PRDM9 in predicting recombination rate variation in multiple great ape species. While previous research showed that PRDM9 is not associated with recombination in western chimpanzees (Auton et al. 2012), we attribute this lack of signal to higher population level diversity at the PRDM9 locus in this group. Additionally, we show that fewer hotspots are shared among chimpanzee subspecies than within human populations, further narrowing the time scale of complete hotspot turnover. We quantified the variation in the biased distribution of recombination rates towards recombination hotspots across great apes, highlighting similar distributions across great apes with Europeans as an outlier. Further, we found that pairwise comparisons of broad scale recombination rates decay more rapidly than pairwise nucleotide divergence between species. We also compared the skew of recombination rates at centromeres and telomeres between species and show a skew from chromosome means extending as far as 10-15 Mb from chromosome ends. Our study is the first to analyze within and between species genome wide recombination rate variation in several close relatives.
Rich FitzJohn – Macquarie University, AU
What drives biological diversification? Detecting the traits under species selection
Species selection – heritable trait-dependent differences in rates of speciation or extinction – may be responsible for variation in both taxonomic and trait diversity among clades. While initially controversial, interest in species selection has been revived by the accumulation of evidence of widespread trait-dependent diversification. I will present several methods for investigating species selection by detecting the association between species traits and speciation or extinction rates. These methods are explicitly phylogenetic and incorporate simple, but commonly used, models of speciation, extinction, and trait evolution. Using these methods, I will present several examples where traits are correlated with speciation or extinction rates in plants and mammals. All methods have assumptions and limitations, and I will discuss the pitfalls that arise when applying these methods (and the widely used methods that they derive from) to messy biological data. Comparative phylogenetic methods must be used with caution, but allow testing of long-standing hypotheses about causes of variation in biological diversity.
Line Ugelvig – Junior fellowship
Tanja Stadler – ETH Zürich, CH
Looking at the present to learn about the past
Phylogenetic trees of present-day species allow inference of the rate of speciation and extinction which led to the present-day diversity. Classically, inference methods assume a constant rate of diversification, or neglect extinction. I will present a new methodology which allows speciation and extinction rates to change through time (environmental-dependent diversification) as well as with the number of species (density-dependent diversification). Particular attention is paid towards the specific species sampling schemes for incomplete phylogenies.
Using this new framework, I show that mammalian diversification rates are mainly determined by environmental effects; however, I reject the hypothesis of accelerated mammalian evolution following the extinction of dinosaurs at the KT-boundary. The other two considered datasets, birds and ants, reveal density-dependence as the main factor determining diversification rates. In contrast to previous results, the new analyses predict high extinction rates for birds, as well as no major environmental impact on diversification for ants.
The methods can easily be applied to other datasets using the R packages TreePar and TreeSim available on CRAN.
Daniel Matute – Junior fellowship
Rowan Barrett – Harvard University, US
The genetics of adaptation to changing environments
Summary statement: The genetics of adaptation: combining theory, lab and field studies to understand the mechanisms that drive ecological and evolutionary responses to changing environments.
Human activities are resulting in extensive worldwide changes to ecosystems, with both ecological and evolutionary consequences. Understanding the process of adaptation to changing environments requires integrative studies that combine approaches from population genetics, evolutionary ecology and molecular biology. Here, I present theoretical, laboratory and field studies with microbes and fish that help to determine the genetic basis, ecological mechanisms, and evolutionary effects of rapid adaptation to changing environments. The work involves direct measures of natural selection acting at the molecular level, thus providing crucial information on the functional links among genotype, phenotype, and fitness. This research is helping to identify some of the primary mechanisms that are likely to drive adaptation to global environmental change.
Emma Hine – Junior fellowship
Tanja Schwander – Simon Fraser University, US
Evolution of genetic caste determination in social insects
Understanding how a single genome can produce a variety of different phenotypes is of fundamental importance in genetics and developmental biology. One of the most striking examples of phenotypic plasticity is the female caste system found in ants and other eusocial insects, where different phenotypes are associated with reproduction (queen caste) or helping behaviour (worker castes). A long-standing paradigm for caste determination was that female eggs are always totipotent with the important morphological and physiological differences between queens and workers stemming solely from a developmental switch during the larval stage under the control of nutritional and other environmental factors. However, there are an increasing number of examples showing genetic components to caste determination as well as maternal effects influencing the developmental fate of females. I will present a broad overview of the studies providing strong direct and indirect evidence for a genetic component to caste differentiation and discuss factors that may have led to the evolution of genetically hardwired caste systems. In addition, I will argue that a purely environment- controlled caste system is very difficult to demonstrate and probably unlikely to occur in genetically heterogeneous societies. Detailed molecular analyses and breeding experiments are likely to uncover additional cases of genetically-determined queen and worker determination and various degrees of genetic predisposition towards a particular caste.
Ben Sadd – Junior fellowship (WiKo Report
Andy Gardner – University of Oxford, UK
The evolution of spite
Spite, altruism’s neglected ugly sister, is the most mysterious and controversial of the four social behaviours. How can an individual be favoured to harm itself and its social partners? Hamilton’s rule, which was devised in order to explain altruistic behaviours, has a darker side that reveals when spite will be favoured. Specifically, it requires that the spiteful actor and its victim be negatively related. I develop theory for the evolution of spite in competitive environments, and show that increasingly strong local competition can favour spiteful behaviour. Application of the theory to chemical warfare in microbes and suicidal sibling rivalry in parasitoid wasps leads to novel predictions for parasite virulence and sex allocation theory. I discuss the semantics of spite and ambiguities in the standard classification of social behaviours.
Daven Presgraves – University of Rochester, US
Speciation genes & selfish genes in Drosophila.
Speciation occurs through the evolution of any of several forms of reproductive isolation, including the intrinsic sterility or inviability of hybrids. These hybrid fitness problems are caused by negative epistatic interactions – new alleles that evolve in one species are sometimes incompatible with alleles at interacting loci from related species. Relatively little is known about the identity and function of such “speciation genes” or about the evolutionary forces driving their divergence. I will present results from a large, fine-scale genetic analysis of loci causing hybrid inviability in Drosophila. The first of these genes to be identified encodes Nup96, an essential protein component of the nuclear pore complex (NPC). I will show that the functional divergence of Nup96, and several other interacting Nup proteins, was driven by adaptive evolution. I will then discuss how this positive selection may be a consequence of genetic conflict mediated by the NPC.
Patricia Beldade – University of California at Irvine, US
The genetic basis of phenotypic variation: evolution and development of butterfly wing patterns.
Heritable phenotypic variation is the “raw material” of evolution by natural selection, and understanding the mechanisms that generate such variation has become a fundamental challenge for contemporary evolutionary biology. In recent years, evolutionary developmental biology has encouraged a change of focus from the sorting of phenotypic variation by selection to the production of that variation through development. The colour patterns decorating butterfly wings provide ideal material to study the reciprocal interactions between evolution and development in this process. They are visually compelling products of selection, often with a clear adaptive value, and are also amenable to a detailed developmental characterization at different levels. We studied different aspects of the process of generation of variants in Bicyclus anynana eyespot patterns. Results will be discussed of experiments where we have used artificial selection to explore the potential for changes in eyespot size phenotypes, which were thought to be constrained by the properties of butterfly wing pattern development. We also report on experiments aimed at identifying the actual genes involved in the response to selection. Our results show that a combination of approaches from evolutionary and developmental biology used to study the patterns of colour on butterfly wings can greatly contribute to understanding how evolutionarily relevant variation is generated.
Alexander Badyaev – Auburn University, US
Paradox of rapid evolution of sexual size dimorphism: the role of ontogeny and maternal effects.
In the summer of 1939, a group of 40-50 house finches Carpodacus mexicanus collected in southern California was released from a pet store in New York City. In the subsequent 62 years, this introduced population has undergone tremendous expansion, spreading across the eastern U.S. and south-eastern Canada and increasing to an estimated 1.3 billion birds. This expansion of ecological range was accompanied by rapid divergence in sexual size dimorphism among new populations. We show that the observed divergence in morphology were caused by population differences in patterns of natural selection acting over the lifespan of both sexes. This represents an apparent paradox of rapid independent evolution of each sex in traits for which there is no sex-biased genetic variance in adults. We show that correlated selection on growth trajectories of males and females in combination with persistent and strongly sex-biased maternal effects can account for the observed adaptive divergence in sexual dimorphism among newly-established populations of the house finch.
Nicolas Galtier – University of Edinburgh, UK & University Montpellier 2, FR
Non stationary models of nucleotide substitution and the evolution of base composition.
Base compositions (A-, C-, G- and T-percent) are highly variable among genes and genomes. Heterogeneous base compositions have been observed in most taxonomic groups sampled, for organellar or nuclear genomes, in coding and non-coding regions. Base composition has some functional implications: depending on the organism, it relates to codon usage, gene density, resistance to high temperature. Observing unequal base compositions between genomes or between homologous genes implies that distinct lineages have undergone distinct evolutionary processes. This raises several interesting questions. First, one may wonder about the robustness of DNA sequence analysis methods – and especially phylogenetic inference methods when the base composition varies between compared sequences. Secondly, the history of diverging base compositions deserves attention: what were the ancestral states, which lineages experienced severe compositional changes? Finally, the mechanisms of compositional divergence are unknown in most cases: what are the evolutionary forces that underlie the observed changes in base composition? Is natural selection acting to shape genomic base compositions, or is the variation between genomes mainly due to variable mutation processes?
These problematics instantiate the dual goal of molecular evolution, namely (i) recovering the history of species and populations through that of their genomes, and (ii) understanding better the structure and function of genomes thanks to the evolutionary perspective. The above questions are addressed thanks to a non-homogeneous, non-stationary model of DNA sequence evolution, allowing diverging GC-content in time and between lineages (Galtier & Gouy 1995, 1998). Maximum-likelihood analyses based on this model allow to (i) correctly estimate phylogenies in case of variable GC-content between sequences, and (ii) estimate ancestral base compositions. The latter possibility is applied to ribosomal RNA sequences from species sampled in all three domains of life (Galtier et al. 1999), yielding evidence that the last universal common ancestor was not a thermophilic organism.
Galtier, N., and Gouy, M. 1995. Inferring phylogenies from sequences of unequal base compositions. Proc. Natl. Acad. Sci. USA. 92: 11317-11321.
Galtier, N., and Gouy, M. 1998. Inferring pattern and process: maximum likelihood implementation of a non-homogeneous model of DNA sequence evolution for phylogenetic analysis. Mol. Biol. Evol. 15: 871-879
Galtier, N., Tourasse, N.J., and Gouy, M. 1999. A non-hyperthermophilic ancestor to extant life forms. Science 283: 220-221.
Marie-Charlotte Anstett – CNRS-CEFE, FR
Facilitation and constraints in the evolution of mutualism?
Parasitism is the ancestral state of most mutualisms. What kinds of traits facilitate the transition from an antagonistic to a mutually beneficial interaction? The only well formalised and tested scenario for the origin of mutualism is based on the evolution of vertical transmission of parasites (from parents to offspring Yamamura, 1996), which leads to reduced virulence and sometimes to the evolution of mutualism. However, this scenario can apply only to symbiotic mutualisms, and even these include examples in which vertical transmission does not occur. For these, formalised models are lacking. What other kinds of traits facilitate the evolution of mutualism? Can we identify traits, maintained by selection on other functions that independently in different lineages acquire the same novel function in a particular type of mutualism? If such “pre-adaptations” exist, what factors intervene to alter the selection pressures acting on them and shape them as new adaptations? How recurrent and predictable is the evolution of mutualism?
Small differences in traits already present at the origin of the mutualism may lead to differences in how the mutualism functions and how it evolves. “Constraint” is the flip side of “pre-adaptation.” While constraints are usually envisaged to limit the range of evolutionary possibilities, constraints may also open evolutionary pathways that are otherwise not possible. For some mutualisms, evolutionary stability appears to be based on a co-evolutionary equilibrium between trait values for the two mutualists. In other cases, however, the interaction appears to be stabilised by constraints imposed by pre-existing traits of one species that the associated species cannot evolve to overcome. These points will be developed using as examples the fig/ fig wasp pollination mutualism and protective ant/plant interactions.