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Recent Advances in Ecological Genomics: From Phenotypic Plasticity to Convergent and Adaptive Evolution and Speciation Christian R. Landry and Nadia Aubin-Horth

Abstract

Biological diversity emerges from the interaction between genomes and their environment. Recent conceptual and technological developments allow dissecting these interactions over short and long time-scales. The 16 contributions to this book by leaders in the field cover major recent progresses in the field of Ecological Genomics. Altogether, they illustrate the interplay between the life-history and genomic architecture of organisms, how the interaction of the environment and the genome is shaping phenotypic variation through phenotypic plasticity, how the process of adaptation may be constrained and fueled by internal and external features of organisms and finally, how species formation is the result of intricate interactions between genomes and the ecological conditions. These contributions also show how fundamental questions in biology transcend the boundaries of kingdoms, species and environments and illustrate how integrative approaches are powerful means to answer the most important and challenging questions in ecology and evolution. Keywords

Phenotypic plasticity • Ecological genomics • Life history • Speciation • Adaptation

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Introduction to Ecological Genomics

One of the major challenges in biology is to connect genotypes to phenotypes and to identify the ecological and demographic parameters C.R. Landry () • N. Aubin-Horth Département de Biologie, Institut de Biologie Intégrative et des Systèmes, Université Laval, 1030 Avenue de la Médecine, Québec, QC G1V 0A6, Canada e-mail: [email protected]

that have shaped genotype frequencies in natural populations (Pavey et al. 2012). Meeting this challenge requires the use of integrative approaches, as different techniques and combination of disciplines are needed to understand processes that act at different levels of organizations, from ecosystems to genes. These integrative approaches have given rise to the field of ecological genomics (Feder and Mitchell-Olds 2003). The chapters contributed to this book reflect the most recent and exciting progress in this young field of research.

C.R. Landry and N. Aubin-Horth (eds.), Ecological Genomics: Ecology and the Evolution of Genes and Genomes, Advances in Experimental Medicine and Biology 781, DOI 10.1007/978-94-007-7347-9__1, © Springer ScienceCBusiness Media Dordrecht 2014

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C.R. Landry and N. Aubin-Horth

The New Synthesis

As a second year graduate student and a new postdoc at Harvard University, we registered to a Gordon Research Conference in 2003 that was taking place in nearby New Hampshire. The conference was the inaugural edition of the “Evolutionary & Ecological Functional Genomics” meeting that takes place biyearly ever since. Because of the limited access to genomic resources for most species, major questions asked at the time were “what are good species in ecological genomics”? and “how can we balance the tradeoff between the ability to perform genomics experiments and the interest of the ecological problem to be investigated for a particular species”? This book demonstrates that we are moving ahead from the preoccupations of what species to choose in ecological genomics. Questions have reached another level, where available genomics tools can be applied to virtually any species, and the range of questions one can ask is virtually unlimited. This book is organized around 16 chapters contributed by leaders in the field and covers three major subjects of prime interest in ecological genomics. The first three chapters illustrate how lifehistory and mating systems can impact or can be influenced by patterns of genomic variation. First, Vincent Castric and colleagues use the diversity of plant mating systems to illustrate how life-history transitions can impinge on plant genomic architecture and diversity and how genomic architecture and physiological features may in turn affect these transitions. This field of research is a particularly rich one in ecological genomics as it is based on strong theoretical predictions, to which are combined very well documented molecular underpinnings of reductive mechanisms. In the third chapter, Paul Magwene examines the role of life-history traits on patterns of genomic variation in budding yeast on a much shorter time scale. The budding yeast is one of the most studied organisms in the laboratory and it has recently become an excellent model as well in ecological genomics (Landry et al. 2006). Its

mode of reproduction has intrigued geneticists for several years because although there is ample opportunity for inbreeding by mating between mother and daughter cells, natural isolates of the budding yeast are often heterozygous at many molecular markers. Here, Magwene reviews these concepts and the main hypotheses that have been put forward to explain these observations, and shows how genome-wide analysis of genetic variation can be used to test these models. Finally, Jean-Baptiste Leducq examines how life-history styles modulate or correlate with the architecture of genomes, using fungi as models. Because most fungi have genomes of limited sizes, a large number of fungal genomes have been fully sequenced or are underway, such that they offer unique opportunities to test hypotheses regarding the relationship between genome organization and ecological traits. Leducq reviews these studies and also many others that have examined the evolutionary ecological genomics of fungi on shorter time scales, such as during experimental adaptation and speciation. The second part of the book focuses on one aspect of biological diversity that can hardly be explained from the patterns of genomic variation alone, the diversity that emerges from the interaction between a given genome and its environment. In his book “The triple helix”, Richard Lewontin (2000) argues that while we can learn a lot about an organism from the analysis of its genomic sequence, our ability to predict what the phenotype of an organism will be based solely on this knowledge is very limited, because phenotypes emerge from the interaction between genes and the environment, which itself is greatly influenced by the organism. With sequencing capabilities that have exploded in the recent years, one would have hoped that the complexity of genotype-to-phenotype mapping would be reduced. However, the major issues pointed by Lewontin are even more critical at this point in time and understanding the role of the environment on the genome in shaping phenotypic variation is all the more important. One type of phenotypic variation that is particularly challenging to grasp is the result of phenotypic plasticity.

1 Recent Advances in Ecological Genomics: From Phenotypic Plasticity to Convergent. . .

Phenotypic plasticity is the ability of a genotype (genomic sequence) to give rise to different phenotypes in different environmental conditions. While for a long time phenotypic plasticity has been studied under statistical terms in quantitative genetics (Stearns 1992), the emergence of genomics approaches in the recent past has allowed to directly probe what the genomics programs of alternative phenotypes are (Aubin-Horth and Renn 2009). In Chap. 5, Matthew Morris and Sean Rogers provide a broad overview of phenotypic plasticity, focusing on its evolution in terms of adaptation and maladaptation and in turn on its impact on evolutionary processes, especially in novel environments and in link with speciation. Morris and Rogers discuss how ecological genomics allow to study these questions further and in novel ways and how the genomic architecture of plastic phenotypes will eventually be uncovered using new approaches. In Chap. 6, Ehab Abouheif and colleagues present the state of the emerging field of eco-evo-devo, which combines the study of development of an organism with the measurement of the environmental factors that affect it and of its evolution. Abouheif and colleagues present several examples of recent advances and outstanding questions about the evolution of development in an ecological context and how the framework of ecological genomics has recently allowed this field to move in giant steps. In Chap. 7, Armin Moczek and colleagues present a model system with ideal characteristics to dissect the genomic mechanisms underlying developmental plasticity of morphology among individuals, among populations and among species: the horned beetles. The presence of a horn has evolved independently in several groups of insects, and in many species, some males of the same population develop a horn while others do not, as a result of developmental plasticity. Moczek et al. present how understanding the molecular pathways that underlie horn development is central to understanding the evolution of plasticity in this trait. They also propose a statistical approach to test the effects of several factors of interest on gene expression,

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allowing to test hypotheses with ecological genomics data in the most efficient way. While several studies such as the ones featuring horned beetles have focused on plasticity in morphology, it has also been recently recognized that plasticity in behavior, resulting both from the environment encountered during development and in adult individuals, can play a major role in the success of organisms in variable abiotic and biotic conditions (Aubin-Horth and Renn 2009). Rayna Harris and Hans Hofmann (Chap. 8) present the state of the field of neurogenomics, which aims, among other things, at understanding the molecular mechanisms underlying behavioral plasticity. Harris and Hofmann review the different temporal scales at which this plasticity can be studied from a genomics perspective. They also give an overview of the wide array of systems that have been studied, from bees to fish, birds and mammals, and of the diversity of behaviors, showing the power of a comparative approach in ecological genomics. Finally, they also advocate the use of reverse genomics to complement the most current approach of going from a phenotype to the molecular level. One of the environmental conditions that can widely affect an individual’s phenotype is the presence of parasites. A fascinating effects of infection by parasites is the alteration of its host’s behavior, often resulting in a higher success rate of transmission to the parasite’s final host where it can reproduce. This plastic change in behavior has been proposed to be an adaptation of the parasite, although this is still an unsettled debate (Poulin 2010). In Chap. 9, François-Olivier Hébert and Nadia Aubin-Horth argue that in order to determine if a parasite actively manipulates its host behavior or, alternatively, if this behavior alteration is merely a “side-effect” of the infection, it is essential to uncover the mechanistic basis of how parasites and their hosts’ genomes interact. They propose that diverse molecular mechanisms could be involved, and that the study of less well known levels of biological organization, such as the interactome, the phosphorylome and the microRNAome, in both the host and the parasite, and an integrative view of the

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“altered phenotype” in the host will lead to a better understanding of this genome-genome interaction. The final chapter of this part of the book investigates what is thought to be an important mechanism underlying plasticity: epigenetics. Kilvitis and colleagues (Chap. 10) discuss how epigenetic modifications of the genome can affect ecologically important traits such as floral or growth traits and potentially the success of individuals facing different environmental conditions. They also discuss how the use of molecular approaches transferred to ecologically and evolutionary model species is gaining ground and will help understand this new layer of complexity in the determination of phenotypic variation. In the third part of the book are contributions to the field of the study of adaptation and speciation. The genomic mechanisms of speciation and adaptation are central to ecological genomics (Pavey et al. 2012), since among the major challenges of the field is the identification of the genes and gene networks involved in these processes. One of the evidence to support evolution by natural selection is the evolution of the same phenotype repeatedly in similar environments (Arendt and Reznick 2008). While there are documented cases of repeated adaptation in the wild, we still have a poor understanding of the likelihood of repeated adaptations to occur and whether they result from similar selective forces or from the fact that there are only a limited number of genetic solutions to any required adaptation. In Chap. 11, Achaz and colleagues examine models dealing with evolutionary convergence and provide examples from the literature where adaptive landscapes have been exhaustively dissected. They demonstrate how experimental evolution allows to strictly control the genotypes studied. Their work has broad impact as they conclude on the need to consider different types of convergent evolution and to integrate them, for instance convergent evolution at the gene level or at the phenotypic level. In addition, they illustrate how experimental evolution, i.e., where the ecology of a population is strictly controlled, can inform us on the genomics bases of adaptive evolution. The issues of convergent evolution at the molecular level are also very important in natural contexts,

C.R. Landry and N. Aubin-Horth

as these issues are central to Chaps. 2, 13, 16, and 17, confirming that this aspect of adaptation is a major question in ecological genomics (Pavey et al. 2012). The genomics study of adaptive divergence offers remarkable insights into the molecular mechanisms underlying adaptive changes. One spectacular example comes from the adaptation of Drosophila to different host plants. In Chap. 12, Luciano Matzkin examines the genomics changes that accompany shifts in host cacti species by Drosophila mojavensis. Among the challenges these shifts pose are different nutritional composition and toxic compounds. Matzkin shows how the combination of genomics tools has allowed to point towards the molecular pathways involved in these host shifts. The Drosophila example offers an excellent illustration of how metabolic changes accompany adaptive evolution. Adaptive evolution can also be driven by morphological and color changes. One of the best model systems to study adaptive radiation are Heliconius butterflies, which builds on several decades of ecological and behavioral observations. In Chap. 13, Megan Supple and colleagues review the recent work in the genomics of speciation in this rich group of species by highlighting studies connecting phenotypes to genotypes and the role of introgression in adaptation. Another excellent model for the study of speciation and adaptation are species of the genus that comprise tomatoes and chili. This group presents a large diversity of floral variation and divergence in addition of representing a group of species of economic interest. In Chap. 14, David Haak and colleagues present new avenues for the dissection of adaptive evolution and speciation in this clade. They discuss how reproductive traits should be jointly studied in terms of adaptation and speciation, as those are key determinants of fitness. They also identify crucial environmental factors driving adaptive evolution in these species and discuss how genomics approaches will allow to identify the genes involved. In Chap. 15, Jun Kitano and colleagues emphasize the central role of hormonal systems in the regulation of the development of adaptive

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traits. They show how the field of evolutionary endocrinology studies the architecture of hormonal signaling pathways, the role of hormones in integrating external and internal signals, in leading to the observed phenotype and to the presence of correlation between traits, as well as how all these are modified during evolution. They also show how the study of the wide-ranging effects of hormone systems is especially improved by large-scale approaches of ecological genomics. In Chap. 16, Andrew Whitehead presents how the rapid changes imposed by human-altered environments are affecting the evolution of traits. The field of evolutionary ecotoxicogenomics is moving fast and Whitehead presents how the large-scale data obtained using ecological genomics approaches is revealing the genomic architecture of the multidimensional phenotypes that evolve to enable individuals to face pollution. Finally, in Chap. 17, Jesse Shapiro presents approaches to survey and understand microbial genome diversity and the evolutionary forces shaping it. He presents how ecological speciation is central in bacteria and how ecological genomics approaches can be used to test hypotheses about the genomics of adaptation in microbes, their ecological functions and the importance of evolutionary convergence. One the most exciting presentation of the 2003 first “Evolutionary and Ecological Functional Genomics” Gordon conference was that of Leroy Hood, director of the Institute for Systems Biology in Seattle. Hood introduced the audience to the then burgeoning field of Systems Biology and to how cellular circuitry could be analyzed and modeled in a comprehensive manner by the precise measurement of molecules and their interactions in the cell. Once again, one needed a fertile imagination to envision how these approaches could be extended to non-model

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species and thus serve to understand how ecological factors are shaping gene and protein networks. However, readers of this book will realize that the field is poised for such integrative approaches in ecological genomics and that the field is moving from a description of how genes are affected by environmental factors in the short (physiological) and long terms (evolutionary) to a better understanding of how the relationships among these genes and their products are also changing. Once again, the field is ready for harnessing the most powerful approaches of the life sciences in order to address the most challenging questions in ecology and evolution.

References Arendt J, Reznick D (2008) Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol Evol 23:26–32 Aubin-Horth N, Renn SC (2009) Genomic reaction norms: using integrative biology to understand molecular mechanisms of phenotypic plasticity. Mol Ecol 18(18):3763–3780 Feder ME, Mitchell-Olds T (2003) Evolutionary and ecological functional genomics. Nat Rev Genet 4(8):651–657 Landry CR, Townsend JP, Hartl DL, Cavalieri D (2006) Ecological and evolutionary genomics of Saccharomyces cerevisiae. Mol Ecol 15(3):575–591 Lewontin RC (2000) The triple helix: gene, organism, and environment. Harvard University Press, Cambridge Pavey SA, Bernatchez L, Aubin-Horth N, Landry CR (2012) What is needed for next-generation ecological and evolutionary genomics? Trends Ecol Evol 27(12):673–678 Poulin R (2010) Parasite manipulation of host behavior: An update and frequently asked questions. In: Brockmann J (ed) Advances in the study of behavior. Elsevier, Burlington, pp 151–186 Stearns SC (1992) The evolution of life histories. Oxford University Press, London, 249p